mycorrhizae experiment

A Way To Garden

'horticultural how-to and woo-woo' | margaret roach, head gardener

feed the soil: my experiment with mycorrhizae

mycorrhizae illustration copyright Bio-Organics

The tipping point had been meeting Graham and Layla Phillips, who had recently taken over Bio-Organics , founded in 1996 and one of the first companies to commercialize mycorrhizal agricultural products (disclosure: they have advertised on A Way to Garden). We got to talking, and I pestered them with my usual endless questions–and then bought myself that jar of a blend of viable beneficial organisms from their online store.

I didn’t just take their word for how it all worked, however; I dug deeper. Extensive Texas A&M research over more than 25 years reports that the benefits of mycorrhizae include plants that are more vigorous, with increased drought and disease resistance and the ability take up more nutrients and water. They may also need less pesticides because of their overall better response to stress. (Mycorrhizae have even been used by Aggie researchers on Texas lignite coal-industry land to try to revitalize it after mining, but I’m hoping your garden isn’t in that condition!)

Even deeper background: Mycorrhizae weren’t “invented,” not by Bio-Organics or Texas A&M any other current commercial producer or research institution. They’re a group of naturally occurring soil organisms, one or more species of which most plants depend on to thrive (different plants, different preferred species). The interaction is mutualistic, not just one-way: The fungi use the Carbon produced by the plants to support their own functions, in turn helping the plant to reach farther into the soil by creating an extensive network or web of fungal filaments–they look like root hairs–called hyphae.

When I first read about using mycorrhizae, it all sounded a little like pre-treating beans and peas with Nitrogen-fixing inoculant, or taking probiotics for a healthy gut—you know, natural, or holistic. But of course those examples are uses of friendly bacteria, not fungi like the mycorrhizae. (And you know how I’m fascinated by the power of fungi .)

Much of the commerce in mycorrhizae to date has been geared to agriculture and the nursery industry. Grapes, for instance, are very dependent on mycorrhizae (as are roses, for another example), so vineyards are one industry that extolls their virtues. Spurred by Texas A&M findings, wholesale nurseries, including giants like Monrovia , have begun inoculating their potting soils, seeking potential benefits such as reduced transplant issues and faster establishment.

Such industries hadn’t initially come to mycorrhizae seeking a ”save the earth” solution, says Graham (read more about the Wharton law-and-business graduate in this “Philadelphia Inquirer” story ), but rather a better economic equation in crop production. For instance, they may harvest at a younger age (as with the grapes), or reduce fertilizer costs, or otherwise improve the bottom line.

Now other potential customers—including more gardeners—are coming asking about natural solutions to growing success.

Like me with my curiosity about fine-tuning my soil-feeding mantra. And so when the raised beds here can be worked in a couple of weeks, I’ll continue my experiment with mycorrhizae, by using the rest of my supply.

I’d love to hear if you’ve begun your own experiments with these fascinating microbes and what your experience has been.

mycorrhizae 101, the basics

I ASKED GRAHAM PHILLIPS a few key practical questions about using mycorrhizae, in this short Q&A:

Q. When do I apply mycorrhizae? Do I re-apply every year?

A. Mycorrhizal products are often used by gardeners when sowing seeds, when transplanting, or to inoculate a bed before planting, working them into the top 4-6 inches. Inoculated soils will actually improve year after year, so it’s a sustainable product.

Q. Do I till in coming seasons?

A. We recommend no- or low-till practices, so the network of filaments, or hyphae, can develop and flourish year to year. Keep using your compost.

Q. Do I use fertilizer as well?

A. Many synthetic plant foods, especially fast-acting liquids, harm microbial activity in the soil and create fertilizer-dependent plants, so we don’t recommend using them. We say that the fungi are not an “add-on-” to a chemical-fertilizer routine, but best used “instead of.” We recommend ongoing use of compost, compost tea, cover crops, and if needed, small amounts of dry organic fertilizers that release slowly.

Q. Does mycorrhizae work on all plants?

A. There are a few plants that are said to be non-mycorrhizal, meaning they don’t form the mutualistic relationship with the microbes. These include blueberries and other ericaceous plants such as azaleas; brassicas (cabbage, broccoli, mustard, etc.); spinach and beets.

Q. Where do I store leftover product, or can I?

A. You can store it for two years, preferably in a cool, dry place, but it will last longer. After two years the spores begin to degrade as time passes, but many will remain viable–you would just have to use a little more each subsequent year.

(Top illustration courtesy of Bio-Organics.)

i’m doing a lot of planting this spring and am eager to give this a trial. my concern is that i need to spray one of my beds with copper (some late blight last year), which would seem to destroy the fungi to begin with. any ideas?

I’ve asked Graham from Bio-Organics for some advice on this, Devra. Stay tuned.

I asked Graham and the founder of the company as well, and here’s what they say, Devra:

“We would recommend not spraying the bed but to rely on the natural protection of the mycorrhizal fungi instead. The mycorrhizal fungi will protect her plant roots from harmful fungi (one of the many benefits of introducing “friendly” fungi) and that there should never again be a need to try to kill off soil organisms. It is also very difficult to completely kill all harmful organisms. If she must do it, she would then inoculate afterwards but she could also destroy other helpful organisms in the process of spraying.”

So glad to find this conversation. There have been some articles about caring for the soil food web that have me wishing to know more about the soil microbes and their beneficial functions. The next step would seem to be to get my hands on Lowenthal’s book(s). I will be watching for any followup comments.

Glad you found us, Lillian. So many mysteries to delve into, even in a single shovelful of soil!

Beth asked in an earlier post about striking a balance in till/no till soil care. Digging or tilling in the fall appears to do the most damage to the microbes and critters that have taken up residence in your soil during the growing season. The current thinking seems to be that shallow cultivation of your garden soil in preparation for spring planting is the most beneficial for the soil and the gardener alike.

If your soil tends to become compacted, using a spading fork or broad fork to punch holes deeply into the soil works well to help get beneficial materials, air , and water to deeper levels This in turn encourages deeper rooting of your plants.

We have a lot of clay in our garden soil, so when I prepare the beds I use a broad fork to punch holes , then rock back just a few inches before removing the tines from the soil. I do this at 6 to 8 inch intervals throughout the beds. Do not lift and turn the soil. As you add amendments some falls to the bottom of the holes, and as the season wears on, water and your microherd carries more goodies downward improving porosity and structure in the proess.

This is just the advice I was after. I have a very reactive black clay soil and am looking for a way to improve the soil, without the “till” damage. What might you suggest for 5 acres of soil needing improving.? Thanks again. Paul

Get you some mycor plus from agusa or listen to Elaine Ingham microbiologist on utube u will get awesome soil results

I have an abundance of the fungi in my garden. I know this because I was concerned when I thought I had veins of mold where I grew my veggies. I took a sample of it in to WSU extension office (Washington State University) and they said it was good fungi. I have a TON of it, and I noticed lots in my compost pile that sat during the winter. My question is….Can there be too much mycorrhizae in the soil? Can this be harmful to breath in while working in the soil?

Hi, Marje. I don’t know (and think it was smart to ask WSU — good for you), but here’s my non-scientist approach to answering:

When I see too much of anything like that happening in the heap — a spot that’s too dry, too wet/slippery, anything that’s getting smelly, or fungi as you describe, I think it’s time to turn things and mix up the blend of ingredients. I believe that fungi are specific to particular materials (they develop on and break down one thing or another — not necessarily everything), so I have mostly had this happen when I got a load of wood chips, for instance, that were all one material…or a load of mulch that was too damp or I applied to thickly (or in a wet season). So I’d turn things to get air in there, add more “green” materials, and not worry.

Thank you for the good info. I intend to try the m. fungi on my Dahlias this year to get better show blooms. Wondering why some plants are more mutualistic than others?

I never heard an update on your experience? Are you still using Mycorrhizae? BTW, I loved you show today on weed ridding!

Thanks Scott re: the show. I’m not sure if there was any perceptible difference — but hmmm, hard to tell I bet, right? I guess I would have to do before/after soil analysis.

Do you ever make it up to the Common Ground Fair? Two years ago I attended a talk about a no till method that is used in Korea. It was fascinating. The mycellium was captured in a box of white rice that was in the wooded part of the property. When one found the Mycellium it would then be used to inoculate a bed that had been solarized. A top layer of mulch would then be used to keep weeds down and feed that mycellium. The farmer giving the talk had stopped using tractors- which is startling when one is talking about acres of crops. He has a higher yiels and it costs less to produce. I bought the book Mycelium Running because I was told it describes how to do this & it will be how I tackle my acre plus plantings this year.

I have the book, too — so interesting! Thanks for saying hello. Some year I must go to the fair in Maine.

where can i buy Bio-Organic products here in Massachusetts ?

Hi, Robert. I believe they sell it mail order via their website , or you can use the contact link there to ask them.

Can you apply mycorrhizae to the lawn with a hose end sprayer?

Hi, Marty. Yes, many versions can be applied that way. Normally each product gives instructions for dilution depending on application method, including that one.

We live on the edge of a river, where we have an long-established “swamp maple”. The tree is doing poorly. It seems to have responded positively to the rotted manure we spread beneath it mid-summer, but we are wondering if mycorrhizae can be part of the help this beautiful tree needs, and how/when to best get the fungi where it can help the tree. Thanks, C&M

What are your thoughts on native vs nonnative mycorrhizae? Could the commercialization of mycorrhizae be introducing invasive fungi into our soils with unintended consequences? This sort of thing has happened before in the nursery world.

I don’t know, Tyler. I did that interview above 10 years ago, and haven’t since that first exploration used any products. Thanks for reminding me of a topic worth investigating.

How do mycorrhizae work?

Have you ever had to work in a garden, or even just grow a single plant? If so, you know it’s hard work—you have to carefully cultivate growth by keeping the weeds at bay and providing the plant with plenty of water and sunshine. At the end, you’re rewarded with an abundance of healthy nutrients in the form of delicious, fresh vegetables or a view of beautiful flowers. But did you know that many plants have their own gardens too? Unlike our gardens, though, the plant’s gardens are entirely underground, and normally you’d never see them except for a brief period each year. They’re called mycorrhizae (my-coh-rise-eh), and they live in a symbiotic relationship with the plant itself.

What are mycorrhizae?

Mycorrhizae are actually a fungus . They exist as very tiny, almost or even entirely microscopic, threads called hyphae . The hyphae are all interconnected into a net-like web called a mycelium , which measures hundreds or thousands of miles—all packed into a tiny area around the plant.

The mycelium of a single mycorrhiza (note: mycorrhizae is plural), in turn, can extend outward, connect multiple plants (even plants of different species!), and even connect with other mycorrhizae to form a Frankenstein-like underground mash-up called a common mycorrhizal network .

In a common mycorrhizal network, it’s hard to tell where one mycorrhiza ends and another begins. Because of this vast network, a single plant can be connected to a completely different species of plant halfway across a forest!

Mycorrhizae actually connect to plants in two ways. One form, called ectomycorrhizae , simply surrounds the outside of the roots. Another form, called endomycorrhizae , actually grows inside of the plant—their hyphae squeeze in between the cell wall and the cell membranes of the roots (sort of like wedging themselves in between a bicycle tire and the inner tube).

Under normal conditions, you’re not likely to see mycorrhizae because they’re so small. But every once in a while, something amazing happens: the mycorrhizae will reproduce and send up fruiting bodies that produce spores—we call them mushrooms! Some of these mushrooms are even edible, like truffles or chanterelles.

How do plants help mycorrhizae?

Plants make great gardeners. Just like we fertilize our gardens, plants feed their own mycorrhizae. Plants will take excess sugar produced in the leaves through photosynthesis and send it to the roots. From here, the mycorrhizae are able to absorb it to sustain themselves. There is very little sunlight underground, and even if there was, the mycorrhizae wouldn’t be able to harvest it like plants because they don’t have the equipment needed for photosynthesis. The sugar from the plants literally keeps the mycorrhizae fed and alive.

How do mycorrhizae help plants?

Plants don’t give up their valuable sugar resources just for the fun of growing fungus gardens. They get a lot of things in return from the mycorrhizae, mostly in the form of nutrients.

Plants are able to get nutrients themselves through their roots, but they have a limited ability to do so. Their roots need to be in direct contact with the soil to absorb the nutrients, and plant roots only grow so small. Fungi, on the other hand, can get much smaller. Fungal hyphae can wedge in between individual bits of soil to cover almost every available cubic millimeter of soil. This increases surface area and allows the plants much greater access to nutrients than they could get by themselves. For many plants living under difficult conditions, they wouldn’t be able to survive at all without mycorrhizae.

The mycorrhizae absorb nutrients such as phosphorus and magnesium and bring it directly to the plant roots. Here, they exchange the nutrients they’ve collected for some sugar. It’s a fair trade, and both sides benefit.

Additionally, the mycorrhizae help plants out in a whole bunch of other ways. Mycorrhizae can help protect their plants against diseases and toxins. Mycorrhizae can also serve as a sugar delivery service when plants shuttle sugar back and forth to different plants connected to the same common mycorrhizal network. Perhaps most bizarrely of all, the common mycorrhizal network can also serve as a means for plants to “talk ” to each other—an Internet made out of fungus!

Putting It All Together

Mycorrhizae form an invaluable part of ecosystems around the world, and can be found in some form or another in just about any ecosystem. In many places, whole forests and ecosystems wouldn’t exist at all without their mycorrhizal friends.

The next time you’re walking in a forest and you see a mushroom growing out of the ground, be thankful and remember that there’s a whole world buzzing along beneath your feet.

Ecology-boo

Aposematism, Müllerian Mimicry, and Batesian Mimicry
Basics of Symbiosis
Competition
Ecology Articles
Mycorrhizae
Predation and Herbivory
Rainforest Conservation
Types of Deep Sleep in Animals: Torpor, Hibernation, Estivation and Brumation

Science Newsletter:

Full list of our videos.

Teaching Biology?

How to Make Science Films

Read our Wildlife Guide

New From Untamed Science

An official website of the United States government

The .gov means it’s official. Federal government websites often end in .gov or .mil. Before sharing sensitive information, make sure you’re on a federal government site.

The site is secure. The https:// ensures that you are connecting to the official website and that any information you provide is encrypted and transmitted securely.

Publications
Account settings

Preview improvements coming to the PMC website in October 2024. Learn More or Try it out now .

Advanced Search
Journal List
v.10(5); 2020 May

Mycorrhiza: a natural resource assists plant growth under varied soil conditions

Chew jia huey.

1 School of Bioprocess Engineering, Universiti Malaysia Perlis, 02600 Arau, Perlis Malaysia

Subash C. B. Gopinath

2 Institute of Nano Electronic Engineering, Universiti Malaysia Perlis, 01000 Kangar, Perlis Malaysia

M. N. A. Uda

Hanna ilyani zulhaimi, mahmad nor jaafar, farizul hafiz kasim.

3 Centre of Excellence for Biomass Utilization, School of Bioprocess Engineering, Universiti Malaysia Perlis, 02600 Arau, Perlis Malaysia

Ahmad Radi Wan Yaakub

In this overview, the authors have discussed the potential advantages of the association between mycorrhizae and plants, their mutual accelerated growth under favorable conditions and their role in nutrient supply. In addition, methods for isolating mycorrhizae are described and spore morphologies and their adaptation to various conditions are outlined. Further, the significant participation of controlled greenhouses and other supported physiological environments in propagating mycorrhizae is detailed. The reviewed information supports the lack of host- and niche-specificity by arbuscular mycorrhizae, indicating that these fungi are suitable for use in a wide range of ecological conditions and with propagules for direct reintroduction. Regarding their prospective uses, the extensive growth of endomycorrhizal fungi suggests it is suited for poor-quality and low-fertility soils.

Introduction

Recently, the looming food security problem has highlighted plant science as an emerging discipline and led to a commitment to devising new strategies to enhance crop productivity. Biotic and abiotic stresses, such as drought, salinity, flooding, plant pathogens, nutrient deficiency and toxicity, which limit global crop productivity, are reasons for food scarcity. Given the potential for food shortages, strategies should be adopted to achieve maximum productivity and economic crop returns (Ahmad et al. 2012 ). The application of fertilizer is one of the methods used to obtain optimum yields, although this may cause environmental issues. If chemical fertilizers are applied continuously, they may lead to the deterioration of soil characteristics and fertility, and heavy metals can accumulate in plant tissues; eventually, the nutrition value and edibility of fruits will be affected (Mosa et al. 2014 ). Instead of using chemical fertilizers, biological fertilizers, such as animal manure, the decaying remains of organic matter, domestic sewage, excess crops and microorganisms (e.g., bacteria and fungi), can be used as a more sustainable alternative. Furthermore, plant growth can be improved through microbial inoculation, including inoculation with plant growth promoting rhizobacteria (PGPR) and mycorrhizal fungi. These microbes play significant roles in the promotion of plant growth through the regulation of nutrition and hormonal balances, production of plant growth regulators, solubilization of nutrients and induction of resistance against plant pathogens. In addition, plant interactions with these microbes have shown synergistic as well as antagonistic interactions with other microbes in the rhizosphere. These interactions are important for sustainable agriculture because they maintain plant growth and development through biological processes rather than through agrochemicals.

Moreover, mycorrhizae can be found in all the soils where plants can grow, and these fungi facilitate the absorption of water and nutrients by plants. Plants send sugars from their leaves to fungi as food. Further, root surface area can be increased by mycorrhizae, allowing plants to uptake water and nutrients more efficiently from a large soil volume (Nadeem et al. 2014 ). In addition, it has been shown that different mycorrhizal species exhibit a variety of responses depending on the plant species with which they are associated (Ortas and Ustuner 2014 ). This is because there is a wide range of mycorrhizal fungal species that could change the strength of plant-plant interactions, and plant growth will vary. It is widely accepted that there are higher growth rates in plants inoculated with mycorrhizae than in control plants because of the increase in photosynthetic activities. Mycorrhizae also play an important role in the supply of essential nutrients to their associated plant; interestingly, fungicides or herbicides will not affect the growth of mycorrhizae.

Glomeromycota, referred to as arbuscular mycorrhizal fungi, are one of the most significant fungi because they form mutualistic relationships with the roots of almost 90% of plant species (Stajich et al. 2009 ). Arbuscular mycorrhizae can be seen in the belowground parts of the earliest plant fossils and facilitate nutrient acquisition by plants in exchange for photosynthate. They are also vital to plant fitness and may determine the compositions of plant communities. Arbuscular mycorrhizae are hyphal and produce highly branched haustoria, which promotes nutrient exchange with their host root cells.

Mycorrhizal fungi

According to the definition by Brundrett in 2002 , mutualistic relationships are formed between the modified absorptive organs of mycorrhizae, which mainly consist of plant roots (photobiont) and fungal hyphae (mycobiont). The main purpose of this relationship is to transfer nutrients between the organisms (Brundrett 2002 ). Mycorrhizal symbiosis plays an important role in ecosystems because mycorrhizae affect plant productivity and plant diversity. Usually, plant productivity is improved by mycorrhizal interactions, but this is not always the case; under different environmental conditions, symbiosis can span various species interactions, from mutualism to parasitism (Maherali 2014 ). Mycorrhizal fungi can even have parasitic interactions with plants when the net benefits of the symbiosis are lower than the net cost. Mycorrhizal associations are complex; thus, an understanding of the several parameters affecting the function of mycorrhizae, such as the morphology and physiology of both symbionts and biotic and abiotic factors at the rhizosphere, community and ecosystem levels, is required. In the commercial production of infected plants, several species of fungi are used, and seedling inoculation with either spores or mycelial cultures is usually the starting point (Grimm et al. 2005 ).

Information on fungi

Fungi are macroscopic and microscopic organisms, such as mushrooms, truffles, puffballs, and glomeromycetes (soil fungi that connect to roots); they are totally separate from the cell walls of plants and are capable of secreting a range of enzymes (Anbu et al. 2004 , 2005 , 2007 ; Gopinath et al. 2002 , 2003 , 2005 ; Kumarevel et al. 2005 ; Lee et al. 2015 ; Zaragoza 2017 ). Fungi can reproduce by both sexual and asexual reproduction and typically produce spores. Fungi are categorized into taxonomic ranks based mainly on morphologies that are described by their structure and phylogeny. They are further categorized by their genetic differences. However, the procedures to classify fungi according to genetic differences are complicated (Ellison et al. 2014 ; Grimm et al. 2005 ).

To understand fungi and simplify their identification, methods have been developed to isolate fungi, such as the pour plate and dilution-based spread plate techniques and spore isolation (Magnet et al. 2013 ). All isolated fungi must be obtained in pure cultures by using a standard technique (Rohilla and Salar 2011 ). Additionally, caution must be taken when performing isolation to avoid cross-contamination, which would significantly affect the final isolation results. Among mycorrhizal fungi, various types of spores have been found to occur (Fig. 1 ).

An external file that holds a picture, illustration, etc.
Object name is 13205_2020_2188_Fig1_HTML.jpg

Various shapes and textures of mycorrhizal spores. Different types, which are widely distributed across a range of plants, are displayed

Wet sieving and decanting method

Wet sieving and decanting methods are simple spore isolation techniques introduced by Gerdemann and Nicolson to extract fungal spores from soil samples (Gerdemann and Nicolson 1963 ) (Fig. 2 ). This technique was used for sieving the coarse particles of the soil and retaining the fungal spores and organic particles on sieves of different sizes. Then, the spores are removed and collected for observation under a microscope. There are different types of spore isolation methods, such as the sucrose centrifugation method, adhesion flotation method, and capillary rise method. However, in the study of Shamini and Amutha, wet sieving and decanting methods were shown to obtain a large number of spores (Shamini and Amutha 2015 ).

An external file that holds a picture, illustration, etc.
Object name is 13205_2020_2188_Fig2_HTML.jpg

Representation of wet sieving and decanting methods. The steps involved are shown. Both methods have been used in the past and have advantages for the separation of mycorrhizal spores. Wet sieving captures smaller spores

Analysis of fungal morphology

The analysis of fungal morphology is mainly based on fungal structures and sizes. Most fungi are composed of structures called mycelia (thread-like hyphae) and grow from the tips of fungi, similar to the binary branching of trees. Fungi can be differentiated because of their lack of a hyphal septum. Spores are the main characteristic used to identify the types of fungi. Particular representative fungi must be isolated, and then their morphologies must be observed (Tsuneo watanabe 2002 ). Generally, fungi are observed by using microscopes, such as stereomicroscopes, compound microscopes and scanning electron microscopes. Moreover, advances in image and particle analysis and micromechanical devices have improved morphological data (Krull et al. 2013 ), which means that the structures of microorganisms can be seen more clearly and in greater detail. In addition, the identification of fungi depends not only on morphology but also on fungal cultures, which can be obtained from single spore isolations (Choi et al. 1999 ).

Spore morphology

According to Levetin, the following characteristics can be used to identify fungi: the spore size and shape, the number of cells in the spore, the spore wall thickness, the spore color and surface ornamentation, and the attachment of scars. Compared with the sizes and shapes of spores, the spore wall characteristics are very useful for the identification of fungi. Additionally, spore walls can be smooth or consist of various ornamentations, which usually occur on the outermost surface and appear spore-like spiny, punctate, warted, striated, ridged, or reticulate (Fig. 1 ). Therefore, ornamentation can also be used for identification.

Types of mycorrhizae

Mycorrhizae are divided into two types based on the structure of their hyphae. The fungal hyphae that do not penetrate the individual cells within the roots are known as ectomycorrhizal fungi, while the hyphae of fungi that penetrate the cell wall and invaginate the cell membrane are called endomycorrhizal fungi (Szabo et al. 2014 ). In addition, according to Heijden and Martin, four main types of mycorrhizal fungi have been classified: arbuscular mycorrhizae, ectomycorrhizae, orchid mycorrhizae and ericoid mycorrhizae (van der Heijden et al. 2015 ). Furthermore, endomycorrhizae include the arbuscular, ericoid, and orchid mycorrhizae, while arbutoid mycorrhizae can be classified as ectomycorrhizae and monotropoid mycorrhizae form a special category.

Arbuscular mycorrhizae

Vesicular–arbuscular mycorrhizal fungi (VAM) and soil fungi are alternative terms for arbuscular mycorrhizal fungi (Vogelsang et al. 2004 ). These fungi belong to the Glomeromycota and are believed to have an asexual reproductive strategy. Plants depend heavily on these fungi to reach their optimal growth potential. Arbuscular mycorrhizal symbiosis is the most common non-pathogenic symbiosis in the soil and is found in 80% of vascular plant roots (Brundrett 2002 ). Additionally, arbuscular mycorrhizae only grow in association with appropriate host plants and plant species and vary by host. Arbuscules are fungal structures growing into individual plant cells (Fig. 3 ). Arbuscular mycorrhizal (AM) fungi can be found within almost all phyla in the Angiosperms (Duhoux et al. 2001 ). According to Miranda and Jennifer, AM fungi not only improve phosphorus nutrition to plants but also enhance the uptake of zinc, copper, nitrogen and iron (Hart and Forsythe 2012 ). They are also resistant to some root diseases and drought tolerant.

An external file that holds a picture, illustration, etc.
Object name is 13205_2020_2188_Fig3_HTML.jpg

Growth pattern of arbuscular mycorrhizae. The formation of vesicles is shown. Arbuscular mycorrhizae are widely reported and commonly used. This is mainly due to their attraction to phosphorous sources. The arbuscules form a vesicle

Ectomycorrhizae (EM)

Ectomycorrhizae are a large group (Szabo et al. 2014 ) with a widespread distribution but only 3–4% of the vascular plant families are associated with these fungi (Brundrett 2004 ). Chiefly, EM are members of the phyla Ascomycota and Basidiomycota, and EM mutualism is thought to be independently derived multiple times from saprophytic lineages (Merckx 2012 ). Plant species that form EM mutualisms have been shown to have antimicrobial components that protect the plants from root pathogens. These fungi are characterized by their growth on the exterior surfaces of roots (Schnepf et al. 2008 ). Thus, roots are covered by fungal tissue, and the covering is known as a hyphal mantle (Fig. 4 ). Strands of mycelium, the fungal filaments, extend from the hyphal mantle into the soil and act as the roots of the plant, absorbing minerals and nutrients.

An external file that holds a picture, illustration, etc.
Object name is 13205_2020_2188_Fig4_HTML.jpg

The growth pattern of endomycorrhizae. The structure of endomycorrhizae is different from that of ectomycorrhizae

Formation of mycorrhizae

Arbuscular mycorrhizal fungi go through several developmental stages in the formation of mycorrhizae (Fig. 5 ). During the symbiotic stage, spores are germinated and limited hyphal development by arbuscular mycorrhizal fungi has been found due to the absence of host plants. However, after germination, the spores enter the presymbiotic stage, which is characterized by extensive hyphal branching when root exudates are present (Kuo et al. 2014 ) . In addition, appressoria are formed once the fungus contacts a root surface and before the hyphae penetrate the root epidermis. This is followed by the symbiotic colonization of the root cortex tissue, which involves the formation of intracellular arbuscules (tree-like, heavily branched structures) or hyphal coils, and concomitantly, the production of a unique extraradical mycelium occurs. Host plants play a primary role in orchestrating the arbuscular mycorrhizal infection process, and it is tempting to speculate that similar changes occur during the colonization of the cortical cells. Overall, these developmental processes require molecular communication between the arbuscular mycorrhizae and the plant, including the exchange and perception of signals by the symbiotic partners.

An external file that holds a picture, illustration, etc.
Object name is 13205_2020_2188_Fig5_HTML.jpg

Developmental stages of arbuscular mycorrhizae. The different stages are indicated. Generally, six stages are involved in the formation of a complete association

Mycorrhizal plant interactions

There are two nutrient uptake pathways for roots colonized by mycorrhizae: the plant uptake pathway (PP) and the mycorrhizal uptake pathway (MP) (Fig. 6 ). The PP involves the uptake of nutrients directly through the transporter and occurs in the root epidermis and root hairs. In the MP, nutrients are indirectly transferred via fungal transporters in the extraradical mycelium (ERM) of the fungus and transported to the hartig net in EM interactions or to the intraradical mycelium (IRM) in arbuscular mycorrhizal interactions (shown in the mycorrhizal interface). The uptake by mycorrhiza-inducible plant transporters occurs in the periarbuscular membrane from the interfacial apoplast. The displayed fungal structures indicate the colonization of one host root by multiple fungal species, which can differ in their efficiency. Through these processes, the fungi are able to obtain nutrients from the soil and transfer these nutrients to their hosts (Bucking et al. 2012 ).

An external file that holds a picture, illustration, etc.
Object name is 13205_2020_2188_Fig6_HTML.jpg

Nutrient uptake pathways. The involvement of the plant uptake pathway and mycorrhizal uptake pathway is shown. The major nutrients are indicated, and the directions of the movements are displayed

The rapid uptake of nutrients, for example, ‘P’, by roots leads to the formation of a depletion zone, and fungal hyphae extend beyond the depletion zones to penetrate and exploit a larger volume of soil to uptake nutrients. From the uptake by the hyphae, nutrients are translocated within the hyphal network to the fungal sheath, intercellularly to the hartig net and with the exception of ectomycorrhizae and monotropoid mycorrhizae, intracellularly into plant cells. The fungal sheath is able to store nutrients, supporting the fungi by continuing to provide nutrients to the plant host when the soil nutrient levels decrease. When receiving extra nutrients, mycorrhizal plants lose between 10 and 20% of the photosynthates they produce; these photosynthates are used by the mycorrhizal fungi and their associated structures for development, maintenance and operation.

Nutrients are moved by the fungal ERM via P i , NO 3 − or NH 4 + transporters (blue); ‘N’ is assimilated into Arg through the anabolic arm of the urea cycle (this is shown only for arbuscular mycorrhizae); and P i is converted into polyP in the ERM. The polyP is then transported from the ERM to the IRM. The polyP is hydrolyzed and Arg and P i are released in the IRM. Arg breaks down to NH 4 + in the catabolic arm of the urea cycle (this is shown only for arbuscular mycorrhizae). This process is facilitated by P i , NH 4 + , and potential amino acid (AA, possibly only in the EM) efflux through the fungal plasma membrane (red) into the interfacial apoplast. The nutrients are taken up by the plant from the mycorrhizal interface through mycorrhiza-inducible P i or NH 4 + transporters. Photosynthesis is stimulated by the improved nutrient supply and is facilitated by the efflux of sucrose through the plant plasma membrane into the interfacial apoplast, sucrose hydrolysis in the interfacial apoplast via an apoplastic plant invertase, and the uptake of hexoses by the mycorrhizal fungi through the fungal monosaccharide transporters.

Phosphate uptake

Mycorrhizal symbioses are recognized for their importance in plant nutrition and ionic transport, particularly in phosphorus uptake (Fig. 7 ). To maintain crop yields, modern agricultural systems are highly dependent on the continual inputs of phosphate-based fertilizers. These fertilizers are processed from phosphate rock, which is a non-renewable natural resource. Therefore, the world could soon face a resource scarcity crisis that might affect global food security. Arbuscular mycorrhizae form a symbiosis with the roots of nearly all vascular plants and could play a key role in solving the phosphate shortage problem. Additionally, by improving the efficiency of nutrient uptake and by increasing plant resistance to pathogens and abiotic stresses, mycorrhizal symbiosis can enhance plant growth and therefore reduce the need for phosphate-based fertilizers. Herein, we provide an update of recent findings and reports on mycorrhizae as the cornerstone of a "second green revolution" and the types of mycorrhizae that enhance plant growth. Different types of mycorrhizae may be obtained from different plant growth materials.

An external file that holds a picture, illustration, etc.
Object name is 13205_2020_2188_Fig7_HTML.jpg

Transport mechanisms in arbuscular and ectomycorrhizal interactions. The transports in the plants and soils are shown. The molecules and ions generally involved in transport are displayed

Plant growth under physiological conditions

Numerous parameters can be used to measure plant growth. The most common and simple measurements are the number of leaves, plant height, and plant color. These parameters may be seen by the naked eye or using tools for daily measurement. Most farmers evaluate the changes in these parameters to assess the growth of their plants because they are easy to observe. In addition, some complicated parameters, such as leaf dry matter content, stem specific density, and the pH of green leaves, can be used to evaluate plant growth (Pérez-Harguindeguy et al. 2013 ). The use of these parameters requires specific formulas and calculations.

Plant growth under greenhouse conditions

Plants are protected from adverse conditions and growers are able to control growth conditions when plants are grown in greenhouses (Fig. 8 a). A high yield, good quality, uniformity, and precise timing of delivery can be achieved with good control. A variety of crops are grown in greenhouses, the products of which include leaves, roots, bulbs, tubers, flowers, fruits, seeds, young plants, and mature plants (herbs, salad plants, bedding plants, potted plants, and garden plants). Technology is required to control the growing conditions in greenhouses, primarily for heating and venting and optionally for root-zone heating, cooling, fogging, misting, CO 2 enrichment, shading, assimilation light, day-length extension and black-out timing. Light, temperature, and humidity are three growth factors that have been identified (Nederhoff 2007 ). These factors influence plant growth and can be controlled in greenhouses.

An external file that holds a picture, illustration, etc.
Object name is 13205_2020_2188_Fig8_HTML.jpg

a Mycorrhizal-associated plants grown in a greenhouse. (i) groundnut; (ii) onion; and (iii) chickpea. b Classifying symbiotic interactions. The classes include mutualism, parasitism, and commensalism. The mutualistic plant-fungus interaction is the midpoint of the continuum of interactions and the exploitation of a plant by a mycorrhizal fungus is the endpoint

Study lines with greenhouses

Greenhouse technology is used for sustainable crop production in regions with adverse climatic conditions. High summer temperatures are a major issue for successful greenhouse crop production throughout the year (Kumar et al. 2009 ). Greenhouse technology refers to the production of plants for economic use in a covered structure, which allows the rapid harvesting of solar radiation and the modification of agroclimatic conditions conducive to plant growth and development. This technology embraces infrastructure modeling, selection of plants for adaptation, production economics, agronomic management and commercial potential. Therefore, greenhouse crop productivity is largely independent of outdoor environmental conditions (Reddy 2016 ).

Enhanced mycorrhizal associations under controlled greenhouse conditions

The definition of symbiosis (two or more organisms living together) can be applied to all mycorrhizal associations (Brundrett 2004 ; Crops 2015 ). The term mutualism indicates mutual benefits in associations involving two or more living organisms. In a review by Brundrett, the terms ‘balanced’ and ‘exploitative’ are proposed for mutualistic and non-mutualistic mycorrhizal associations, respectively (Brundrett 2004 ). Most mycorrhizal associations, except mycoheterotrophic associations, are ‘balanced’ mutualistic associations, in which the fungus and plant benefit from the association. Mycoheterotrophic plants have an ‘exploitative’ mycorrhizal association that benefits only the plants. Thus, exploitative associations are symbiotic but are not mutualistic. In the research of Bronstein, it was proposed that rather than classifying symbiotic interactions into distinct categories (e.g., mutualism, parasitism, and commensalism), they should be viewed as dynamic points along a continuum (Merckx 2012 ). The mutualistic plant–fungus interaction is the midpoint, and the exploitation of a plant by a mycorrhizal fungus is the endpoint (Fig. 8 b). In mycoheterotrophic interactions, the mycorrhizal fungi are exploited by the plants to obtain carbon and other nutrients (Merckx 2012 ).

Creating a beneficial environment for endomycorrhizal (VAM) colonies requires a plant to have a symbiotic relationship with a VAM. First, the amount of inorganic phosphorus should be low in the soil solution; mycorrhizae will not grow or colonize roots when the phosphorus level is high. This is because the relationship between plants and fungi evolved to help the plants access low levels of phosphorus in the soil. Mycorrhizae cannot grow or establish when phosphorus levels are above 10 ppm in the soil. The mycorrhizae are not killed; they create an environment in which they do not germinate or grow and are rendered ineffective. When plant roots release sugars and hormones and form an association with mycorrhizal spores, the spores start to germinate. This trigger allows the spores to stay dormant, suspended in the soil, until plants actively grow. Thus, the shelf life of mycorrhizae is typically longer (up to two years) than that of other biological additives. As far as it is known, the typical lime addition rates and moderate pH levels of professional growing medium products do not have a significant positive or negative effect on the growth and colonization of mycorrhizae. Mycorrhizae can be used with other bioproducts. There are other helper bacteria or fungi that are often added to mycorrhizal blends, which stimulate and support the growth of the mycorrhizal colonies. In addition, at the beginning of production, chemical fungicides should be avoided until time has passed to allow root colonization (Miller 2012 ). Although there is a long history of mycorrhizal research, it is still continuing due to the potential of mycorrhizae to benefit humans and society and boost economies (Bauer et al. 2020 ; Quiroga et al. 2020 ; Wulantuya et al. 2020 ).

Prospective uses

In the agricultural field, there are several variables when growing plants outdoors, including weather, watering, fertilization and soil quality. These variables can introduce the potential for greater plant stress and therefore highly benefit from endomycorrhizal fungi. Endomycorrhizae can be incorporated directly into the soil, but if plants are grown in a growth medium, their roots will continue to be colonized even after transplanting into the soil. The benefits are the same as those potentially seen by the grower and include resistance to transplant shock and increased numbers of fruits and flowers. Unlike roots, endomycorrhizal fungi establish quickly in new soil environments. Therefore, they can ease transplant shock by providing water and nutrients for the plant and serve as a buffer to help the plant adjust to its new soil environment. Plants reach their optimum growth rate with endomycorrhizae as a result of reduced stress; therefore, edible plants have the ability and resources to produce more vegetables/fruits and larger vegetables/fruits per plant and flowering plants often produce more flowers. Plants such as beech, willow, birch, pine, fir, oak, and spruce receive many benefits from mycorrhizal associations, and the association of legume and cereal plants with mycorrhizae increases the benefits of these plants to humans. Overall, plants are often larger when grown with endomycorrhizal fungi, especially if plants are grown in poor-quality and low-fertility soils.

Acknowledgements

The author would like to acknowledge the support from Malaysia Fundamental Research Grant Scheme (FRGS) to H.I.Z. (Grant number 9003-00750) and Short Term Grant by Universiti Malaysia Perlis to S.C.B.G. (Grant number 9001-00558).

Author contributions

All the authors contributed to the preparation of the manuscript and discussion. Both authors read and approved the final manuscript.

Compliance with ethical standards

On behalf of all the authors, the corresponding author states that there is no conflict of interest.

Ahmad P, Kumar A, Gupta A, Hu X, Hakeem R, Azooz MM, Sharma S. Crop production for agricultural improvement. Crop Prod Agric Improv. 2012 doi: 10.1007/978-94-007-4116-4. [ CrossRef ] [ Google Scholar ]
Anbu P, Hilda A, Gopinath SCB. Keratinophilic fungi of poultry farm and feather dumping soil in Tamil Nadu, India. Mycopathologia. 2004; 158 :303–309. doi: 10.1007/s11046-004-3465-1. [ PubMed ] [ CrossRef ] [ Google Scholar ]
Anbu P, Gopinath SCB, Hilda A, Lakshmi T, Annadurai G. Purification of keratinase from poultry farm isolate- Scopulariopsis brevicaulis and statistical optimization of enzyme activity. Enzyme Microb Tech. 2005; 36 :639–647. doi: 10.1016/j.enzmictec.2004.07.019. [ CrossRef ] [ Google Scholar ]
Anbu P, Gopinath SCB, Hilda A, Lakshmipriya T, Annadurai G. Optimization of extracellular keratinase production by poultry farm isolate Scopulariopsis brevicaulis . Bioresour Technol. 2007; 98 :1298–1303. doi: 10.1016/j.biortech.2006.05.047. [ PubMed ] [ CrossRef ] [ Google Scholar ]
Bauer JT, Koziol L, Bever JD. Local adaptation of mycorrhizae communities changes plant community composition and increases aboveground productivity. Oecologia. 2020 doi: 10.1007/s00442-020-04598-9. [ PubMed ] [ CrossRef ] [ Google Scholar ]
Brundrett MC. Coevolution of roots and mycorrhizas of land plants. New Phytol. 2002; 154 :275–304. doi: 10.1046/j.1469-8137.2002.00397.x. [ PubMed ] [ CrossRef ] [ Google Scholar ]
Brundrett M. Diversity and classification of mycorrhizal associations. Biol Rev Camb Philos Soc. 2004; 79 :473–495. doi: 10.1017/S1464793103006316. [ PubMed ] [ CrossRef ] [ Google Scholar ]
Bucking H, Liepold E, Ambilwade P (2012) The role of the mycorrhizal symbiosis in nutrient uptake of plants and the regulatory mechanisms underlying these transport processes. World â€ TM s largest Science, Technology and Medicine Open Access book publisher. Intech Open
Choi Y, Hyde KD, Ho WWH. Single spore isolation of fungi. Fungal Divers. 1999; 3 :29–38. [ Google Scholar ]
Crops V. Effect of four mycorrhizal products on Fusarium root rot on different vegetable crops. Plant Pathol Microbiol. 2015; 6 :2–6. doi: 10.4172/2157-7471.1000255. [ CrossRef ] [ Google Scholar ]
Duhoux E, Rinaudo G, Diem HG, Auguy F, Fernandez D, Bogusz D, Franche C, Dommergues Y, Huguenin B. Angiosperm Gymnostoma trees produce root nodules colonized by arbuscular mycorrhizal fungi related to Glomus. New Phytologist. 2001; 149 :115–125. doi: 10.1046/j.1469-8137.2001.00005.x. [ PubMed ] [ CrossRef ] [ Google Scholar ]
Ellison CE, Kowbel D, Glass NL, Taylor JW, Brem RB. Discovering functions of unannotated genes from a transcriptome survey of wild fungal isolates. MBio. 2014; 5 :e01046–e1113. doi: 10.1128/mBio.01046-13. [ PMC free article ] [ PubMed ] [ CrossRef ] [ Google Scholar ]
Gerdemann JW, Nicolson TH. Spores of mycorrhizal Endogone species extracted from soil by wet sieving and decanting. Trans Br Mycol Soc. 1963; 46 :235–244. doi: 10.1016/S0007-1536(63)80079-0. [ CrossRef ] [ Google Scholar ]
Gopinath SCB, Hilda A, Priya TL, Annadurai G. Purification of lipase from Cunninghamella verticillata and optimization of enzyme activity using response surface methodology. World J Microbiol Biotechnol. 2002; 18 :449–458. doi: 10.1023/A:1015579121800. [ CrossRef ] [ Google Scholar ]
Gopinath SCB, Hilda A, Lakshmi Priya T, Annadurai G, Anbu P. Purification of lipase from Geotrichum candidum : conditions optimized for enzyme production using Box-Behnken design. World J Microbiol Biotechnol. 2003; 19 :681–689. doi: 10.1023/A:1025119222925. [ CrossRef ] [ Google Scholar ]
Gopinath SCB, Anbu P, Hilda A. Extracellular enzymatic activity profiles in fungi isolated from oil-rich environments. Mycoscience. 2005; 46 :119–126. doi: 10.1007/s10267-004-0221-9. [ CrossRef ] [ Google Scholar ]
Grimm LH, Kelly S, Krull R, Hempel DC. Morphology and productivity of filamentous fungi. Appl Microbiol Biotechnol. 2005; 69 :375–384. doi: 10.1007/s00253-005-0213-5. [ PubMed ] [ CrossRef ] [ Google Scholar ]
Hart MM, Forsythe JA. Scientia Horticulturae Using arbuscular mycorrhizal fungi to improve the nutrient quality of crops; nutritional benefits in addition to phosphorus. Sci Hortic (Amsterdam) 2012; 148 :206–214. doi: 10.1016/j.scienta.2012.09.018. [ CrossRef ] [ Google Scholar ]
Krull R, Wucherpfennig T, Esfandabadi ME, Walisko R, Melzer G, Hempel DC, Kampen I, Kwade A, Wittmann C. Characterization and control of fungal morphology for improved production performance in biotechnology. J Biotechnol. 2013; 163 :112–123. doi: 10.1016/j.jbiotec.2012.06.024. [ PubMed ] [ CrossRef ] [ Google Scholar ]
Kumarevel TS, Gopinath SCB, Hilda A, Gautham N, Ponnusamy MN. Purification of lipase from Cunninghamella verticillata by stepwise precipitation and optimized conditions for crystallization. World J Microbiol Biotechnol. 2005; 21 :23–26. doi: 10.1007/s11274-004-1005-2. [ CrossRef ] [ Google Scholar ]
Kumar KS, Tiwari KN, Jha MK. Design and technology for greenhouse cooling in tropical and subtropical regions: a review. Energy Build. 2009; 41 :1269–1275. doi: 10.1016/j.enbuild.2009.08.003. [ CrossRef ] [ Google Scholar ]
Kuo A, Kohler A, Martin FM, Grigoriev IV. Expanding genomics of mycorrhizal symbiosis. Front Microbiol. 2014; 5 :1–7. doi: 10.3389/fmicb.2014.00582. [ PMC free article ] [ PubMed ] [ CrossRef ] [ Google Scholar ]
Lee LP, Karbul HM, Citartan M, Gopinath SCB, Lakshmipriya T, Tang TH. Lipase-secreting Bacillus species in an oil-contaminated habitat : promising strains to alleviate oil pollution. BioMed Res Int. 2015; 2015 :820575. [ PMC free article ] [ PubMed ] [ Google Scholar ]
Magnet MH, Sarkar D, Ahmed Z. Samples Of different industry side in Dhaka city, Bangladesh. Int J Innov Res Dev. 2013; 2 :338–339. [ Google Scholar ]
Maherali H. Is there an association between root architecture and mycorrhizal growth response? New Phytol. 2014; 204 :192–200. doi: 10.1111/nph.12927. [ PubMed ] [ CrossRef ] [ Google Scholar ]
Merckx VSFT. Mycoheterotrophy: the biology of plants living on fungi. Mycoheterotrophy Biol Plants Living Fungi. 2012 doi: 10.1007/978-1-4614-5209-6. [ CrossRef ] [ Google Scholar ]
Miller BM (2012) Using mycorrhizae in a professional mix.
Mosa W, Paszt L, EL-Megeed N. The role of bio-fertilization in improving fruits productivity-a review. Adv Microbiol. 2014; 4 :1057–1064. doi: 10.4236/aim.2015.51003. [ CrossRef ] [ Google Scholar ]
Nadeem SM, Ahmad M, Zahir ZA, Javaid A, Ashraf M. The role of mycorrhizae and plant growth promoting rhizobacteria (PGPR) in improving crop productivity under stressful environments. Biotechnol Adv. 2014; 32 :429–448. doi: 10.1016/j.biotechadv.2013.12.005. [ PubMed ] [ CrossRef ] [ Google Scholar ]
Nederhoff EM (2007) Using a greenhouse for controlling plant growth© 57: 126–133.
Ortas I, Ustuner O. Determination of different growth media and various mycorrhizae species on citrus growth and nutrient uptake. Sci Hortic (Amsterdam) 2014; 166 :84–90. doi: 10.1016/j.scienta.2013.12.014. [ CrossRef ] [ Google Scholar ]
Pérez-Harguindeguy N, Díaz S, Garnier E, et al. New handbook for standardised measurement of plant functional traits worldwide. Aust J Bot. 2013; 61 :167–234. doi: 10.1071/BT12225. [ CrossRef ] [ Google Scholar ]
Quiroga G, Erice G, Aroca R, Delgado-Huertas A, Ruiz-Lozano JM. Elucidating the possible involvement of maize aquaporins and arbuscular mycorrhizal symbiosis in the plant ammonium and urea transport under drought stress conditions. Plants (Basel) 2020; 9 :E148. doi: 10.3390/plants9020148. [ PMC free article ] [ PubMed ] [ CrossRef ] [ Google Scholar ]
Reddy PP. Sustainable crop protection under protected cultivation. Sustain Crop Prot under Prot Cultiv. 2016 doi: 10.1007/978-981-287-952-3. [ CrossRef ] [ Google Scholar ]
Rohilla SK, Salar RK. Isolation and characterization of various fungal strains from agricultural soil contaminated with pesticides. Res J Recent Sci. 2011; 1 :297–303. doi: 10.1016/j.scienta.2009.07.019. [ CrossRef ] [ Google Scholar ]
Schnepf A, Roose T, Schweiger P. Growth model for arbuscular mycorrhizal fungi. J R Soc Interface. 2008; 5 :773–784. doi: 10.1098/rsif.2007.1250. [ PMC free article ] [ PubMed ] [ CrossRef ] [ Google Scholar ]
Shamini S, Amutha K (2015) Techniques for extraction. Int J Front Sci Technol pp 0–6
Stajich J, Berbee ML, Blackwell M, et al. The fungi. Curr Biol. 2009; 19 :R840–R845. doi: 10.1016/j.cub.2009.07.004. [ PMC free article ] [ PubMed ] [ CrossRef ] [ Google Scholar ]
Szabo K, Böll S, Erős-Honti ZS. Applying artificial mycorrhizae in planting urban trees. Appl Ecol. 2014; 12 :835–853. doi: 10.15666/aeer/1204. [ CrossRef ] [ Google Scholar ]
Tsuneo W. Pictorial atlas of soil and seed fungi: morphologies of cultured fungi and key to species. 2. Boca Raton: CRC Press; 2002. [ Google Scholar ]
van der Heijden MGA, Martin FM, Selosse MA, Sanders IR. Mycorrhizal ecology and evolution: the past, the present, and the future. New Phytol. 2015; 205 :1406–1423. doi: 10.1111/nph.13288. [ PubMed ] [ CrossRef ] [ Google Scholar ]
Vogelsang KM, Bever JD, Griswold M, Schultz PA (2004) The use of mycorrhizal fungi in erosion control applications. Contract 1–150.
Wulantuya MK, Bayandala FY, Matsukura K, Seiwa K. Gap creation alters the mode of conspecific distance-dependent seedling establishment via changes in the relative influence of pathogens and mycorrhizae. Oecologia. 2020; 192 :449–462. doi: 10.1007/s00442-020-04596-x. [ PubMed ] [ CrossRef ] [ Google Scholar ]
Zaragoza O. Mycology. Ref Modul Life Sci. 2017 doi: 10.1016/B978-0-12-809633-8.12378-7. [ CrossRef ] [ Google Scholar ]

Farmers of Fungi: Growing Mushrooms and Mycorrhizae in Your Vegetable Patch

In the last 40 years, human understanding of fungi, and their role in farm and garden ecosystems, has grown dramatically. As a result, there is a wealth of new products on the market that help home gardeners and farmers alike in improving soil fertility while diversifying their harvest. I love mushrooms on my dinner plate , but even more so, I love what various fungi, both the edible and the nearly invisible, can do for small farms and homesteaders. The two major applications of fungi for the vegetable grower are called soil mycorrhizae [mahy-k uh – rahy -zee], and myco-gardening. Soil mycorrhizae consist of vast networks of underground fungi that help our plants absorb diffuse nutrients while improving overall soil quality. Myco-gardening goes a step further, and utilizes edible and gourmet mushroom species as symbiotic, or companion plantings among various vegetable species.

The modern veggie grower has a number of commercial options to support the growth of these helpful fungi, as well as some low-tech, cost-saving, management practices that can improve your results. Before you dive into either mycorrhizae, myco-gardening, or both, take a little time to learn more about these exciting new tools in your gardening “toolbox”.

Soil Mycorrhizae

In the inches below our garden beds and vegetable fields lies a vast network of fungi—mobilizing nutrients, and improving soil conditions. The name for these fungi is mycorrhizae, literally meaning “fungus root”. Acting much like an extension of your vegetable plants’ roots, these extensive mycorrhizal networks serve as a critical link in allowing your garden to tap the full potential of your soil. While some mycorrhizal species will produce non-toxic—but inedible—mushrooms, most will simply remain as a beautiful, nearly invisible, white network of sub-soil mycelium.

Author, and founder of Fungi Perfecti (see sources), Paul Stamets, has spoken and written about the role of mycorrhizal fungi in vegetable and flower gardens extensively. Stamets has even conducted his own formal, and informal, research studies photo-documenting very impressive yield and quality differences among veggies and flowers grown with his mycorrhizal fungi inoculants. These studies do underscore the critical role that soil mycorrhizae play in plant productivity, but further analysis also reveals some important and practical lessons for home gardeners to consider.

Do I Need Mycorrhizae?

Many gardeners simply want to know, “Do I need them?”. The short answer is “yes”, followed with a “but maybe…”.

Yes, you do need—or at minimum, want—to have a rich network of soil mycorrhizae. Besides the increase in nutrient accessibility, your plants will also benefit from increased disease resistance and improved vigor. Now, you can go out and purchase packets of mycorrhizal spores to spread into your garden beds, but maybe… maybe you already have them in your soil!

In the controlled, small-scale experiments performed as testimonials for Fungi Perfecti’s Myco-Grow mycorrhizal products, photos sometimes display two- to three-fold crop-yield increases compared with the uninoculated control. But what is important for gardeners to remember when looking at these and similar photos, is that these trials are most often conducted using pasteurized soils. That is, a steam injection into the soil prior to planting eliminates all existing micro-flora, including potentially existing mycorrhizae, within the bed. This is not intended to mislead and is simply a valid scientific control, but it points to an important lesson in when mycorrhizal products should and shouldn’t be used.

If properly managed, a healthy vegetable garden, rich in organic matter, balanced in pH, and bio-diverse in planting, will naturally develop a luxuriously micro-thin web of white, utilizing the native fungal spores already present in your fields. Author Jeff Gillman writes critically on the subject in his book, The Truth about Garden Remedies: What Works, What Doesn’t and Why . Gillman believes that the basic principles of organic soil management will lead to abundant natural populations of the requisite beneficial fungi within your food plot. He also suggests that it is questionable whether the “non-native” mycorrhizae supplied by companies will survive for any extended period of time.

Where experts do seem to agree is the helpful role of these fungi in the greenhouse. Just as the impressive results from the Stamets trials were achieved in steam-sterilized soils, our greenhouses are often filled with soil-less seedling mixes—or relatively sterile compost blends. Here it seems that an infusion of purchased mycorrhizae products provides unquestioned benefit. Seedlings inoculated with mycorrhizae will benefit from the same nutrient absorption as garden plants, but also gain the advantage of improved vigor to transplanting.

The bottom line: cultivate native mycorrhizae through the good gardening practices you already know and that are listed below. When dealing with very poor soils, or seedlings in a greenhouse , it can be helpful to purchase and supplement non-native mycorrhizal spores from the sources listed in this article, or other reputable, recommended suppliers of mycological and/or plant health inoculants.

How do I cultivate mycorrhizae?

The good news for many readers, is that you probably already know how to cultivate these important mycorrhizal fungi. Some of the primary, basic principles of “sustainable” or “organic” agriculture are also the primary practices required to cultivate a healthy, balanced population of native mycorrhizal species. A complex as soils are, by focusing on some core management practices, your mycorrhizal population will flourish.

Briefly, some of the most important practices to focus on are:

Improving organic matter through the addition of compost.
Elimination of synthetic pesticides and fertilizers.
Balanced soil amendment practices.
Minimal tillage/herbicide-free no-till.
Rotation of crops within garden beds by season and year.

Adding mycorrhizae to greenhouse seedlings or depleted soils is fairly easy. The preserved spore or mycelial material will come in one of several dried forms—usually a powder or tablet. Follow the directions for dilution and apply evenly and directly at the soil level to the targeted seedlings or plot.

Myco-Gardening: A Gourmet Mushroom Bed in Your Own Backyard!

Growing your own edible, gourmet mushrooms will become another joyous series of events dotting the summer growing season. As a beginning myco-gardener, you will purchase, rather than grow, the initial mushroom mycelium , or substrate, which will be planted. The techniques below will guide you through the basic options, with some recommended resources for further exploration. Following the techniques is a brief overview of the major mushrooms appropriate to grow in your vegetable garden.

Myco-gardening Techniques

When it comes to getting started with your myco-garden, you simply need to remember three out of the next five words: “Put IT IN the GROUND”. “IT” is a chunk of mycelium—or pre-grown mushroom roots, ready to be planted in the ground. “IN” means about 1-1.5 inches deep in the soil, where you’ll place and cover the mycelium. And “GROUND” refers to the soil surrounding one or more of the recommended garden species you are probably already growing.

Below, are a few variations and suggestions made to this basic outline. Here, I include some brief first-hand accounts, where possible, to share the details of how I have approached a situation. “Mycelium Running: How Mushrooms Can Help Save the World”, by Paul Stamets, is the definitive guide to myco-gardening techniques. However, I have found it is most important for you to get hands-on with the concepts, get some experience, and “put it in the ground” .

(See my sources at the end of the article to find suppliers of mushroom mycelium and further resources.)

Growing Mushrooms in Direct Substrate

I started growing mushrooms the way most people do today: through a mail-order kit from Fungi Perfecti. I had been growing shiitake and reishi using just the plastic-bag kit the mushroom company had supplied, as I had done off-and-on for years.

My reishi mushrooms were flourishing but my woodchip block of shiitake had become contaminated with a bluish-green mold. I sliced off the half of the block that was contaminated and, being late may in coastal Maine, I buried the contaminated block of fungus roots near the herb garden in our back yard.

To my surprise, perhaps about three weeks later and following a rainstorm, a small family of perfectly formed shiitakes emerged right from where I had put it in the ground. I picked the first handful, and 2 days later the second flush was ready. But a stir-fry and omelet later, the patch went dry and nothing more was ever seen.

Since then, I have repeatedly seen mushroom mycelium that is contaminated from indoor cultivation, become healthy and invigorated by being buried in the shade of garden vegetables. This is the simplest way to begin to understand the methods of myco-gardening. Purchase one or more “production blocks” of mushroom mycelium from the suppliers listed. Cut off a good-sized chunk and put it in the ground.

Growing Mushrooms in Wood Chips

If you have access to wood chips and sawdust from non-aromatic hardwoods, you can really start producing some fabulous field mushrooms . By breaking your mycelium into small chunks and “sandwiching” those pieces between two layers of wood chips, you can create an entire bed of production for several species of edibles. If you begin using wood chips, I recommend reading one or more of Paul Stamet’s books, as he highlights several helpful points to consider.

Growing Mushrooms in Straw

In 2008/09 I worked with a group of 7th- and 8th-grade students in coastal Maine to grow elm oyster mushrooms alongside their kale crop for their school cafeteria garden, as part of their Farm-to-School Program.

In April 2008, the 7th-grade science class used basic kitchen equipment to pasteurize chopped straw from the local feed store. This cooled, wet straw was placed into medium-sized plastic bags with air-holes and allowed to ferment indoors for 3-4 weeks. By May, the bags of colonized mycelium were brought outside and planted in holes and trenches alongside the kale seedlings.

Volunteers watered and tended the garden as usual over the summer. During an early October garden harvest for the school lunch program, 8th-grade students studying world hunger discovered a full bloom of elm oyster mushrooms in the cool misty shade of the now overgrown kale patch. Enough to create a specialty stir-fried side dish for the hot lunch program, and teach students about alternative sources of protein.

The straw method is simple and appears productive. Several informative videos are available on YouTube. Although these resources all direct you to fruit the mushrooms in a greenhouse of specialized grow room, we have had luck by directly burying the colonized straw alongside brassica beds.

Growing Mushroomson Bur ied Logs

Some species, specifically Shiitake and Reishi mushrooms, particularly prefer to grow off of logs. These can still benefit from being placed in food and pesticide-free landscaping beds due to the moisture and shade provided by the plant life. Several mushroom mycelium producers advocate cultivating buried logs of shiitake and/or reishi. Both Fungi Perfecti and Mushroom Harvest, listed below, offer all of the supplies and simple tools required to inoculate hardwood logs such as oak, poplar, beech, birch, willow, and other non-aromatic hardwoods. What is required is the block of mushroom mycelium, a drill, and preferably a hand-inoculator available from listed mushroom supply companies.

Mushroom Species overview:

Elm Oyster ( Hypsizgus ulmanarius )

Elm Oyster mushroom (Hypsizgus ulmanarius)

Second only to every day “ Agaricus ” varieties of button mushroom, the delicate and mild oyster mushroom (Pleurotus ostreatus) ranks top among production for mushrooms considered “gourmet”. Yet the elm oyster mushroom ( Hypsizgus ulmanarius ), while similar in appearance to it’s commonplace namesake, is a completely different species. Elm oysters have a nutty flavor and more firm texture, but their culinary benefits are just a starting point. This species also has reported beneficial symbiotic relationships with certain vegetable crops—especially brassica species , and grows exceedingly well among kale and broccoli plants. Paul Stamets has reported a 2-fold increase in brassica yields and a 3-fold total food production increase when the vegetables were grown in the same bed as elm oyster mushrooms.

Both Fungi Perfecti, and Mushroom Harvest carry elm oyster strains, but be sure that you don’t confuse this with the common pleurotus species of oyster—of which there are many varieties as well. The pleurotus species of oyster mushroom actually appears to have negative impacts on some vegetable species and should not at this time be grown in the garden.

Natural Growing Method: Direct Substrate, Wood Chips, Straw

Wine Cap ( Stropharia rugosoannulata )

Wine Cap mushroom (Stropharia rugosoannulata)

A traditional symbiont of the grain fields for many European peasant farmers, the giant “wine cap” mushroom—so called for its burgundy aroma at maturity—can be a choice edible at best, pig food compost at worst. Thought to share a mutually beneficial relationship with corn, wine caps can become a perennial crop in your garden rotation for many growing regions in the US.

Shiitake ( Lentinula edodes )

A classic for both superb taste, and well-documented medicinal value. Shiitakes have a long history in Chinese medicine and are a delicious addition to many dishes.

Shiitakes will dry well, and store for a a very long time. Shiitake genetics vary widely. The small, pale varieties mostly sold in super markets pale in comparison o the meaty beasts that Fungi Perfecti and Mushroom Harvest are able to offer.

Natural Growing Method: Direct Substrate, Buried Logs, Wood Chips

Reishi ( Ganoderma lucidum )

If you drink tea, you should be growing reishi mushroom in your garden. This venerable and ancient medicinal tea-mushroom provides innumerable health benefits from consuming it, and incalculable joy in producing it. It’s almost alien-like, smooth, lacquered fruit body emerges from wooden substrates, responding to even minute changes in the environment. Before long, the durable, spiraling, bright-red conk is available for harvest. Substrate buried in the spring can produce enough conks for your winter’s tea supply!

Natural Growing Method: Direct Substrate, Buried Logs

Mushroom Preservation Techniques

Just like gardening with plants, myco-gardens are extremely seasonal. Also just like the plant world, mushrooms have those species born to store, storable with some help, and even those difficult to impossible to put away for much time. Reishi mushrooms are hard, durable conks that can be difficult to even saw apart. They will store at room temperature for a long time, I even keep a couple of whole conks out on a window sill for decoration.

For all other mushrooms, low-temperature drying is the preferred preservation method. The simplest method for this is to simply place the mushrooms on clean trays in a sunny, protected area until fully dried. Shiitake mushrooms dried with their gills facing the sun will actually produce a significant amount of vitamin D. For the high-tech handyman, any of the solar-vegetable drier plans available will also dry most mushrooms. Oyster mushrooms can be dried but with significant loss of quality, and enoki mushrooms should not be dried at all.

Final Thoughts: “Experiment, Reflect, Experiment Again”

As you venture into the exciting world of home mushroom and mycorrhizae cultivation, remember to experiment, reflect on what worked, what didn’t, and then experiment again. Things may seem unfamiliar at first, but if you start small and pay attention you’ll be sure to succeed in no time.

Mushroom Growing Sources and More Info

www.SoilFoodWeb.com: An excellent resource on the practical management of fungi and other life forms in your agricultural ecosystem.

www.Mycorrhizae.com : Mycorrhizal Applications inc. has a number of interesting and/or helpful references on the subject, and a number of products as well.

www.Fungi.com: Paul Stamets website and e-store: Fungi Perfecti. Excellent books, and a wide range of mycorrhizal products, under the “Myco-Grow” label. Paul’s extensive in-vivo and in-vitro spore preservation work has led his company to hold absolutely superb mushroom genetics. His shitakes are truly unlike anything you will see in stores or even most farmers’ markets. Paul is the original gourmet mushroom producer. He has changed the face of the industry and the ability for home gardeners to work with mushrooms and mycorrhizae!

www.MushroomHarvest.com: A wonderful company out of the mid-west. A small team of dedicated and professional mushroom producers with a complete line of mushroom cultivation supplies. You can buy a simple mushroom kit and put it in the ground, or you can buy everything you need to start from the mushroom spore itself! Mushroom Harvest has excellent prices and wonderful service.

Useful Links

SUBMISSIONS

Top Categories

Homestead.org Cookbook

Subscribe Now

Subscribe to our newsletter to get our newest articles instantly!

Made by Digiwolves

Privacy Policy
Cookie Policy

Username or Email Address

Remember Me

Mizzou Logo

Integrated Pest Management

University of missouri.

Taking an environmentally sensitive approach to pest management

Missouri Produce Growers

David Trinklein University of Missouri Plant Science & Technology (573) 882-9631 [email protected]

Mycorrhizae: Nature's Gift to Plant Health

David Trinklein University of Missouri (573) 882-9631 [email protected]

Published: February 10, 2020

Late in the 19th century, a Polish scientist by the name of Franciszek Kamienski made a remarkable discovery. He found there were soil-borne fungi that formed a mutually beneficial (symbiotic) relationships with the root systems of plants. Today, those fungi carry the common name of mycorrhizae which, literally interpreted, means "fungus-roots". Nearly 150 years later, scientists continue to make novel discoveries about these unique micro-organisms, and the benefits they bring to modern agriculture.

A symbiotic relationship can be defined as two living organisms living in close physical association, most often to the benefit of both. It is estimated that nearly 80 percent of all plant species on earth form mycorrhizal associations of one type or another. Mycorrhizal classification is based on the relationship of the hyphae (branching filamentous structure that form the main body of the fungus) and the roots of plants.

Ectomycorrhizae, commonly found on the roots of woody plant species, produce hyphae primarily on the exterior of plant roots. The result is a hyphal sheath known as a mantel. In contrast, endomycorrhizae (a.k.a. arbuscular mycorrhizae) grow inside the roots both between and within root cells. The relationship between fungus and plant of endomycorrhizae is a more invasive then that of ectomycorrhizae. Endomycorrhizae colonize a wide array of plants species.

At one time skeptical about the importance of mycorrhizae, the scientific community now acknowledges their benefits as both numerous and important to plant growth. For example, because of an improved "connection" of a plant's root system and the soil that surrounds it, mycorrhizae allow for increased uptake of both water and essential mineral elements, especially phosphorus. These benefits lead to improved drought tolerance, a reduction in the amount of fertilizer need to be applied to soil and increased disease resistance.

The benefit of increased disease resistance imparted by mycorrhizae has been the result of much research. It has long been theorized that a healthy, vigorous plant is better able to withstand disease pressure when compared with a malnourished, stressed plant. Causing a plant's root system to be able to take in additional nutrients and water, undoubtedly makes for a healthier plant. However, there are additional reasons why mycorrhizae help plants to resist diseases.

Since some mycorrhizae form a mantel enveloping roots, their presence represents a physical shield against invasion by other soil-borne microbes. In short, they compete with microbial pathogens for both space and root exudates. Additionally, they cause cell walls to thicken, making pathogen invasion more difficult.

Additional to the above, it has been demonstrated that mycorrhizae excrete enzymes that are toxic to soil-borne pathogens such as nematodes. Disease suppressive effects against soil-borne fungi such as Fusarium, Verticillium and Phytothora also have been documented.

Of great curiosity is the defense response plants exhibit when mycorrhizal affiliations are present. In short, plants respond with countermeasures when under the attack of disease organisms. For example, certain chemical compounds with anti-microbial actions (e.g. alkaloids) are released by plants when disease organisms attack. Again, these responses appear to be stronger in plants having mycorrhizal associations compared with those that do not.

Although most mineral soils contain mycorrhizae, their numbers often are insufficient for adequate root colonization. Additionally, soilless media used in container production lack mycorrhizae unless blended into the mix as an additive.

In light of the many benefits of mycorrhizae, supplements of the latter are available to make certain sufficient populations are present in the root zone area. Brand names* include but are not limited to Asperello® ( Trichoderma asperellum , strain T34), Obtego® ( Trichoderma asperellum, strain ICC 012 + Trichoderma gamsii, strain ICC 080), PreStop® ( Gliocladium catenulatum ), RootShield® ( Trichoderma harzianum ), RootShield Plus® ( Trichoderma harzianum + Trichoderma virens ) and SoilGard® ( Gliocladium virens ). All are OMRI listed and labeled for use on both vegetable and ornamental crops. Although natural, the above products are considered (bio)pesticides and should be handled with care. Always read and follow label directions.

Additional biofungicides labeled for vegetable crops include Actinovate® ( Streptomyces lydicus ) and Cease® ( Bacillus subtilis ). However, the latter two contain beneficial bacteria rather than mycorrhizae.

In most cases, the above products are applied both before and after transplanting crops such as vegetables. Typically, the first application is made as a drench to transplants (e.g. tomato) growing in a greenhouse. Additional applications normally are made after setting plants in the field (or production greenhouse/high tunnel) via "chemigation", using drip irrigation equipment. Frequency of repeated field application depends both upon product and disease pressure.

*Mention of brand names does not imply endorsement by the author or University of Missouri Extension.

Subscribe to receive similar articles sent directly to your inbox!

Mycorrhizae: Nature's Gift to Plant Health (02/10/20)

Copyright © #thisyear# — Curators of the University of Missouri. All rights reserved. DMCA and other copyright information. An equal opportunity/access/affirmative action/pro-disabled and veteran employer.

Printed from: https://ipm.missouri.edu E-mail: [email protected]

REVISED: February 10, 2020

Mycorrhizae

Fostering plant health through fungal symbiosis.

Mycorrhizae Introduction

Mycorrhizae, a term that refers to the symbiotic relationship between certain soil fungi and plant roots, represent a revolutionary approach to natural gardening and farming.

These beneficial fungi colonize plant roots, extending their network into the soil and significantly enhancing the plant's ability to absorb water and nutrients.

This guide will delve into the myriad benefits of incorporating mycorrhizae into your gardening practices, explore its nutritional contributions to plant health, offer guidance on application, and discuss its compatibility with various plants and soil types, all while highlighting its sustainability and positive environmental impact.

Mycorrhizae Key Benefits

Incorporating mycorrhizae into the garden soil or potting mix offers profound benefits:

Enhanced Nutrient Uptake : Mycorrhizal fungi increase the surface absorbing area of roots, significantly improving the uptake of water and nutrients, particularly phosphorus.
Drought Resistance : Plants with mycorrhizal associations are more resilient to water stress and can survive better in drought conditions.
Improved Soil Structure : The mycelium of mycorrhizal fungi produces substances that bind soil particles together, improving soil aeration and water retention.
Disease Suppression : Mycorrhizae can help protect plants from certain soil-borne diseases by outcompeting harmful pathogens for space and resources.

Mycorrhizae Nutritional Profile

While mycorrhizae themselves do not provide nutrients directly, they play a crucial role in facilitating nutrient availability and uptake.

By forming a network of hyphae that extends far beyond the root zone, mycorrhizae can access and transport water and soil nutrients, including phosphorus, nitrogen, and micronutrients, back to the plant more efficiently than roots alone.

This symbiotic relationship is essential for the optimal growth and health of most plant species.

How to Use Mycorrhizae

Applying mycorrhizae to your garden is straightforward and can be done in several ways:

At Planting : Directly apply mycorrhizal inoculant to the roots of transplants or sprinkle in the planting holes of seeds. The close contact between the roots and fungi is crucial for the symbiosis to establish.
Existing Plants : For established plants, mix mycorrhizal inoculant with water according to the product instructions and apply it around the base of the plants, allowing it to seep into the soil and reach the roots.
Potting Mixes : Incorporate mycorrhizal inoculant into your potting mix before planting to ensure new plants benefit from the start.

Ideal Plants and Soil Types

Mycorrhizae are beneficial for a wide range of plant species, including vegetables, fruits, flowers, and trees.

Most plants form these symbiotic relationships, with the exception of some families like Brassicaceae (e.g., broccoli, cabbage) and Chenopodiaceae (e.g., beets, spinach).

Mycorrhizae can be particularly advantageous in nutrient-poor soils, helping plants thrive in less-than-ideal conditions by enhancing nutrient availability and uptake.

Sustainability and Environmental Impact

The use of mycorrhizae in gardening and agriculture promotes sustainability by reducing the need for chemical fertilizers and water. This natural symbiosis enhances plant health and growth using biological processes, minimizing environmental impact and supporting soil health.

Furthermore, by improving soil structure and increasing organic matter through the life cycle of the fungi, mycorrhizae contribute to the carbon sequestration capacity of soils, helping to mitigate climate change.

Mycorrhizae Tips and Tricks

To maximize the benefits of mycorrhizae in your garden, consider the following tips:

Choose the Right Type : Ensure you are using the appropriate type of mycorrhizal fungi (endomycorrhizae for most plants, ectomycorrhizae for certain trees and shrubs) for your specific plants.
Avoid High-Phosphorus Fertilizers : High levels of phosphorus can inhibit the formation of mycorrhizal associations. Use fertilizers with balanced or low phosphorus levels.
Maintain Soil Health : Organic matter, proper aeration, and adequate moisture support the growth and function of mycorrhizal fungi, enhancing their benefits to plants.

Mycorrhizae Conclusion

Mycorrhizae represent a powerful tool for natural gardening, offering a way to enhance plant health, improve nutrient uptake, and support sustainable soil management practices.

By integrating mycorrhizae into your gardening routine, you can enjoy healthier plants and more bountiful harvests, all while contributing to the ecological balance of your garden ecosystem. Explore our shop and experiment with mycorrhizal inoculants , fostering a community of gardeners committed to sustainability and the well-being of our planet.

Mycorrhizae

Reviewed by: BD Editors

Mycorrhizae Definition

Mycorrhizae literally translates to “fungus-root.” Mycorrhiza defines a (generally) mutually beneficial relationship between the root of a plant and a fungus that colonizes the plant root. In many plants, mycorrhiza are fungi that grow inside the plant’s roots, or on the surfaces of the roots. The plant and the fungus have a mutually beneficial relationship, where the fungus facilitates water and nutrient uptake in the plant, and the plant provides food and nutrients created by photosynthesis to the fungus. This exchange is a significant factor in nutrient cycles and the ecology, evolution, and physiology of plants.

In some cases, the relationship is not mutually beneficial. Sometimes, the fungus is mildly harmful to the plant, and at other times, the plant feeds from the fungus.

Not all plants will have mycorrhizal associations. In environments in which water and nutrients are abundant in the soil, plants do not require the assistance of mycorrhizal fungi, nor might mycorrhizal fungi germinate and grow in such environments.

Types of Mycorrhizae

There are two predominant types of mycorrhizae: ectomycorrhizae, and endomycorrhizae. They are classified by where the fungi colonize on the plants.

Ectomycorrhiza

Ectomycorrhiza tend to form mutual symbiotic relationships with woody plants, including birch, beech, willow, pine, oak, spruce, and fir. Ectomycorrhizal relationships are characterized by an intercellular surface known as the Hartig Net. The Hartig Net consists of highly branched hyphae connecting the epidermal and cortical root cells. Additionally, ectomycorrhiza can be identified by the formation of a dense hyphal sheath surrounding the root’s surface. This is known as the mantle. In other words, ectomycorrhiza live only on the outside of the root. Overall, only 5-10% of terrestrial plant species have ectomycorrhiza.

Endomycorrhiza

On the other hand, endomycorrhizae are found in over 80% of extant plant species -including crops and greenhouse plants such as most vegetables, grasses, flowers, and fruit trees. Endomycorrhizal relationships are characterized by a penetration of the cortical cells by the fungi and the formation of arbuscules and vesicles by the fungi. In other words, endomycorrhiza have an exchange mechanism on the inside of the root, with the fungi’s hyphae extending outside of the root. It is a more invasive relationship compared to that of the ectomycorrhiza.

Endomycorrhiza are further subdivided into specific types: Arbuscular Mycorrhizae, Ericaceous Mycorrhizae, Arbutoid Mycorrhizae, and Orchidaceous Mycorrhizae.

Examples of Mycorrhiza

Orchid mycorrhiza.

As mentioned above, some orchids cannot photosynthesize prior to the seedling stage. Other orchids are entirely non-photosynthetic. All orchids, however, depend on the sugars provided by their fungal partner for at least some part of their lives. Orchid seeds require fungal invasion in order to germinate because, independently, the seedlings cannot acquire enough nutrients to grow. In this relationship, the orchid parasitizes the fungus that invades its roots. Once the seed coat ruptures and roots begin to emerge, the hyphae of orchidaceous mycorrhiza penetrate the root’s cells and create hyphal coils, or pelotons, which are sites of nutrient exchange.

Arbuscular Mycorrhiza

Arbuscular mycorrhizae are the most widespread of the micorrhizae species and are well known for their notably high affinity for phosphorus and ability for nutrient uptake. They form arbuscules, which are the sites of exchange for nutrients such as phosphorus, carbon, and water. The fungi involved in this mycorrhizal association are members of the zygomycota family and appear to be obligate symbionts. In other words, the fungi cannot grow in the absence of their plant host.

Ericaceous Mycorrhiza

Ericaceous mycorrhizae is generally found on plants of the order Ericales and in inhospitable, acidic environments. While they do penetrate and invaginate the root cells, ericoid mycorrhiza do not create arbuscules. They do, however, help regulate the plant’s acquisition of minerals including iron, manganese, and aluminum. Additionally, mycorrhizal fungi form hyphal coils outside of the root cells, significantly increasing root volume.

Arbutoid Mycorrhiza

Arbutoid mycorrhiza are a type of endomycorrhizal fungi that look similar to ectomycorrhizal fungi. They form a fungal sheath that encompasses the roots of the plant; however, the hyphae of the arbutoid mycorrhiza penetrate the cortical cells of plant roots, differentiating it from ectomycorrhizal fungi.

Ectotrophic Mycorrhiza

The fungi involved in this mycorrhizal association are from the Ascomyota and Basidiomyota families. They are found in many trees in cooler environments. Unlike their wood-rotting family members, these fungi are not adapted to degrade cellulose and other plant materials; instead, they derive their nutrients and sugars from the roots of their living plant host.

Plant Benefits from Mycorrhizae

Mycorrhiza associations are particularly beneficial in areas where the soil does not contain sufficient nitrogen and phosphorus, as well as in areas where water is not easily accessible. Because the mycorrhizal mycelia are much finer and smaller in diameter than roots and root hairs, they vastly increase the surface area for absorption of water, phosphorus, amino acids, and nitrogen—almost like a second set of roots! As these nutrients are essential for plant growth, plants with mycorrhizal associations have a leg-up on their non-mycorrhizal associated counterparts that rely solely on roots for the uptake of materials. Without mycorrhiza, plants can be out-competed, possibly leading to a change in the plant composition of the area.

Additionally, studies have found that plants with mycorrhizal associations are more resistant to certain soil-borne diseases. In fact, mycorrhizal fungi can be an effective method of disease control. In the case of sheathing mycorrhiza, they create a physical barrier between pathogens and plant roots. Mycorrhiza also thicken the root’s cell walls through lignifications and the production of other carbohydrates; compete with pathogens for the uptake of essential nutrients; stimulate plant production of metabolites that increases resistance to disease; stimulate flavonolic wall infusions that prevent lesion formation and invasion by pathogens; and increase plant root concentrations of orthodihydorxy phenol and other allochemicals to deter pathogenic activity. In addition to disease resistance, mycorrhizal fungi can also impart to its host plant resistance to toxicity and resistance to insects, ultimately improving plant fitness and vigor.

In more complex relationships, mycorrhizal fungi can connect individual plants within a mycorrhizal network. This network functions to transport materials such as water, carbon, and other nutrients from plant to plant, and even provides some type of defense communication via chemicals signifying an attack on an individual within the network. Not only can plants use these signals to start producing natural insect repellants, they can also use them to start producing an attractant to bring in natural predators of the plant’s pests!

In some cases, mycorrhizal fungi allow plants to bypass the need for soil uptake, such as trees in dystrophic forests. Here, phosphates and other nutrients are taken directly from the leaf litter via mycorrhizal hyphae.

Mycorrhizal fungi are also able to interact with and change the environment in the favor of the host plants—namely, by improving soil structure and quality. The filaments of mycorrhizal fungi create humic compounds, polysaccharides, and glycoproteins that bind soils, increase soil porosity, and promote aeration and water movement into the soil. In environments that have highly compacted or sandy soils, improved soil structure can be more important for plant survival than nutrient uptake.

Some ectomycorrhizal associations create structures that host nitrogen-fixing bacteria, which would largely contribute to the amount of nitrogen taken up by plants in nutrient-poor environments, and would play a large part in the nitrogen cycle. The mycorrhizal fungi, however, do not fix nitrogen themselves.

Fungi Benefits from Plants

When the plant is provided with enough water and nutrients, it is able to photosynthesis and produce glucose and sucrose—some of which is made directly accessible to the mycorrhizal fungi. The fungi are also provided with photosynthetically fixed carbon from the host, which functions as a trigger for nitrogen uptake and transport by the fungi. All of this is necessary for fungal growth and reproduction.

Ectomycorrhiza. (2017, May 14). Retrieved May 16, 2017, from https://en.wikipedia.org/wiki/Ectomycorrhiza What are Mycorrhizae? – GrowersGold. (2011, March 3). Retrieved May 16, 2017, from http://www.growersgold.net/what-is-mycorrhizae Zeng, R. (2006). Disease Resistance In Plants Through Mycorrhizal Fungi Induced Allelochemicals. Allelochemicals: Biological Control of Plant Pathogens and Diseases Disease Management of Fruits and Vegetables, 181-192. doi:10.1007/1-4020-4447-x_10

Cite This Article

Subscribe to our newsletter, privacy policy, terms of service, scholarship, latest posts, white blood cell, t cell immunity, satellite cells, embryonic stem cells, popular topics, cellular respiration, animal cell, acetic acid, homeostasis, natural selection, scientific method.

Mysterious mycorrhizae? a field trip and classroom experiment to demystify the symbioses formed between plants and fungi

Earth and Sustainability

Research output : Contribution to journal › Article › peer-review

Original language	English (US)
Pages (from-to)	424-429
Number of pages	6
Journal
Volume	71
Issue number	7
DOIs
State	Published - Sep 2009

ASJC Scopus subject areas

Agricultural and Biological Sciences (miscellaneous)
General Agricultural and Biological Sciences

Access to Document

10.2307/20565346

Wisconsin Horticulture

Division of Extension

Mycorrhizae

Share on Facebook
Share on X (Twitter)
Share via Email

Ectomycorrhizal roots of Picea abies (photo by H. Blaschke).

Additional Information

Components of Ectomycorrhizal Associations – nice diagram of fungus-plant interrelationship
Mycorrhiza Literature Exchange – a global clearinghouse for mycorrhizal information maintained by the University of Tennessee
International Mycorrhiza Society – for professional scientific researchers

Ask Your Gardening Question

If you’re unable to find the information you need, please submit your gardening question here:

Latest Horticulture News

Upcoming Online Gardening Programs Focused on Pollinators
Plant Diseases: Sometimes the Best Medicine is No Medicine
How to Deal with Surface Tree Roots
Spring is Tick Season in Wisconsin

Featured Articles by Season

Soil microbiome indicators can predict crop growth response to large-scale inoculation with arbuscular mycorrhizal fungi

Stefanie Lutz ORCID: orcid.org/0000-0002-3845-0862 1 na1 ,
Natacha Bodenhausen ORCID: orcid.org/0000-0001-9680-1176 2 na1 ,
Julia Hess 1 ,
Alain Valzano-Held ORCID: orcid.org/0000-0002-0911-5467 1 ,
Jan Waelchli ORCID: orcid.org/0000-0002-4384-6570 3 ,
Gabriel Deslandes-Hérold ORCID: orcid.org/0000-0002-5072-1450 3 , 4 nAff6 ,
Klaus Schlaeppi ORCID: orcid.org/0000-0003-3620-0875 3 na1 &
Marcel G. A. van der Heijden ORCID: orcid.org/0000-0001-7040-1924 1 , 5 na1

Nature Microbiology volume 8 , pages 2277–2289 ( 2023 ) Cite this article

16k Accesses

17 Citations

491 Altmetric

Metrics details

Arbuscular mycorrhiza

An Author Correction to this article was published on 19 December 2023

This article has been updated

Alternative solutions to mineral fertilizers and pesticides that reduce the environmental impact of agriculture are urgently needed. Arbuscular mycorrhizal fungi (AMF) can enhance plant nutrient uptake and reduce plant stress; yet, large-scale field inoculation trials with AMF are missing, and so far, results remain unpredictable. We conducted on-farm experiments in 54 fields in Switzerland and quantified the effects on maize growth. Growth response to AMF inoculation was highly variable, ranging from −12% to +40%. With few soil parameters and mainly soil microbiome indicators, we could successfully predict 86% of the variation in plant growth response to inoculation. The abundance of pathogenic fungi, rather than nutrient availability, best predicted (33%) AMF inoculation success. Our results indicate that soil microbiome indicators offer a sustainable biotechnological perspective to predict inoculation success at the beginning of the growing season. This predictability increases the profitability of microbiome engineering as a tool for sustainable agricultural management.

Global turnover of soil mineral-associated and particulate organic carbon

A global atlas of soil viruses reveals unexplored biodiversity and potential biogeochemical impacts

Conceptualizing soil fauna effects on labile and stabilized soil organic matter

Agricultural intensification has achieved substantial yield increases but also contributed to biodiversity loss, soil degradation, soil pollution, greenhouse gas emissions and water eutrophication 1 , 2 . Ensuring food security for a growing population while reducing environmental impacts poses a dual challenge to agricultural production 3 . Alternative solutions to agrochemicals are urgently needed to increase the sustainability of agriculture.

Soil ecological engineering is an important strategy to increase sustainability and reduce the need for external resources 4 , 5 , 6 . Promoting beneficial soil biota is an integral part of this management practice and arbuscular mycorrhizal fungi (AMF) in particular have enormous potential to play a pivotal role 4 , 7 . AMF belong to the phylum Glomeromycota and form symbiotic relationships with the majority of terrestrial plants. They provide the plants with nutrients in exchange for carbohydrates 8 . A range of studies have shown that AMF inoculation in the greenhouse and in the field can enhance growth of a wide range of plants, including many agricultural crops 9 , 10 , 11 . AMF are best known for their ability to enhance plant nutrient uptake, in particular phosphorus, but also other nutrients 8 , 12 . In addition, a range of studies have shown that AMF also can improve soil structure, nutrient retention in the soil 13 , reduction of greenhouse gas emission 14 , 15 , drought tolerance 16 , 17 and disease resistance 18 , 19 .

Harnessing the beneficial properties of AMF can be achieved in two ways. Native AMF communities can be promoted through favourable agricultural practices such as low tillage intensity, crop diversification and organic farming 20 , 21 , 22 . Alternatively, AMF can also be deliberately introduced into the soil. The latter can be a valuable strategy for restoring exhausted soils with low abundance of native AMF. While positive effects are often reported in greenhouse studies, the results of field inoculations with AMF are highly variable 9 , 10 , 23 . The mycorrhizal growth response (MGR) is a metric to express the effects of AMF inoculation on crop yield 24 . Depending on the soil and plant context, MGR effects range from beneficial to detrimental 25 , 26 . One unsolved aspect of the variable inoculation success is that the extent to which the introduced AMF are established often remains unknown 27 . Thus, the impact of field inoculations with AMF on crop yield is highly unpredictable and their application is currently not reliable.

For AMF inoculations to become an agronomically useful management practice, reliable predictions of the conditions under which AMF enhance crop yields are urgently needed. Therefore, we conducted inoculation trials with AMF in arable fields and investigated their effect on maize growth in combination with measurements of the local chemical, physical and biological soil parameters (hereafter, ‘soil parameters’) and soil fungal microbiome, as well as changes in root microbiome composition in response to AMF inoculation (Fig. 1 ).

To develop a soil diagnostic tool to predict the success of AMF inoculation, a total of 52 soil parameters and the soil microbiome were analysed in 54 fields at the beginning of the growing season. After sowing, inoculations with the AMF R. irregulare SAF22 (or a control substrate) were carried out. At harvest, the mycorrhizal growth response, total root colonization and composition of the root microbiome were analysed to assess the success of AMF inoculation.

Here we aimed to test whether field inoculations with AMF are feasible and whether their success can be successfully predicted. In our proof-of-concept study, we identified the most important predictors of MGR. This will pave the way for developing a soil diagnostic tool that will inform farmers about the expected benefits of AMF inoculations in their fields, thus improving the reliability and profitability of their application.

Maize growth responses to AMF inoculation vary strongly

Inoculation trials with the native AM fungus Rhizoglomus irregulare SAF22 were carried out in 54 maize fields in Northern Switzerland and their effects on maize growth were investigated (Supplementary Table 1 ). The MGR varied widely, ranging from −12 to +40 % (Fig. 2 ). Significant positive growth responses (+12 to +40%) were observed in a quarter (14) of the fields. In two fields, a significant reduction in growth (−12 %) was observed. For downstream analyses, we categorized fields according to the 25th (<−2.4% MGR) and 75th (>12.1% MGR) quantiles of the MGR range, hereafter referred to as ‘low-MGR’ and ‘high-MGR’ fields, respectively.

MGR varied widely, ranging from −12 to +40%. Plot shows mean values (circle), as well as the confidence interval of MGR for each field ( n = 8 independent control and inoculated plots). Significant differences are highlighted by filled circles. High- and low-MGR fields (75th and 25th quantiles) are highlighted by shaded areas and bold x- axis labels. We observed a slight year effect. 2019 was the year with the lowest number of fields with significant positive effects (4 out of 25 fields, 16% of fields) and 2020 was the year with the highest number (5 out of 12 fields, 41% of fields). This could be due to different weather conditions during the 3 yr.

All inoculation trials were performed without phosphorus fertilization. In a subset of the fields (18 fields in 2018), we also tested whether the addition of phosphorus influenced inoculation success (Extended Data Fig. 1 ). In the majority of tested fields, we did not find a significant effect of fertilizer type.

Most important soil parameters for MGR prediction

To identify the main factors explaining the variation in MGR, we measured a total of 52 soil parameters. Field sites used in this study differed widely in terms of soil properties (for example, total phosphorus (P) content varied with a factor of 4 (from 570 to 2,312 mg kg −1 dry soil), mineralized nitrogen (N) content varied with a factor of 11 (from 9 to 102 mg kg −1 dry soil) and soil organic carbon content varied with a factor of 4 (from 0.8 to 3.4%); Supplementary Table 1 ). Different soil types were examined in ref. 28 . We first assessed pairwise correlations between soil properties and MGR for 54 fields. This yielded only few and weak relationships (Supplementary Table 2 ).

Because such one-factor analyses were clearly insufficient to explain MGR, we examined the relationship between soil properties and MGR with multivariate models in a second step. For this we reduced the pool of 38 parameters for which data were available for all 54 fields and filtered out strongly correlated variables ( r > 0.8 or r < −0.8; Extended Data Figs. 2 and 3 ). This resulted in a subset of 22 variables (Supplementary Table 3 ). Further reductions were achieved using three different approaches including a random forest analysis 29 (Fig. 3a and Supplementary Table 4 ), stepwise model selection using ‘stepAIC’ 30 and exhaustive screening using ‘glmulti’ 31 ( Methods and Supplementary Table 5 ). The following 6 variables were identified by all approaches: magnesium (EDTA), magnesium (H 2 O), manganese, mineralized N (N min ), iron and microbial biomass carbon (cMIC). The final pool of soil parameters for subsequent MGR prediction was derived from the combined result of all three analyses and comprised 15 variables (Fig. 3a and Supplementary Table 5 ).

a , Soil parameters were initially filtered through the removal of co-correlated variables, followed by random forest, stepAIC and glmulti analyses resulting in a final set of 15 variables, displayed as loading vectors in the PCA plot of all soil parameters. b , Soil fungal OTUs were selected using indicator species, differential abundance and random forest analyses, and a further refinement step using glmulti. This resulted in a final set of 13 sOTUs, depicted as loading vectors in the partial (adjusted for year effect) dbRDA plot, showing a clear grouping by MGR category. c , Establishment success of the inoculated AMF. Fields are shown in descending order of MGR (grey bars, representing the confidence interval of MGR for each field, displayed on the secondary y axis). AMF establishment success (displayed on the primary y axis) is shown as the difference (Δ) between inoculated and control samples for the relative abundances of SAF22 rOTUs and total colonization. The plot shows that there is no relationship between MGR and establishment success (indicated by the smoothed lines, which follow a different trend from that of MGR). However, the relative abundance of SAF22 and total root colonization are strongly correlated (see Extended Data Fig. 5c for pairwise correlations).

Most important soil OTUs for MGR prediction

We determined the soil fungal communities with long-read sequencing and found a high relative abundance of Ascomycota, followed by Mortierellomycota and Basidiomycota 28 (Supplementary Table 6 ). Rarefaction analysis confirmed that sufficient sequencing depth was reached to capture the fungal diversity 28 . Unconstrained ordination revealed that soil fungal communities were grouped by year, which was subsequently included as a co-variable in all downstream analyses (Extended Data Fig. 3 ).

Analogous to the soil parameters, we reduced the number of fungal taxa (represented as operational taxonomic units (OTUs), hereafter referred to as sOTUs for soil OTUs) for model input using different approaches (Fig. 3b ). The combined results of an indicator species analysis (Supplementary Table 7 ) and differential abundance analysis (Supplementary Table 8 ) comparing high- and low-MGR fields, as well as a random forest analysis performed on the continuous MGR values (Supplementary Table 9 ), yielded a total of 44 sOTUs (see Supplementary Methods for more details).

To further refine the pool of sOTUs, another exhaustive automated model selection was performed using glmulti 31 , resulting in the selection of 7 and 6 sOTUs associated with high and low MGR, respectively (Fig. 3b and Supplementary Table 10 ). The genus Phaeohelotium was represented with two sOTUs that were associated with low MGR. In contrast, sOTUs that were more abundant in fields with high MGR included several genera with plant pathogenicity potential. These comprised Fusarium , Olpidium , Myrothecium , Striaticonidium and Chaetomium . The summed relative abundances of these sOTUs associated with low and high MGR each correlated well with MGR (Fig. 4a,b ). In fields with high MGR, up to two indicator sOTUs for high MGR were present (Fig. 4c ), while in fields with low MGR, two to three indicator sOTUs for low MGR were abundant (Extended Data Fig. 4 ).

a , b , The summed relative abundances of the 7 and 6 sOTUs indicative of high ( a ) and low ( b ) MGR, respectively, correlate well with the residuals of MGR after fitting the 15 soil parameters. The correlation coefficients (Pearson, rho) and the significance values ( P ) are displayed in the plots. The regression line is shown in grey and the 95% confidence interval is the grey shaded area. c , The relative abundance of high-MGR sOTUs was standardized using z transformation for better visualization and is displayed on the primary y axis. The MGR range per field is indicated by grey bars (representing the confidence interval of MGR) and is displayed on the secondary y axis. Fields are arranged in descending order of MGR. The plot shows that on average, only one or two of these OTUs were abundant in a field with high MGR. Therefore, these predictors are only suitable in combination in a multiple linear regression model. NA, unknown. Full information on taxa identities can be found in Supplementary Table 10 . The corresponding plot for low MGR OTUs can be found in Extended Data Fig. 4 .

Establishment success is insufficient to explain MGR

To examine the establishment of the AMF inoculum in the maize roots, we measured total root colonization by microscopy and establishment success of the inoculated strain SAF22 by profiling the fungal root microbiome using long-read sequencing (root (r)OTUs). However, none of these parameters correlated with MGR (Fig. 4c and Extended Data Fig. 5 ).

The fungal root microbiome was determined using PCR primers that enrich for AMF (Supplementary Fig. 1 and Table 11 ). Rarefaction analysis confirmed that sufficient sequencing depth was reached (Supplementary Fig. 2 ). Similar to the soil microbiome, albeit less pronounced, the native root microbiome (control samples) showed a year effect (Extended Data Fig. 6 ). With the ratio between inoculated and control samples, we quantified the establishment success of the inoculum R. irregulare SAF22, which ranged between 17.8% and 100% in 38 fields (Supplementary Table 13 ). In 5 fields, establishment was very low (0.7–9.4%), while in 11 fields, it did not establish at all (0%). Overall, we found clear differences between control and inoculated samples (Extended Data Fig. 7 and Supplementary Fig. 3 ).

Soil pathogenic fungi are most important predictors of MGR

For prediction of MGR, we then modelled all the previously selected 15 soil parameters and 13 sOTUs (Fig. 5 ). Combining these predictors in a full model, they were able to explain 86% of the variation in MGR ( P < 0.001; Fig. 5a ). Interestingly, the 15 soil parameters were by far less important (29%) than the 13 sOTUs (53%). A reduction of predictors, comparing all possible models with a maximum size of 10 predictors, resulted in a model consisting of 3 high-MGR sOTUs ( Trichosporon , Myrothecium , unknown), 3 low-MGR sOTUs ( Powellomyces , two unknown), as well as N min , cMIC, ammonium and magnesium (H 2 O) (Fig. 5b ). Although highly simplified, this model was still able to explain 68% of the variation in MGR ( P < 0.001). An alternative model with only the 13 sOTUs (Fig. 5c ) was almost as good, reaching 66% explanation ( P < 0.001).

Predictors are displayed on the y axis. The combined relative importance of soil parameters and sOTUs associated with low and high MGR is summarized in grey bars. A higher value of a predictor in blue is associated with a higher MGR, while a higher value of a predictor in red is associated with a lower MGR. The genus identity of the OTUs is given in brackets. a , Full model with 15 soil parameters, 13 soil fungal OTUs and year. The growth responses of maize to mycorrhizal inoculation were best predicted by the soil fungi that were present in the fields (53%) and to a lower degree by the soil parameters (29%). b , Reduced model with the top 10 predictors. c , Soil fungal model. F -test: *** P < 0.001, ** P = 0.001–0.01, * P = 0.01–0.05, ‘.’ P = 0.05–0.1.

sOTU18, identified as Trichosporon sp., was the most important predictor for high MGR in all models. Species of the genus Trichosporon are known pathogens; however, there are currently no reports on plant pathogenicity. Interestingly, the abundance of sOTU18 correlated with variables indicative of low-carbon and low-nutrient fields (Extended Data Fig. 8 ).

We followed a binary classification approach to cross-validate our models since the ultimate goal is not to predict the exact value of the MGR, but to provide recommendations on whether inoculation provides a benefit (significant positive growth response, >12.2%, as this was the lower limit for significant positive effects in this study) or not (neutral or negative growth response, <12.2%). This resulted in a high mean accuracy of 80% (full model) and 83% (reduced model and soil fungus model). We are thus able to make the right decision (to inoculate or not) with a high probability.

Root microbiome data confirm results of prediction model

To investigate the relationships between plant pathogenic soil fungi and the inoculated AMF, we investigated the root fungal profiles for community shifts in response to inoculation. We performed a differential abundance analysis comparing control vs inoculated plots in low-MGR fields and control vs inoculated plots in high-MGR fields. In low- as well as high-MGR fields, we find a lower relative abundance of several native AMF (including the genera Funneliformis , Rhizophagus , Glomus and Paraglomus ; Fig. 6 , and Supplementary Tables 14 and 15 ) in the plots inoculated with R. irregulare SAF22. It is important to note that AMF inoculation changed community composition, but it had no significant effect on AMF diversity (AMF OTU richness increased in 42% of the fields and decreased in 44% of the fields upon inoculation; Supplementary Table 16 ).

Differential abundances were assessed using DESeq2 (Wald test; significance threshold, 0.1; P values adjusted for multiple comparison; dashed lines correspond to a log 2 FC of −1 and 1 to guide the eye). In fields with low MGR (left), the inoculated R. irregulare SAF22 (represented by several OTUs corresponding to rRNA variants, see Methods ) replaced the native AMF, while in fields with high MGR (right), not only the native AMF but also pathogenic fungi were replaced. Full taxonomic assignments of the OTUs can be found in Supplementary Tables 14 and 15 . It should be noted that primers targeting AMF were used for the root data, so a number of fungi could not be detected, including some pathogens (for example, Fusarium , Myrothecium ) that had been identified as significant in the soil data. Of note, we identified Trichosporon , the most important soil fungal OTU in the predictive model, also in the data of the root fungal communities (rOTU20 shares 100% sequence similarity with sOTU18 over its entire amplicon length). Even though it does not appear in the plot of fields with high MGR as it was below the significant threshold ( P = 0.252), it showed a similar trend (log 2 FoldChange = −0.583) as the displayed pathogens (Supplementary Table 15 ).

Even more remarkably, in fields with high MGR, the introduced strain SAF22 also reduced the relative abundance of several plant pathogenic taxa. These included the genera Olpidium , Cladosporium , Mycochaetophora , Pyrenochaeta and Vishniacozyma (Fig. 6 and Supplementary Table 15 ). Taken together, the in-depth analysis of the root fungal profiles revealed a plausible mechanistic basis for positive MGR: the introduced AMF outcompetes the otherwise plant pathogenic fungi from the roots most probably resulting in better growth of the maize plants.

Here we show that inoculation with arbuscular mycorrhizal fungi significantly increased maize yield. We achieved a significant positive increase in biomass of 12–40% in a quarter of the fields, which is considerably higher than the annual yield increases through breeding for a range of crops (which are often below 1%) 32 . Moreover, effect sizes of adding cover crops (up to 8%) 33 and other biofertilizers (up to 12%) 34 in comparable climatic regions and production systems are also lower compared with growth increases in inoculated high-MGR fields in this study.

While many studies pointed to the importance of AMF for plant nutrition, this study links AMF inoculation to soil pathogen protection. Pathogen abundance in the soil best explained AMF inoculation success (33% of variance explained), while soil parameters were less important (29%; Fig. 5a ). While a range of studies have shown that inoculation with AMF can promote plant growth in the field 9 , 10 , 11 , results are variable and none have used soil characteristics and molecular-based soil microbiome analysis to specifically predict under which conditions AMF can promote plant growth.

Phosphorus availability tended to be negatively associated with inoculation success in previous studies 35 . In our study, phosphorus explained less than 2% of the variation in MGR, which was also reflected in the outcome of the fertilizer trial (see Supplementary Results and Extended Data Fig. 1 ). Despite a large (factor of 26) variation in immediately plant-available phosphorus levels (0.34–9.07 mg kg −1 , H 2 O-CO 2 extraction; Supplementary Table 1 ), most soils were above the threshold for phosphorus deficiency in Swiss soils (0.58 mg kg −1 ) 36 , perhaps also explaining why AMF inoculation success was best explained by other factors.

Further, positive growth responses were associated with lower soil organic carbon levels and especially with reduced soil microbial biomass carbon (Fig. 5b ). Soil microbial biomass represents the living fraction of organic carbon and is an important component of soil health 37 , 38 . Fields with low microbial carbon content appeared to benefit more from AMF inoculations, suggesting that AMF are particularly important when soil health is low. It is also known that organic amendments can suppress a wide range of pathogens in the soil 39 , 40 . Therefore, protection from pathogens by inoculated AMF may be particularly important in soils with low organic content. Consequently, AMF inoculations in healthier soils with high abundance of OTUs associated with low MGR (for example, Phaeohelotium ; Supplementary Table 10 ) are less likely to provide economic benefits.

Several sOTUs associated with high MGR in this study are known as plant pathogenic taxa (Supplementary Table 10 ) and can infect important crops including maize 41 , 42 , 43 , 44 , 45 . These comprise Olpidium brassicae 41 , 42 , Myrothecium sp. 43 and Fusarium equiseti 44 , 45 . The most important predictor in the model, however, was sOTU18 with the genus assignment Trichosporon , known to cause diseases in human 46 . So far, this genus has not been described in relation to plant pathogenicity; yet, it best explained inoculation success with AMF and especially in high-MGR fields where it was less abundant in inoculated plots, AMF had a positive impact on plant yield (Supplementary Tables 14 and 15 ), suggesting a negative effect of this taxon on maize growth. Moreover, sOTU18 is an indicator of poorer soil properties (that is, negatively correlated with organic carbon and soil fertility, and positively correlated with sand content; Extended Data Fig. 8 ). Overall, pathogen abundance might be more pronounced in poorer soil. The addition of AMF provides additional protection and plants growing in these fields might benefit more from mycorrhizal inoculation. Given the limitations of marker genes in predicting fungal lifestyles, further studies need to isolate these fungi and test whether they indeed negatively affect maize growth to experimentally verify their pathogenicity potential and to what extent AMF can contribute to pathobiome management.

Only few pathogens seem to be important in the studied context, as the summed abundances of all soil fungal pathogens identified by guild-based screening was not able to predict MGR (see Supplementary Results and Extended Data Fig. 4 ). AMF strains are probably specialized in their ability to protect against specific pathogens. Here we inoculated an AMF strain that was isolated from Swiss soil and can establish well in a wide range of soil types 24 , 35 . The inclusion of other AMF genotypes to be screened for their properties to protect against specific pathogens would not only broaden the scope of this management practice and facilitate establishment under a wide range of conditions, but could also prevent possible agricultural intensification and biodiversity loss through the employment of only one AMF strain. Even though we did not observe a reduction in AMF diversity (Supplementary Table 16 ), future studies need to investigate the long-term effects of inoculations, as well as the persistence and invasiveness of native vs exotic AMF inocula. The unintended consequences of non-native inoculants in natural and agricultural systems are not known, but if inoculants are invasive, they may pose a threat to soil and plant biodiversity and ecosystem functioning 47 . Furthermore, complementary to more diverse and complex inocula, the possibility of AMF rotations—analogous to crop rotations—could also mitigate the risk of low-diversity microbial treatments on soil biodiversity.

The ability of AMF to protect plant roots from attack by soil-borne pathogens can be explained by various mechanisms including improved plant nutrient uptake and consequently plant health 48 , induced systemic resistance 49 , alteration of the root microbiome 50 and direct competition for root space 18 , 19 , 51 . In our study, several of these mechanisms of action probably occurred simultaneously. Our root microbiome data partly point to direct competition for root colonization. In fields with high MGR, pathogenic fungi were significantly less abundant in inoculated roots (Fig. 6 ). These included the previously identified important soil pathogens Olpidium and (potentially plant pathogenic) Trichosporon , as well as Cladosporium , Mycochaetophora , Pyrenochaeta and Vishniacozyma . Myrothecium and Fusarium , which were also identified as important predictors, could not be found in the root microbiome data, possibly because the molecular primers used for roots were specifically designed to target AMF 52 . Thus, general ITS (internal transcribed spacer) primers for the roots also need to be included in future studies to cover full fungal diversity.

Moreover, it was striking that there was no correlation between root colonization and plant growth response. Inoculation of the AMF strain SAF22 was the experimental factor, but inoculum success and how well the AMF strain established was not a good predictor. Instead, differences in its functions explained the variation in MGR. In contrast to the common interpretation where biofertilizers stimulate plant growth, here the interpretation is the other way around: abundant pathogenic soil fungi, which are present in ‘high-MGR’ fields, cause a growth reduction in the control treatment, while this otherwise negative effect is mitigated by the inoculated AMF. We believe this could be due to several reasons closely related to the many ways AMF can suppress pathogens. First, if AMF establish first and fast, this could prevent or reduce pathogen establishment. Second, a range of studies have shown that AMF can trigger induced systemic resistance 49 , 53 , 54 , 55 , and AMF may indirectly affect pathogens by altering the microbiome 50 . Time-resolved studies that follow the processes and mechanisms in the roots throughout the growing season are needed.

Several studies have shown that the abundance and activity of AMF are also explained by the bacterial microbiome 56 and pesticide application 57 , 58 . Further, differences in microclimatic conditions may be another factor contributing to differences in MGR. The inclusion of such factors may resolve even more of the unexplained variance. However, while field inoculations must be economically viable, simple and cost-effective prediction of inoculation success must also be possible. Predicting MGR based solely on sequencing soil fungal pathogens, for instance, would represent a simplified diagnostic approach. Here we present an initial list of pathogenic sOTUs that could be quantified directly in the field at the beginning of the growth season, with results being available within a few hours and at a reasonable cost using quantitative PCR or rapid sequencing 59 . Furthermore, automated and affordable microbial diagnostic assays could be developed (for example, Loop-mediated isothermal amplification). Subsequently, pathogen abundance can predict inoculation success.

With this work using 54 fields, we have shown that field inoculation with AMF can successfully be predicted and can give a yes/no recommendation with high accuracy of 80–83%; this means a successful prediction in 4 out of 5 fields. We have solved the context dependency for one maize variety in one geographic area. The approach presented here is easily transferable and further studies need to test different maize varieties, as their responsiveness to mycorrhiza can vary greatly 23 , 60 . The inclusion of a broad range of soil types and climatic zones will further extend the scope of the work. To maximize the potential of AMF for more sustainable agricultural production systems, future work needs to include settings with reduced use of agrochemicals. Furthermore, our approach can be used as a blueprint to predict inoculation success and resolve context dependency of other widely used biofertilizers including Rhizobium spp. or Bacillus amyloliquefaciens 61 .

With our results, we provide a crucial starting point for the development of a diagnostic tool using soil microbial indicators that can ultimately increase the reliability of field inoculations. As a result, AMF inoculations can become a powerful management option for microbiome engineering in arable land and thus an integral part of agricultural sustainability.

Field sites

The field inoculations were carried out in three consecutive years in a total of 54 maize fields in northern Switzerland. In 2018, 22 fields were inoculated between 23 April and 16 May. In 2019, 25 fields were sampled between 18 April and 7 June. In 2020, 12 fields were sampled between 22 April and 16 May. The exact GPS locations are available but are not provided here for confidentiality reasons. The farms were chosen on the basis of the farmers’ willingness to participate in this study and planned cultivation of maize for the respective growing season. Apart from inoculum and fertilizer application, the experimental sites were managed by the farmers according to Swiss standards of conventional farming 62 .

All fields were fertilized with N and potassium (K). Since it has previously been shown that MGR is negatively correlated with the fertilized amount of P 35 , a subset of the 2018 plots (see below) were additionally fertilized with P to further verify these results. The amount of N, K and P was calculated on the basis of the Principles of Agricultural Crop Fertilisation (PRIF) in Switzerland 62 , which gives recommendations on the amount of fertilizer to be applied based on the plant and its specific nutrient needs. The following granular fertilizers were used: N in the form of 24% ammonium nitrate (NH 4 NO 3 ), P as triple superphosphate (46% P 2 O 5 ) and K as 60% water-soluble potassium oxide (K 2 O). The correct amount of fertilizer that was going to be applied (20.1 g N, 8.2 g of P 2 O 5 and 22.1 g K 2 O per m 2 ) was filled into sealed bags.

Experimental setup

In 2018, a split plot design was used for practicality reasons. Each experimental field comprised 12 maize rows of 24 m length, with the spacing between two maize rows being 75 cm. Fertilizer types (NK and NPK) were randomly assigned to whole plots, and inoculum types (control and AMF) were randomly assigned to split plots within each whole plot. A total of 16 whole plots was installed in a square 2 × 8 design, each of them comprising an area of 13.5 m 2 (corresponding to 6 maize rows of 3 m length). Each whole plot contained an AMF and a control treatment, separated by two maize rows, resulting in eight replicates per treatment combination. In 2019 and 2020 a randomized complete block design was used with 8 blocks. It was ensured that there were at least three maize rows serving as a buffer zone between the first inoculated maize row and the edge of the field, to avoid edge effects.

Inoculation

The control (carrier substrate) and AMF inocula ( R. irregulare isolate SAF22) were produced in the greenhouse. Plantago lanceolata L. was planted in 7 l pots filled with an autoclaved soil:sand mixture (3:17 v/v) 35 and inoculated with SAF22 or no AMF (control). The pots were watered regularly and after 3 months, the watering was stopped and the pots dried out. The resulting mixture of sand, soil, roots and AM fungal spores was used to inoculate the fields.

The maize variety LG 30.222 (UFA) was chosen on the basis of its high responsiveness to SAF22 in a previous study 35 . In addition, in 2019, an inoculation trial with individual and combined inoculations of different AMF species ( R. irregulare SAF22, Funneliformis mosseae , Clareoideoglomus claroideum ) was carried out on a subset of 10 fields (Extended Data Fig. 10 ).

After sowing, inoculations were performed as soon as possible (after 2–7 d), except for fields F10, F16 and F17 (9–11 d) due to late notice by the farmer. In each plot, the farmers’ seeds were carefully removed and the seed furrow was dug out to ~15 cm deth and 15 cm width. The soil and the respective inoculum (control or AMF) were alternately filled back into the hole and mixed well. A stretch of 80 cm in a maize row was inoculated with 450 g of the respective inoculum, which corresponds to an inoculum concentration of ~5% (v/v). Seeds of the maize variety LG 30.222 (UFA) were placed back into the soil–inoculum mix in their former position and covered with soil. Within the inoculated stretch, five seeds were placed ~3–4 cm deep in the soil with a 15 cm spacing between them and loosely covered with soil. The seeds were coated with standard fungicides as well as the insecticide and bird repellent Mesurol, as this is common practice in conventional farming in Switzerland. We controlled for possible adverse effects of the fungicide coating on the AMF by using the same coating in all fields. To avoid contamination, all equipment was used only for either control or AMF inoculations, and control plots were set up before AMF plots.

Soil sampling and processing

Soil sampling took place before fertilization of the fields and was performed using a half-cylindrical gouge auger (Eijkelkamp; effective auger body 100 cm, Ø 3 cm). Twenty soil cores were mixed to form composite samples and kept cold during transportation back to the laboratory. Samples were stored at 4 °C for a maximum of 2 weeks before sieving to 2 mm. A subsample was stored frozen for DNA extraction.

A total of 52 soil analyses were carried out in the Environmental Analytics lab and Soil Biology lab at Agroscope as well as the LBU (laboratory for soil and environmental analytics) according to their standard protocols. All data are provided in Supplementary Table 1 .

Shortly before the farmer’s planned harvest, after ~4–5 months of plant growth, two plants from the centre of each of the eight plots per treatment and field (that is, 16 plants in total) were cut 10 cm above the soil surface and their fresh weight was determined. The plants were dried at 60 °C until they reached a constant weight. Dry plant biomass was used for the predictions as maize is mostly grown for silage in Switzerland. Both parameters are strongly correlated (rho = 0.73; Supplementary Fig. 5 ).

Roots were collected and thoroughly washed with water, cut into pieces of ~1–2 cm length and mixed well. Subsamples of the roots for DNA extraction were stored at −20 °C. For assessment of total root colonization by microscopy, roots were stored in 50% ethanol until staining.

General statistics and graphics

All statistical analyses described below were carried out in R (v.4.0.3) 63 and plots were created using the R packages ggplot2 (v.3.3.5) 64 , graphics (v.4.0.3) 63 or ggpubr (v.0.4.0) 65 . Inkscape (v.092) 66 was used to finalize Fig. 3 .

MGR was calculated as previously described 24 to evaluate the percentage change in maize biomass in AMF-inoculated plots in relation to the average biomass in control plots. The 25th and 75th quantiles of the MGR range were calculated and fields were grouped by MGR categories comprising low- (bottom 25%), medium- (intermediate 25%–75%) and high- (top 25%) MGR fields (Fig. 1 and Supplementary Table 1 ).

Differences in MGR between the subset of fields fertilized with and without phosphorus were assessed using a two-way analysis of variance (ANOVA) using the ANOVA function of the R package stats (v.4.0.3) 63 with the two grouping variables ‘field’ and ‘fertilizer’ and their interaction effect (Extended Data Fig. 1 ).

Analysis of soil predictors

To find pairwise correlations among all 52 measured soil parameters and MGR, Spearman rank correlations (corr.test function of the R package psych (v.2.1.9)) 67 were calculated and corrected for multiple testing using the Benjamini–Hochberg method 68 (Supplementary Table 2 ).

Further, we performed multiple linear regression analysis. To assess the most important predictors for MGR, a stepwise reduction of parameters had to be performed. Only parameters that were measured in all 54 fields were selected (Supplementary Table 1 ). First, strongly correlated parameters ( R < −0.8, R > 0.8) were assessed using the cor function in the R package stats (v.4.0.3) 63 , visualized in a heat map using the R packages reshape2 (v.1.4.4) 69 and ggplot2 (v.3.3.5) 65 (Extended Data Fig. 2 ), and subsequently reduced (Supplementary Table 3 ).

Further analyses were conducted to identify the most important predictors of MGR from this pool. Random forest analysis was performed using the R package randomForest (v.4.6-14) 29 and 1,000 trees. The importance of predictors was ranked on the basis of their IncNodePurity values (Supplementary Table 4 ). Stepwise model selection was performed using the function stepAIC of the R package MASS (v.7.3.54) 30 , including backward and forward selection. The selected predictors can be found in Supplementary Table 5 . To compare all possible models and identify the best model from this pool, the R package glmulti (v.1.0.8) 31 was used with exhaustive screening, the Akaike information criterion with correction for small sample sizes (aicc) and a maximum model size of 10 predictors (Supplementary Table 5 ). The combined output of these analyses was used as input for the final model selection (see below).

Principal component analysis was performed using the prcomp function in the R package stats (v.4.0.3) 63 . A biplot was created with the loading vectors corresponding to the 15 selected parameters of the glmulti, stepAIC and randomForest analyses described above (Fig. 3a ).

Soil microbiome sequencing

Samples for DNA extraction were stored at −20 °C. Details of DNA extraction, PCR, library preparation and sequencing have been previously described 28 . DNA was extracted from four subsamples from each field using the NucleoSpin soil kit (Macherey-Nagel) and ~250 mg of soil. The entire ITS region was amplified using primers ITS1F (5′-CTTGGTCATTTAGAGGAAGTAA-3′) 70 and ITS4 (5′-TCCTCCGCTTATTGATATGC-3′) 71 , employing a two-step PCR protocol. First, the ITS region was amplified from genomic DNA. A 5 Prime Hot Master Mix (Quantabio) with a total reaction volume of 20 μl containing 0.3% BSA and 500 nM of each primer was used. The PCR programme consisted of an initial denaturation step of 2 min at 94 °C, followed by 25 cycles of denaturation at 94 °C for 45 s, annealing at 55 °C for 1 min and elongation at 72 °C for 1 min, with a final elongation step of 10 min at 72 °C. Cleanup was followed by reversible solid-phase immobilization with SPRIselect beads (Beckman Coulter). In the second PCR step, barcoded ITS1F and ITS4 primers were used but without the addition of BSA. The same PCR programme was used, but with only 10 steps. DNA was quantified using Picogreen and pooled in equimolar ratios. Four libraries were prepared in the same way and sequenced using the PacBio single molecule real-time (SMRT) technology 72 . The raw data were converted to circular consensus sequences (min. passes = 5) and demultiplexed with SMRT software (v.9.0.0, Pacific Biosciences). The raw sequencing data are stored in the European Nucleotide Archive ( http://www.ebi.ac.uk/ena ) under accession number PRJEB53587 .

Root microbiome sequencing

The DNA from roots from each block was extracted separately according to ref. 72 with some modifications. After lyophilisation, roots were ground with glass beads (1 mm and 0.1 mm) in a tissue lyser (FastPrep-24) twice for 1 min at 6 m s −1 . The NucleoSpin soil kit (Macherey-Nagel) was used as before to extract DNA from the powdered roots (~50 mg) using buffer SL1. After quantification with AccuClear Ultra High Sensitivity dsDNA quantification kit (Biotium), DNA was diluted to 1 ng µl −1 . Samples from all the blocks for one treatment of one field were pooled using equal amounts.

We used primers that target AMF so that the community profiles included Glomeromycota besides Ascomycota and Basidiomycota taxa. A ~1.5-kb fragment was amplified using the wobble-containing variants 52 of the AMF-specific primers SSUmCf (5′-TATYGYTCTTNAACGAGGAATC-3′) and LSUmBr (5′-AACACTCGCAYAYATGYTAGA-3′), spanning part of the small ribosomal subunit, the entire ITS region and part of the large ribosomal subunit 73 . In contrast to the original paper, the PCR method was improved by adding Q-Solution (Qiagen) and by using touchdown PCR. The polymerase system was Phusion High-Fidelity DNA system (Thermo Scientific). Two-step PCR was used to prepare the library for sequencing: the first step amplified the target gene, the second PCR used primers with a barcode specific for each sample. Reactions of the first step were prepared in 20-µl volume with HF Phusion buffer, 500 nM of each primer, Q-Solution diluted 4 times and 2 ng of DNA. Cycling programme of the first PCR consisted of an initial denaturation at 98 °C for 3 min, 10 touchdown cycles (30 s at 98 °C, 45 s annealing with temperature starting from 65 °C and reducing to 55 °C with 1 °C less per cycle, 1 min at 72 °C), followed by 25 cycles of standard PCR (10 s at 98 °C, 30 s at 55 °C, 1 min at 72 °C) and a final elongation of 10 min at 72 °C. PCR products were cleaned up using solid-phase reversible immobilization SPRIselect beads (Beckman Coulter). Reactions for the second step were prepared in 30-µl volume with the same concentrations of barcoded primers but without Q-Solution and 5 µl of the PCR product from the first reaction. The cycling programme of the second step consisted of an initial denaturation of 2 min at 98 °C, 10 cycles (10 s at 98 °C, 30 s at 55 °C, 1 min at 72 °C), followed by 10 min final elongation. After final cleanup with SPRIselect beads, DNA was quantified with AccuClear Ultra High Sensitivity dsDNA quantification kit and pooled in equimolar fashion.

Negative controls did not result in any amplification. A positive control of the inoculated AMF was included to identify OTUs corresponding to R. irregulare SAF22 and identified 4 abundant and 3 rare variants of the ribosomal (r)RNA operon. The resulting amplicons were sequenced in three libraries using the PacBio SMRT technology. The circular consensus sequences are stored in the European Nucleotide Archive ( http://www.ebi.ac.uk/ena ) under accession number PRJEB56590 .

Bioinformatics

Samples for each library were analysed together to form one OTU table. Samples were demultiplexed with SMRT (v.9.0.0, Pacific Biosciences). Primer removal, quality filtering (maximum expected errors 2, minimum length 500 bp, discarded reads that match phiX), truncation (after 1,800 bp or at the first instance of a quality score <3), dereplication, denoising and chimaera removal were carried out using the R package dada2 (v.3.10) 74 . ASVs (amplicon sequence variants) were clustered by 97% similarity using the R package DECIPHER (v.2.16.1) 75 . A Bayesian classifier was used to assign the taxonomy with the UTAX reference dataset (utax_reference_dataset_10.05.2021.fasta) from the UNITE database 76 .

Analysis of soil microbiome predictors

The OTU and taxonomy tables as well as the sample data were imported into the R package phyloseq (v.1.36.0) 77 . OTUs with zero counts were removed and the four replicates of each sample were merged and the counts summed. All samples were rarefied to an even sampling depth using the smallest sample number (that is, 4,272 reads). The resulting OTU table can be found in Supplementary Table 6 . Rarefaction curves (rarecurve function in the R package vegan v.2.5-7) 78 were calculated to determine sufficient sampling depth.

Spearman rank correlations (corr.test function of the R package psych v.2.1.9) 67 were calculated for individual OTUs and MGR, and corrected for multiple testing using the Benjamini–Hochberg procedure 68 .

To filter the OTU table to a more reduced candidate set for model selection, three independent analyses were performed. An indicator species analysis was performed with low- and high-MGR fields (multipatt function in the R package indicspecies (v.1.7.9), function ‘r.g’, 999 permutations) 79 . Indicator OTUs with P < 0.1 were retained. A less stringent significance threshold of 0.1 was chosen to obtain a larger candidate set of 29 OTUs (Supplementary Table 7 ). Differential abundance of OTUs between low- and high-MGR fields was assessed using DESeq2 (v.1.30.1) 80 , and the Wald significance tests and parametric fitting. Using a significance threshold of 0.1 resulted in the selection of 18 OTUs (Supplementary Table 8 ). Random forest analysis (R package randomForest v.4.6-14) 29 was performed to identify the most important predictors of MGR. OTUs with IncNodePurity >30 are listed in Supplementary Table 9 . The combined results of these analyses produced a subset of 44 OTUs. For final model selection in combination with soil parameters, this subset was further reduced using glmulti (v.1.0.8) 31 with exhaustive screening of all possible models and the Akaike information criterion with correction for small sample sizes (aicc).

Automatic species assignment against the reference database often did not result in annotations at lower taxonomic levels. Therefore, the most important OTUs were additionally subjected to a BLAST search against the NCBI database (Supplementary Table 10 ).

Principal coordinate analysis (PCoA) was performed on the square-root-transformed OTUs on the basis of Bray–Curtis dissimilarities (vegdist function in the R package vegan v.2.5-7) 78 to investigate a possible year effect (Extended Data Fig. 3 ). Subsequently, to explore relationships between soil fungal community composition and MGR, partial distance-based redundancy analysis (dbRDA) was performed using the capscale function in the R package vegan (v.2.5-7) 78 , with the variable ‘Year’ as the condition that was partialled out. The loading vectors corresponding to the final set of 13 soil OTUs selected by the methods described above were added to the partial dbRDA plot (Fig. 3b ).

FUNGuild (v1.2) 81 was used to assess fungal guilds and group pathogen sOTUs (Supplementary Table 13 ).

Linear regression models

The lm function of the R package MASS (v.7.3-54) 30 was used to develop linear regression models. Violation of normality assumption was assessed using Ols_test_normality in the R package olsrr (v.0.5.3) 82 . The relative importance of each predictor in the models was evaluated using the package relaimpo (v.2.2-6) 83 (Fig. 5 ). For the correlation plots of summed high- and low-MGR OTUs and MGR, a linear regression model was developed using only the 15 soil parameters. Residuals were extracted using the residual function in the R package stats (v.4.0.3) 63 and plotted against OTU abundance.

Cross-validation of models

To cross-validate our models, we split the dataset into a training dataset (90% of the dataset) and a test dataset (10%) using the createDataPartition function of the R package caret (v.6.0-94) 84 . Since the ultimate goal is not to predict the exact value of MGR, a binary classification approach was chosen to test the accuracy of the model in predicting inoculation success. An MGR of 12.2% was chosen since this represented the lower limit for significant positive effects (‘yes’: positive growth effect, >12.2% MGR; ‘no’: neutral or negative growth effect, <12.2% MGR). The linear regression models were developed as described above using the test dataset. MGR values of the test dataset were predicted using the predict function of the R package car (v.3.1.0) 85 . The number of true positive, true negative, false positive and false negative predictions were assessed using the confusionMatrix function of the R package car (v.3.1.0). The mean accuracy was assessed over 1,000 iterations (randomly splitting the dataset into training and test data).

Root microbiome analysis

The OTU and taxonomy tables as well as sample data were imported into the R package phyloseq (v.1.36.0) 77 . OTUs with zero counts were removed. All samples were subsampled to an even sampling depth using the smallest sample number (that is, 1,660). The relative abundances at the phylum level were assessed and visualized in a bar chart (Supplementary Fig. 3 ). Rarefaction curves (rarecurve function in the R package vegan v.2.5-7) 78 were calculated to assess sufficient sampling depth (Supplementary Fig. 2 ). The rarefied root OTU table can be found in Supplementary Table 11 . For the visualization of the community composition at the genus level, the 15 most abundant genera were selected from the rarefied OTU table (Supplementary Fig. 3 ).

To investigate similarities of the native root microbiome between the MGR categories (that is, low, medium, high) and a possible year effect, control samples were selected from the OTU table. First, PCoA (cmdscale function in the R package stats (v.4.0.3)) 63 was performed on the root-transformed OTUs and on the basis of the Bray–Curtis dissimilarities (vegdist function in the R package vegan v.2.5-7) 78 and samples were coloured by year. Subsequently, partial dbRDA was performed using the capscale function in the R package vegan (v.2.5-7) 78 , with the variable ‘Year’ as the condition that was partialled out (Extended Data Fig. 6 ).

To evaluate the establishment success of the inoculated SAF22, PCoA was performed on control and inoculated samples, and results were coloured according to these two treatment categories (Extended Data Fig. 9 ). Further, OTUs corresponding to SAF22 (rOTU2, rOTU4, rOTU9, rOTU16, rOTU74, rOTU84, rOTU165) were summed and their relative abundances recorded for control and inoculated samples, as well as their differences (Fig. 3c and Supplementary Table 12 ).

To investigate whether shifts in community structure differed between low- and high-MGR fields, we performed a differential abundance analysis (that is, control vs inoculated) for low- and high-MGR fields separately. We used the R package DESeq2 (v.1.30.1) 80 , Wald significance tests, parametric fitting and a significance threshold of 0.1 (Fig. 6 , and Supplementary Tables 14 and 15 ).

Root colonization

Total root colonization by AMF was assessed using the magnified section method 86 . First, roots were cleared with KOH and stained with an ink–vinegar mixture 87 . Approximately 30 cm of roots, consisting of 1–2-cm-long pieces, were mounted on a microscope slide and 100 intersections per sample were counted. The intersection types included ‘negative’, ‘arbuscule’, ‘vesicle’ and ‘internal hypha’. Total root colonization was recorded as a percentage of all non-negative intersections (Fig. 3c and Supplementary Table 12 ).

Reporting summary

Further information on research design is available in the Nature Portfolio Reporting Summary linked to this article.

Data availability

The raw sequencing data are stored in the European Nucleotide Archive ( http://www.ebi.ac.uk/ena ) under accession numbers PRJEB53587 (soil microbiome) and PRJEB56590 (root microbiome). All other data are available in the supplementary material.

Code availability

All code and input files are available at https://github.com/PMI-Basel/Lutz_et_al_Predicting_crop_yield .

Change history

19 december 2023.

A Correction to this paper has been published: https://doi.org/10.1038/s41564-023-01577-7

Foley, J. A. et al. Solutions for a cultivated planet. Nature 478 , 337–342 (2011).

Article CAS PubMed Google Scholar

Foley, J. A. et al. Global consequences of land use. Science 309 , 570–574 (2005).

The State of Food Security and Nutrition in the World 2022 (FAO, 2022).

Bender, S. F., Wagg, C. & van der Heijden, M. G. A. An underground revolution: biodiversity and soil ecological engineering for agricultural sustainability. Trends Ecol. Evol. 31 , 440–452 (2016).

Article PubMed Google Scholar

Banerjee, S. & van der Heijden, M. G. A. Soil microbiomes and one health. Nat. Rev. Microbiol. 21 , 6–20 (2022).

Trivedi, P., Leach, J. E., Tringe, S. G., Sa, T. & Singh, B. K. Plant–microbiome interactions: from community assembly to plant health. Nat. Rev. Microbiol. 18 , 607–621 (2020).

Trivedi, P., Batista, B. D., Bazany, K. E. & Singh, B. K. Plant–microbiome interactions under a changing world: responses, consequences and perspectives. New Phytol. 234 , 1951–1959 (2022).

Walder, F. & van der Heijden, M. G. A. Regulation of resource exchange in the arbuscular mycorrhizal symbiosis. Nat. Plants 1 , 15159 (2015).

Lekberg, Y. & Koide, R. T. Is plant performance limited by abundance of arbuscular mycorrhizal fungi? A meta-analysis of studies published between 1988 and 2003. New Phytol. 168 , 189–204 (2005).

Hoeksema, J. D. et al. A meta-analysis of context-dependency in plant response to inoculation with mycorrhizal fungi. Ecol. Lett. 13 , 394–407 (2010).

Chaudhary, V. B. et al. MycoDB, a global database of plant response to mycorrhizal fungi. Sci. Data 3 , 160028 (2016).

Article CAS PubMed PubMed Central Google Scholar

Watts-Williams, S. J. & Cavagnaro, T. R. Nutrient interactions and arbuscular mycorrhizas: a meta-analysis of a mycorrhiza-defective mutant and wild-type tomato genotype pair. Plant Soil 384 , 79–92 (2014).

Article CAS Google Scholar

Cavagnaro, T. R., Bender, S. F., Asghari, H. R. & van der Heijden, M. G. A. The role of arbuscular mycorrhizas in reducing soil nutrient loss. Trends Plant Sci. 20 , 283–290 (2015).

Bender, S. F. et al. Symbiotic relationships between soil fungi and plants reduce N 2 O emissions from soil. ISME J. 8 , 1336–1345 (2013).

Article PubMed PubMed Central Google Scholar

Zhang, X., Wang, L., Ma, F. & Shan, D. Effects of arbuscular mycorrhizal fungi on N 2 O emissions from rice paddies. Water Air Soil Pollut. 226 , 222 (2015).

Article Google Scholar

Begum, N. et al. Improved drought tolerance by AMF inoculation in maize ( Zea mays ) involves physiological and biochemical implications. Plants 8 , 579 (2019).

Augé, R. M., Kubikova, E. & Moore, J. L. Foliar dehydration tolerance of mycorrhizal cowpea, soybean and bush bean. New Phytol. 151 , 535–541 (2001).

Newsham, K. K., Fitter, A. H. & Watkinson, A. R. Arbuscular mycorrhiza protect an annual grass from root pathogenic fungi in the field. J. Ecol. 83 , 991–1000 (1995).

Azcón-Aguilar, C., Jaizme-Vega, M. C. & Calvet, C. in Mycorrhizal Technology in Agriculture (eds Gianinazzi, S. et al.) 187–197 (Springer, 2002).

Jansa, J. et al. Diversity and structure of AMF communities as affected by tillage in a temperate soil. Mycorrhiza 12 , 225–234 (2002).

Verbruggen, E. et al. Positive effects of organic farming on below-ground mutualists: large-scale comparison of mycorrhizal fungal communities in agricultural soils. New Phytol. 186 , 968–979 (2010).

Loit, K. et al. The indigenous arbuscular mycorrhizal fungal colonisation potential in potato roots is affected by agricultural treatments. Agron. Res. 16 , 510–522 (2018).

Google Scholar

Zhang, S., Lehmann, A., Zheng, W., You, Z. & Rillig, M. C. Arbuscular mycorrhizal fungi increase grain yields: a meta-analysis. New Phytol. 222 , 543–555 (2019).

Köhl, L., Lukasiewicz, C. E. & van der Heijden, M. G. A. Establishment and effectiveness of inoculated arbuscular mycorrhizal fungi in agricultural soils. Plant Cell Environ. 39 , 136–146 (2016).

Klironomos, J. N. Variation in plant response to native and exotic arbuscular mycorrhizal fungi. Ecology 84 , 2292–2301 (2003).

van der Heijden, M. G. A. in Mycorrhizal Ecology Ecological Studies Vol 157 (eds van der Heijden, M. G. A. & Sanders, I. R.) 243–265 (Springer, 2002).

Salomon, M. J. et al. Global evaluation of commercial arbuscular mycorrhizal inoculants under greenhouse and field conditions. Appl. Soil Ecol. 169 , 104225 (2022).

Bodenhausen, N. et al. Predicting soil fungal communities from chemical and physical properties. J. Sustain. Agric. Environ. 2 , 225–237 (2023).

Liaw, A. & Wiener, M. Classification and regression by randomForest. R News 2 , 18–22 (2002).

Ripley, W. N. & Venables, B. D. Modern Applied Statistics with S (Springer, 2002).

Calcagno, V. & de Mazancourt, C. glmulti: an R package for easy automated model selection with (generalized) linear models. J. Stat. Softw. https://doi.org/10.18637/jss.v034.i12 (2010).

Sinclair, T. R. Challenges in breeding for yield increase for drought. Trends Plant Sci. 16 , 289–293 (2011).

Wittwer, R. A., Dorn, B., Jossi, W. & van der Heijden, M. G. A. Cover crops support ecological intensification of arable cropping systems. Sci. Rep. 7 , 41911 (2017).

Schmidt, J. E. & Gaudin, A. C. M. What is the agronomic potential of biofertilizers for maize? A meta-analysis. FEMS Microbiol. Ecol. https://doi.org/10.1093/femsec/fiy094 (2018).

Bender, S. F., Schlaeppi, K., Held, A. & van der Heijden, M. G. A. Establishment success and crop growth effects of an arbuscular mycorrhizal fungus inoculated into Swiss corn fields. Agric. Ecosyst. Environ. 273 , 13–24 (2019).

Hirte, J., Richner, W., Orth, B., Liebisch, F. & Flisch, R. Yield response to soil test phosphorus in Switzerland: pedoclimatic drivers of critical concentrations for optimal crop yields using multilevel modelling. Sci. Total Environ. 755 , 143453 (2021).

Ngatia, L. W. et al. Land use change affects soil organic carbon: an indicator of soil health. Environ. Health https://doi.org/10.5772/INTECHOPEN.95764 (2021).

Toda, M., Walder, F. & van der Heijden, M. G. A. Organic management and soil health promote nutrient use efficiency. J. Sustain. Agric. Environ. 2 , 215–224 (2023).

Bonanomi, G., Antignani, V., Capodilupo, M. & Scala, F. Identifying the characteristics of organic soil amendments that suppress soilborne plant diseases. Soil Biol. Biochem. 42 , 136–144 (2010).

Vida, C., de Vicente, A. & Cazorla, F. M. The role of organic amendments to soil for crop protection: induction of suppression of soilborne pathogens. Ann. Appl. Biol. 176 , 1–15 (2020).

Mozafar, A., Anken, T., Ruh, R. & Frossard, E. Tillage intensity, mycorrhizal and nonmycorrhizal fungi, and nutrient concentrations in maize, wheat, and canola. Agron. J. 92 , 1117–1124 (2000).

Agrios, G. N. Plant Pathology 5th edn (Elsevier, 2005).

Saira, M. et al. First report of Myrothecium verrucaria causing leaf spot of maize in Pakistan. Plant Dis. 101 , 633 (2017).

Mesterházy, Á., Lemmens, M. & Reid, L. M. Breeding for resistance to ear rots caused by Fusarium spp. in maize – a review. Plant Breed. 131 , 1–19 (2012).

Goswami, R. S. & Kistler, H. C. Heading for disaster: Fusarium graminearum on cereal crops. Mol. Plant Pathol. 5 , 515–525 (2004).

Colombo, A. L., Padovan, A. C. B. & Chaves, G. M. Current knowledge of Trichosporon spp. and trichosporonosis. Clin. Microbiol. Rev. 24 , 682–700 (2011).

Hart, M. M., Antunes, P. M., Chaudhary, V. B. & Abbott, L. K. Fungal inoculants in the field: is the reward greater than the risk? Funct. Ecol. 32 , 126–135 (2018).

van der Heijden, M. G. A. et al. The mycorrhizal contribution to plant productivity, plant nutrition and soil structure in experimental grassland. New Phytol. 172 , 739–752 (2006).

Cordier, C., Pozo, M. J., Barea, J. M., Gianinazzi, S. & Gianinazzi-Pearson, V. Cell defense responses associated with localized and systemic resistance to Phytophthora parasitica induced in tomato by an arbuscular mycorrhizal fungus. Mol. Plant Microbe Interact. 11 , 1017–1028 (2007).

Lareen, A., Burton, F. & Schäfer, P. Plant root-microbe communication in shaping root microbiomes. Plant Mol. Biol. 90 , 575–587 (2016).

Whipps, J. M. Prospects and limitations for mycorrhizas in biocontrol of root pathogens. Can. J. Bot. 82 , 1198–1227 (2004).

Schlaeppi, K. et al. High-resolution community profiling of arbuscular mycorrhizal fungi. New Phytol. 212 , 780–791 (2016).

Gerlach, N. et al. An integrated functional approach to dissect systemic responses in maize to arbuscular mycorrhizal symbiosis. Plant Cell Environ. 38 , 1591–1612 (2015).

Pozo, M. J. & Azcón-Aguilar, C. Unraveling mycorrhiza-induced resistance. Curr. Opin. Plant Biol. 10 , 393–398 (2007).

Pieterse, C. M. J. et al. Induced systemic resistance by beneficial microbes. Annu. Rev. Phytopathol. 52 , 347–375, (2014).

Svenningsen, N. B. et al. Suppression of the activity of arbuscular mycorrhizal fungi by the soil microbiota. ISME J. 12 , 1296–1307 (2018).

Riedo, J. et al. Widespread occurrence of pesticides in organically managed agricultural soils – the ghost of a conventional agricultural past? Environ. Sci. Technol. 55 , 2919–2928 (2021).

Edlinger, A. et al. Agricultural management and pesticide use reduce the functioning of beneficial plant symbionts. Nat. Ecol. Evol. 6 , 1145–1154 (2022).

Tedersoo, L., Albertsen, M., Anslan, S. & Callahan, B. Perspectives and benefits of high-throughput long-read sequencing in microbial ecology. Appl. Environ. Microbiol. 87 , e0062621 (2021).

Sawers, R. J. H. et al. Phosphorus acquisition efficiency in arbuscular mycorrhizal maize is correlated with the abundance of root-external hyphae and the accumulation of transcripts encoding PHT1 phosphate transporters. New Phytol. 214 , 632–643 (2017).

Chowdhury, S. P., Hartmann, A., Gao, X. W. & Borriss, R. Biocontrol mechanism by root-associated Bacillus amyloliquefaciens FZB42 – a review. Front. Microbiol. 6 , 780 (2015).

Richner, W., Bretscher, D., Menzi, H. & Prasuhn, V. Grundlagen für die Düngung landwirtschaftlicher Kulturen in der Schweiz. Agrarforsch. Schweiz 8 , 1–12 (2017).

R Core Team. R: A Language and Environment for Statistical Computing (R Foundation for Statistical Computing, 2020).

Villanueva, R. A. M. & Chen, Z. J. ggplot2: elegant graphics for data analysis (2nd edn). Measurement 17 , 160–167 (2019).

Kassambara, A. ggpubr:’ggplot2’ based publication ready plots. R package version 3.3.5 https://cran.r-project.org/package=ggpubr (2020).

Bah, T. Inkscape Guide to a Vector Drawing Program 3rd edn (Prentice Hall Press, 2011).

Revelle, W. Procedures for Personality and Psychological Research (Northwestern Univ., 2015).

Benjamini, Y. & Hochberg, Y. Controlling the false discovery rate: a practical and powerful approach to multiple testing. J. R. Stat. Soc. B 57 , 289–300 (1995).

Wickham, H. Reshaping data with the reshape package. J. Stat. Softw. https://doi.org/10.18637/jss.v021.i12 (2007).

Gardes, M. & Bruns, T. D. ITS primers with enhanced specificity for basidiomycetes-application to the identification of mycorrhizae and rusts. Mol. Ecol. 2 , 113–118 (1993).

White, T. J., Bruns, T., Lee, S. & Taylor, J. in PCR Protocols (eds Innis, M. A. et al.) 315–322 (Elsevier, 1990); https://doi.org/10.1016/B978-0-12-372180-8.50042-1

Bodenhausen, N. et al. Petunia - and Arabidopsis -specific root microbiota responses to phosphate supplementation. Phytobiomes J. 3 , 112–124 (2019).

Krüger, M., Krüger, C., Walker, C., Stockinger, H. & Schüßler, A. Phylogenetic reference data for systematics and phylotaxonomy of arbuscular mycorrhizal fungi from phylum to species level. New Phytol. 193 , 970–984 (2012).

Benjamin, J. et al. DADA2: high-resolution sample inference from Illumina amplicon data. Nat. Methods 13 , 581–583 (2016).

Wright, E. S. Using DECIPHER v2.0 to analyze big biological sequence data in R. R J. 8 , 352–359 (2016).

Nilsson, R. H. et al. The UNITE database for molecular identification of fungi: handling dark taxa and parallel taxonomic classifications. Nucleic Acids Res. 47 , D259–D264 (2019).

McMurdie, P. J. & Holmes, S. phyloseq: an R package for reproducible interactive analysis and graphics of microbiome census data. PLoS ONE 8 , e61217 (2013).

Oksanen, J. et al. vegan: An R package for community ecologists. R package version 2.5-7 https://cran.r-project.org/package=vegan (2020).

De Cáceres, M. & Legendre, P. Associations between species and groups of sites: indices and statistical inference. Ecology 90 , 3566–3574 (2009).

Love, M. I., Huber, W. & Anders, S. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol. 15 , 550 (2014).

Nguyen, N. H. et al. FUNGuild: an open annotation tool for parsing fungal community datasets by ecological guild. Fungal Ecol. 20 , 241–248 (2016).

Hebbali, A. olsrr: Tools for building OLS regression models. R package version 0.5.3 https://cran.r-project.org/package=olsrr (2020).

Grömping, U. Relative importance for linear regression in R: the package relaimpo. J. Stat. Softw. https://doi.org/10.18637/jss.v017.i01 (2007).

Hyndman, R. J. & Athanasopoulos, G. Forecasting: Principles and Practice Ch. 3.1 (OTexts, 2013).

Fox, J. & Weisberg, S. An R Companion to Applied Regression (SAGE Publications, 2018).

McGonigle, T. P., Miller, M. H., Evans, D. G., Fairchild, G. L. & Swan, J. A. A new method which gives an objective measure of colonization of roots by vesicular–arbuscular mycorrhizal fungi. New Phytol. 115 , 495–501 (1990).

Vierheilig, H., Coughlan, A. P., Wyss, U. & Piché, Y. Ink and vinegar, a simple staining technique for arbuscular–mycorrhizal fungi. Appl. Environ. Microbiol. 64 , 5004–5007 (1998).

Download references

Acknowledgements

This study was supported by the Gebert Rüf Foundation (grants GRS-072/17 to N.B., M.G.A.v.d.H. and K.S., and GRS-088/20 to M.G.A.v.d.H.) and an Implementation grant from the Swiss National Science Foundation (grant 40IN40_215832/1 to M.G.A.v.d.H., N.B. and K.S.). We thank the Functional Genomics Center Zurich, the Next Generation Sequencing Platform (NGSP) at the University of Bern and the Genetic Diversity Centre at ETH Zurich for generating the sequencing data; our technicians A. Bonvicini and S. Mueller from Agroscope for the analysis of the microbial respiration and biomass data; and our students A. Ötnü, M. Diener and L. Brülisauer for help with acquiring the root colonization data.

Author information

Gabriel Deslandes-Hérold

Present address: Plant Biochemistry, Institute of Molecular Plant Biology, ETH Zurich, Zurich, Switzerland

These authors contributed equally: Stefanie Lutz, Natacha Bodenhausen. These authors jointly supervised this work: Klaus Schlaeppi, Marcel G. A. van der Heijden.

Authors and Affiliations

Plant–Soil Interactions, Department of Agroecology and Environment, Agroscope, Zurich, Switzerland

Stefanie Lutz, Julia Hess, Alain Valzano-Held & Marcel G. A. van der Heijden

Department of Soil Sciences, Research Institute of Organic Agriculture (FiBL), Frick, Switzerland

Natacha Bodenhausen

Plant Microbe Interactions, Department of Environmental Sciences, University of Basel, Basel, Switzerland

Jan Waelchli, Gabriel Deslandes-Hérold & Klaus Schlaeppi

Institute of Plant Sciences, University of Bern, Bern, Switzerland

Department of Plant and Microbial Biology, University of Zürich, Zurich, Switzerland

Marcel G. A. van der Heijden

You can also search for this author in PubMed Google Scholar

Contributions

N.B., K.S. and M.G.A.v.d.H. conceived the study and acquired funding; S.L. performed the data analysis with contributions from N.B. and wrote the manuscript with major inputs from N.B., K.S. and M.G.A.v.d.H.; J.H. and N.B. performed the field inoculation trials; J.H. coordinated the soil analyses; A.V.-H. and G.D.-H. carried out DNA extractions and prepared samples for sequencing; J.W. processed sequencing data; all authors reviewed the draft and gave final approval.

Corresponding authors

Correspondence to Klaus Schlaeppi or Marcel G. A. van der Heijden .

Ethics declarations

Competing interests.

The authors declare no competing interests.

Peer review

Peer review information.

Nature Microbiology thanks Debatosh Das, Peer Schenk and Zhong Wei for their contribution to the peer review of this work.

Additional information

Publisher’s note Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Extended data

Extended data fig. 1 fertilisation trial with and without phosphorus..

All fields were fertilised with nitrogen (N) and potassium (K). In a subset of the fields (18 fields in 2018) we also tested whether phosphorus (P) fertilisation influenced inoculation success. Fertilisation alone had no significant effect on MGR (p = 0.3680); yet, we examined a negative interaction effect of field and fertiliser (p = 0.0001). In three fields, inoculation did not have the same effect in the presence and absence of P fertiliser, and MGR was lower in the presence of additional P (highlighted by a bold rectangle; F17: p = 0.0033, F21: p = 0.0352, F10: p = 0.0760). Fertiliser types: NK = nitrogen + potassium, NPK: nitrogen + phosphorus + potassium. The boxes represent the interquartile range (IQR, 25th to 75th percentile). The horizontal line within the box represents the median (50th percentile). The whiskers represent the minima and maxima of the data in comparison to the IQR (±1.5*IQR). Outliers are represented as individual data points.

Extended Data Fig. 2 Correlation matrix of soil parameters.

Matrix shows Spearman rank correlations between all 38 soil variables for which data were available for all 54 fields.

Extended Data Fig. 3 Soil fungal communities group by year.

PCoA was performed on the square root transformed sOTUs based on Bray-Curtis dissimilarities. Plot shows an underlying year effect in the soil fungal data.

Extended Data Fig. 4 Relative abundance of sOTUs associated with low MGR across fields.

The relative abundance of OTUs was standardised using z-transformation for better visualization (primary y-axis). MGR is displayed in grey bars on the secondary y-axis and fields are arranged in descending order of MGR. The plot shows that on average only one or two of these OTUs were abundant in a field with low MGR. Full information on taxa identities can be found in Supplementary Table 10 .

Extended Data Fig. 5 Relationship between the establishment of AMF and MGR.

The relative abundance of the inoculated SAF22 was analysed using long-read sequencing. Total root colonisation was determined by microscopy. The values for the relative abundance of SAF22 and total root colonisation represent the differences between inoculated and control plants (Δ in the plots). No correlations were found between MGR and the relative abundance of sequenced SAF22 rOTUS (A) or total root colonisation (B). However, the relative abundance of SAF22 and total root colonisation were positively correlated (C). The correlation coefficients (Spearman rank, rho) and the significant values (p) are displayed in the plots. The blue shaded area represents the 95% confidence interval.

Extended Data Fig. 6 Ordination plots of native root fungal communities.

In order to explore a possible year effect and the relationship between the overall community composition and MGR, ordinations were performed on the control samples. The principal coordinate analysis on the left shows only weak grouping by year. Similarly, the partial distance-based redundancy analysis, after partialling out the effect of the variable year, only shows weak grouping by the response variable MGR. Ordinations were performed on the square root transformed rOTUs based on Bray-Curtis dissimilarities.

Extended Data Fig. 7 Ordination of control and inoculated root microbiome.

The principal coordinate analysis shows clear separation between the control and inoculated samples, indicating that the inoculated SAF22 established well in most fields (see Supplementary Table 12 for relative abundance values of each field), and thus, causing a shift in the root microbiome. Ordination was performed on the square root transformed OTUs based on Bray-Curtis dissimilarities.

Extended Data Fig. 8 Significant correlations of soil parameters with the most important sOTU associated with high MGR.

sOTU18 (Trichosporon sp.) showed the highest relative importance in the MGR prediction model. Its abundance correlates strongly with properties of poor soils (that is, lower organic carbon and nutrient contents and higher sand fraction). The correlation coefficients (Spearman rank) and the significant values (p) are displayed in the plots The blue shaded area represents the 95% confidence interval.

Extended Data Fig. 9 Scatter plots of significant correlations of soil physico-chemical variables with the most important indicator OTU for low MGR.

OTU58 (no database match) correlates significantly with properties indicative of healthy soils (that is, high respiration, fertility and organic carbon). The correlation coefficients (Spearman rank) and the significant values (p) are displayed in the plots. The blue shaded area represents the 95% confidence interval.

Extended Data Fig. 10 Inoculation trial with different AMF species.

Individual and combined inoculations of different AMF species did not result in any significant differences in MGR between species (p = 0.2006, F = 1.51) or significant interactions between fields and different species (p = 0.4124, F = 1.04,), as revealed by a 2-wy ANOVA (n = 8 individual plots per treatment group). The boxes represent the interquartile range (IQR, 25th to 75th percentile). The horizontal line within the box represents the median (50th percentile). The whiskers represent the minima and maxima of the data in comparison to the IQR (±1.5*IQR). Outliers are represented as individual data points.

Supplementary information

Supplementary information.

Supplementary Figs. 1–5; Tables 2–5, 7–10, 12, 14–16; and Results and Discussion.

Reporting Summary

Supplementary tables.

Supplementary Tables 1, 6, 11, 13.

Rights and permissions

Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/ .

Reprints and permissions

About this article

Cite this article.

Lutz, S., Bodenhausen, N., Hess, J. et al. Soil microbiome indicators can predict crop growth response to large-scale inoculation with arbuscular mycorrhizal fungi. Nat Microbiol 8 , 2277–2289 (2023). https://doi.org/10.1038/s41564-023-01520-w

Download citation

Received : 16 January 2023

Accepted : 11 October 2023

Published : 29 November 2023

Issue Date : December 2023

DOI : https://doi.org/10.1038/s41564-023-01520-w

Share this article

Anyone you share the following link with will be able to read this content:

Sorry, a shareable link is not currently available for this article.

Provided by the Springer Nature SharedIt content-sharing initiative

This article is cited by

Bacteria associated with spores of arbuscular mycorrhizal fungi improve the effectiveness of fungal inocula for red raspberry biotization.

Rafał Ważny
Roman J. Jędrzejczyk
Katarzyna Turnau

Microbial Ecology (2024)

Quick links

Explore articles by subject
Guide to authors
Editorial policies

REVIEW article

Common mycorrhizae network: a review of the theories and mechanisms behind underground interactions.

$\nAline Fernandes Figueiredo$

Institute of Soil Science, Leibniz Universität Hannover, Hannover, Germany

Most terrestrial plants establish symbiotic associations with mycorrhizal fungi for accessing essential plant nutrients. Mycorrhizal fungi have been frequently reported to interconnect plants via a common mycelial network (CMN), in which nutrients and signaling compounds can be exchanged between the connected plants. Several studies have been performed to demonstrate the potential effects of the CMN mediating resource transfer and its importance for plant fitness. Due to several contrasting results, different theories have been developed to predict benefits or disadvantages for host plants involved in the network and how it might affect plant communities. However, the importance of the mycelium connections for resources translocation compared to other indirect pathways, such as leakage of fungi hyphae and subsequent uptake by neighboring plant roots, is hard to distinguish and quantify. If resources can be translocated via mycelial connections in significant amounts that could affect plant fitness, it would represent an important tactic for plants co-existence and it could shape community composition and dynamics. Here, we report and critically discuss the most recent findings on studies aiming to evaluate and quantify resources translocation between plants sharing a CMN and predict the pattern that drives the movement of such resources into the CMN. We aim to point gaps and define open questions to guide upcoming studies in the area for a prospect better understanding of possible plant-to-plant interactions via CMN and its effect in shaping plants communities. We also propose new experiment set-ups and technologies that could be used to improve previous experiments. For example, the use of mutant lines plants with manipulation of genes involved in the symbiotic associations, coupled with labeling techniques to track resources translocation between connected plants, could provide a more accurate idea about resource allocation and plant physiological responses that are truly accountable to CMN.

Mycorrhiza Network: Theoretical Background

Mutualistic associations between mycorrhizal fungi and plants are well-known. Within the diverse mycorrihza types, the arbuscular mycorrhizae (AM), from the phylum Glomeromycota, is one of the most common, ancient and widespread, associating with around 80% of all land plant species ( Schüßler and Walker, 2011 ). This fungi type is more predominant in warm climates and species rich ecosystems, such as tropical forests. The second most common fungi type in nature is the ectomycorrhizal (EM) fungi. Although a lower number of plant species have been found to form symbiosis with EM, in comparison to AM, the hosts of EM tend to be widely dispersed, abundant and dominant members of their groups ( Brundrett, 2009 ; Teste et al., 2020 ). Different from AM, EM fungi are mainly found in colder regions and ecosystems, where less host species are present, e.g., temperate and boreal forests ( Brundrett, 2009 ; Gorzelak et al., 2015 ). AM and EM networks are assumed to differ in their structure, but both affect plant responses, such as growth, photosynthesis rate, nutrition, survival, and others ( Gorzelak et al., 2015 ). Besides, AM and EM fungi species are frequently found co-existing in the same ecosystem. Some exceptional plants are even able to host both types of fungi in its roots, although the proportion of the association with each may differ along plant's life ( Gorzelak et al., 2015 ).

Mycorrhizae fungi are widely recognized to improve plant nutrition by being able to access soil spaces and nutrient sources inaccessible for roots ( Smith and Read, 2010 , Wipf et al., 2019 ; Andrino et al., 2021 ). The great majority of mycorrhizae fungi are not host specific, being that a single mycorrhizae fungi specie is able to colonize a wide range of plant species. Once a fungi colonize the host plant, its mycelium is able to grow over large distances in the soil and may reach and colonize the roots of multiple neighboring plants, from the same or different species ( Van Der Heijden and Horton, 2009 ). Therefore, plants sharing the same host fungi are reported to become interconnected by the so-called common mycorrhiza network (CMN) ( Heaton et al., 2012 ; Rhodes, 2017 ; Wipf et al., 2019 ). Connectivity are therefore likely to occur between plants able to associate with the same fungi species.

As ecosystems are usually dominated by mycorrhizal plants, including most temperate and tropical grasslands as well as boreal, temperate and tropical forests ( Read, 1991 ; Van Der Heijden, 2016 ), abundant and extensive mycorrhizal fungal networks are formed ( Wipf et al., 2019 ). It is believed that plant species can interact and communicate via these CMNs ( Gorzelak et al., 2015 ; Pickles et al., 2017 ; He et al., 2019 ). This may affect survival and behavior of connected plants as well as competitive and cooperative patterns, consequently influencing plant diversity at local and regional scales ( Deslippe and Simard, 2011 ; Simard et al., 2012 ; Bücking et al., 2016 ). Among the reported effects of such connectivity are the improvement of seedling establishment ( Bingham and Simard, 2011 ; Seiwa et al., 2020 ), impact on plant and microorganism community compositions ( Meng et al., 2015 ; Teste et al., 2015 ; Kadowaki et al., 2018 ), induction of plant defense responses ( Babikova et al., 2013 ; Song et al., 2014 ), plant communication through a variety of phytohormones such as jasmonic acid, methyl jasmonate and zeatin riboside ( Song et al., 2010 ), and nutrient exchange, which may play a pivotal role for interplant nutrition ( Bücking et al., 2016 ; He et al., 2019 ; Fang et al., 2021 ).

In the review made by Van Der Heijden and Horton (2009) it is stated that CMN can be compared either to “socialist” or “capitalist” systems, or even to a “superorganism.” For the “socialist” behavior, individuals are able to have equal opportunities and resources are distributed more evenly providing benefits for all connected plants. For the “capitalist” network, mycorrhizal would be privately controlled for the profit of certain group of plants, increasing therefore competition between connected plants. If network behaves as a “superorganism,” fungal species in the network are considered redundant physical extensions of the roots, which might translocate nutrients freely between plants. Therefore, the mode of interplant connection might have evolutionary consequences of CMN by substantially defining the community ecology of a site, leading to ecosystem-wide impacts ( Gorzelak et al., 2015 ). This depends largely on which of these responses are predominant (“socialist,” “capitalist,” or simple physical extensions) in the moment plants are connected; together with the question whether these responses may change if plants from the same or from different species are connected.

In face of all the possible effects of CMN on plant interactions, many different theories have been raised with the intention to predict how mutual association and co-existence of species in the system is stabilized. By one hand, we have the biological market theory, for example, which is based on the assumption that fungi might recognized the best plant partner and re-allocate nutrient accordingly to its carbon (C) gain. On the other hand, we have the source-sink theory in which resource would move in a concentration gradient. This could lead resources to be distributed more equally among partner involved in the network, which is the opposite of what is expected if the biological market is driven resource allocations. Both theories will be more detailed discussed in the following sections. Nevertheless, benefits and disadvantages from the interactions between connected plants are hard to distinguish in nature, once most of the plants are colonized simultaneously by multiple fungal species, each one with its own cost–benefit. In addition, in natural ecosystems, not only mutualistic interaction between connected mycorrhizal plants takes place, but networks may also include commensalistic and even antagonistic interactions ( Toju et al., 2013 ). Therefore, some plant species might benefit from CMN more than others, depending on the fungi and plants involved in the association. It is important to note that, even if plants would be connected mainly by a single mycorrhiza type, i.e., AM fungi, variations in the functional properties and temporal patterns of different strains can also be observed ( Kiers et al., 2011 ). This adds further complexity to the potential mechanisms by which such network would determine plant community composition and productivity through their facilitative and antagonistic effects on plants ( Wagg et al., 2015 ). Therefore, predicting ecosystem dynamics of connected plants is still a huge challenge.

Due to the high complexity to discriminate effects of CMN in natural ecosystem, the majority of studies aimed to evaluate the influence of CMN for connected plants were mainly performed with few species of plants growing in pairs in microcosms and under controlled environmental conditions. Even under such controlled situation, the outcomes may still vary significantly, once benefits of connected plants may change according to host's physiological status, plants and fungal species involved, environment conditions, nutrient availability, etc. ( Wagg et al., 2011 ). With this in mind, it is necessary to assess the most recent findings in literature and define still open questions, in order to guide upcoming studies in the area aimed to have a better understanding of possible plant-to-plant interactions via CMN and its effect shaping plants community. The present paper therefore evaluates results and theories of the functionality of CMN for plant-to-plant communication, especially, for resource exchange. Here, we also point the gaps of such studies in order to highlight especial points that need to be address in further studies.

Source Sink Theory

In the source-sink model, the source is defined as the entity that can produce more of a given resource than it uses and the sink as the entity that has the potential/necessity to use more of a given resource than it produces ( Heaton et al., 2012 ). The primary importance of plant–sink strength in governing the magnitude and direction of resource transfer through CMNs is illustrated in studies showing transfer of C to rapidly growing young EM trees with high transpiration rates, or to shaded seedlings with high respiration demands, increasing its survival and growth ( Lekberg et al., 2010 ; Philip et al., 2010 ). Similarly, transfer of other resources, such as nitrogen (N), were also reported following a source-sink pattern ( Montesinos-Navarro et al., 2017 ; Muneer et al., 2020 ). This mechanism has been proposed to increase the regenerative capacity of forest ecosystems ( Teste et al., 2009 , 2010 ). However, there are also reports of reduced transfer of C within a CMN to sink (shaded, defoliated, seedling) plants ( Kytöviita et al., 2003 ; Walder et al., 2012 ), and even C transfer from sink (shaded) plants to source plants ( Deslippe and Simard, 2011 ). Thus, a better understanding of the forces driving such interactions is required, since it has profound implications for our understanding of plant communities and competition. Depending on the species involved in the CMN and the possible effects for its fitness, it will drive forest community composition and dynamics ( Beiler et al., 2010 ; Simard et al., 2015 ).

Biological Market Theory

Asymmetry on resource allocation has been also demonstrated to increase competition between connected species ( Merrild et al., 2013 ; Weremijewicz et al., 2016 ). Merrild et al. (2013) found that the growth suppression of small neighboring plants was diminished by clipping the shoots of large plants, which also increased the P uptake by interconnected small neighbors 6.5-fold. In order to exclude that suppression was caused by a general negative growth response, treatments including solitary vs. networked seedling was performed. In the referred study, suppression occurs only when seedlings were linked to the extraradical mycelium (ERM) of the large plant. Therefore, the authors concluded that the observed effects could solely be attributable to the CMN effect. However, such results has to be interpreted carefully, since inherent characteristics of plant species involved, such as growth rate, size, and root:shoot ratio, are likely to influence observed nutrient uptake.

Nevertheless, based on the observed results, an alternative theory has been proposed to elucidate such effects, the biological market theory. This theory is based on the assumption that both, plant and fungi, are able to detect variation in quality and amount of the resource supplied by their partner, allowing them to adjust their own resource allocation according to its gains ( Kiers et al., 2011 ; Walder and van der Heijden, 2015 ; Werner and Kiers, 2015 ; Wang et al., 2019 ). Kiers et al. (2011) used molecular markers and stable isotope probing to track C flow from Medicago truncatula hosts into fungal RNA of roots colonized by mixed AM fungal communities with different cooperative behavior to the host plant. The authors found greater C enrichment in the most beneficial fungal species, suggesting a preferential allocation of C by the host, operating in a small spatial scale. The opposite flux was also observed, in which the fungi delivered more P for the host, which provided more C to fungi. Fellbaum et al. (2014) also evidenced fungal discrimination by greater N allocation to the host under elevated C allocation. If “rewards” indeed are reciprocal between mycorrhizal fungi and host plants, larger plants are supposed to obtain larger amounts of limiting nutrients by the fungal networks once they can produce and allocate much more C to the fungal partner. Increasing competition and suppressing growth of smaller individuals thus makes CMN a stronghold to avoid outcompeting its own kind.

It is important to note that the market theory proposed by some authors goes in an opposite direction to what was stated in the “source-sink” theory presented above. Neither theory should be defined as an universal framework to explain resource exchange in the mycorrhizal association nor predict plant interactions within a CMN, since the outcome of such interactions may vary with environmental conditions, functional diversity, competition for surplus resources, reciprocity and sink strength. Therefore, the effect of each variable should be tested separately and considered into the proposed models in order to define a more universal framework.

Underground Connectivity

Both the source-sink theory and the market theory relies on the prerequisite of an underground connectivity of plants via CMN. In general, ecologists agree on the definition of CMN as a physical linkage among plants via the mycelia of the mycorrhiza fungi and that this linkage is common in nature ( Simard and Durall, 2004 ; Simard et al., 2012 ; Hoeksema, 2015 ). However, this premise comes from observations that species of AM fungi are often compatible with multiple host plant species. In addition, Giovannetti et al. (2001) have demonstrated the ability of genetically compatible hyphae to anastomose (fusion), with disappearance of hyphal walls and exchange of cytoplasm and nuclei ( Barreto de Novais et al., 2017 ). Both findings suggesting that CMNs are probably ubiquitous, although confirmation of such assumption still requires direct evidence for these linkages in the field. In this context, plants of same and different species have been reported sharing same fungi species or even same genet in several ecosystems ( Simard et al., 2012 ; Beiler et al., 2015 ). Some authors have estimated the potential of plants to become interconnected by evaluating the similarity between mycorrhizal community composition, assuming a greater similarity when plants are connected through a CMN ( Beiler et al., 2010 ; Diédhiou et al., 2010 ). ( Beiler et al., 2010 ), for example, evaluated the distribution of genets of two species of ECM fungi ( Rhizopogon vesiculosus and R. vinicolor ) among roots of individual trees of Interior Douglas-fir ( Pseudotsuga menziesii ) as a network link. The authors proposed a model where trees of different ages were connected in a scale-free architecture and the larger trees served as hubs of nutrition, favoring understory regeneration, and functional continuity in the stand.

These achievements were of great importance to demonstrate the complexity of the CMN and the number and diversity of individuals that are potentially linked, resulting in a multitude of interactions involving multiple generations. However, sharing compatible species or even the same genets, does not necessarily indicate a direct connection among the host plants. Collembolas, for example, are known to feed on fungal hyphae. Such as AM fungi, they are widespread and abundant in the soil ( Ekblad et al., 2013 ; Ngosong et al., 2014 ). By grazing the hyphae of a genet connecting two or more plants, this genet can still be identified in the roots of those plants although they would no longer be connected ( Rotheray et al., 2008 ; Beiler et al., 2010 ). This is one of the examples of CMN disruption that could occur in the soil, and would be hard to identify ( Wu et al., 2005 ; Beiler et al., 2015 ). Consequently, technical difficulties in proving hyphal connections between plants are the main obstacle when identifying whether any observed effect is really an intrinsic property of a CMN.

Therefore, it is also important to prove the extent and continuity of the mycelial network, together with mechanisms driving such connections and its consequences for plant fitness. In this context, there are few non-destructive methods for mycelium network observation, especially for AM fungi, mostly by the use of root observation chambers ( Mikkelsen et al., 2008 ; Gyuricza et al., 2010 ) and in vitro dual systems ( Kiers et al., 2011 ; Van't Padje et al., 2021 ). Such studies have nicely demonstrated the architecture of the extraradical mycelium of the fungi connecting two neighboring plants, but yet the relative importance of such network under realistic conditions is frequently under debate. For experiments developed in the forest, many interferences are found and the effects and mechanisms involved in the CMN cannot be excluded from other effects, such as positive and negative plant-soil feedback due to modulation of soil microbiota and biogeochemical cycles or even by production of roots exudates that might affect growth of nearby plants ( Hu et al., 2018 ). Therefore, mycorrhizae studies still face challenges, raising questions if the data represents a natural situation, since there are no guarantees that evaluated effects are caused by mycorrhizae network.

Mechanisms Involved for Plant Interaction VIA CMN

Currently, the mechanisms that drive benefits and competitive interactions between plants involved into a CMN has been under debate (e.g., Fellbaum et al., 2012 ; Bücking et al., 2016 ), raising diverse theories about the mechanism in these associations. The first one is based on the assumption that established mycorrhizal plants would facilitate mycorrhization of neighboring seedlings, acting as an inoculum and C source. In this case, seedlings would be able to join a CMN, which were already stablished and supported, in terms of translocation of reduced C by the older plants. Thus, seedling would be able to get access to limiting nutrients provided by the fungi without contributing with C supply to maintain the network. The second mechanism is based on the idea that CMN will act as conduits for interplant nutrient transfer ( Gilbert and Johnson, 2017 ; Wipf et al., 2019 ). In this context, depending on how resources are distributed between connected plants, plants may either benefit by a more equilibrate distribution of resources or by increasing discrepancies of resources. In the first case, plants with higher nutritional conditions may donate excess of their resources to the receiver plants by a direct transfer. In the second case, resources might be distributed unequally favoring a certain group of individuals increasing therefore competitive interactions.

Inoculum Source and Carbon Provision

Firstly, CMN may provide an inoculum source. Association with hyphae from the CMN can be much faster in comparison to soil spore bank, by the provision of an already established fungal inoculum source by the mature tree, permitting seedlings to quickly tap into a large soil resource pool that they could not access by their own ( Bingham and Simard, 2012 ). Thus, this faster access to mycorrhizal services in the early plant stage, where mortality is high due to drought and biotic interactions, may be of critical importance, especially under harsh environmental conditions ( Simard et al., 2012 ; Teste et al., 2015 ). In the experiment developed by Varga and Kytöviita (2016 ), the proportion of colonized seedlings by three different AM fungi was strongly related to the fungal species as well as to the source of inoculum. Seedlings inoculate much faster from nearby mycorrhized plants than from spores, despite a high spore density. This premise is also supported by some field experiments showing a positive relationship between the survival rate of seedling and its distance from the mature tree ( McGuire, 2007 ; Grove et al., 2019 ). In addition, experiments involving barriers (e.g., mesh bags) or soil disturbance to manipulated seedling contact with CMN have shown higher seedling mortality when seedling are impeded to join the network ( Nara, 2006 ; Pec et al., 2020 ).

Secondly, seedling may benefit from sharing a CMN with adult established tree since adult trees might provide much more C to sustain the network while seedling invest very little C and still obtain nutrients provided by the fungi. The maintenance of fungal symbiosis can be costly, resulting in a high C demand by the fungi for its development and activity ( Smith and Read, 2010 ; Keymer et al., 2017 ; Rezáčová et al., 2017 ). In this context, sugars and lipids are the main C source derived from host plants transported to the fungal symbiont. Those C derived components will provide the fungi with the energy necessary for nutrient acquisition and the C skeleton for mycorrhizal growth ( Bravo et al., 2017 ; Bezrutczyk et al., 2018 ). A benefit for seedlings would arise if larger trees pay the C cost required for the growth and maintenance of the CMN, so seedlings could potentially become mycorrhized and receive the benefits of this association without expending their own C for this ( Diédhiou et al., 2010 ; Walder et al., 2012 ; Weremijewicz et al., 2016 ). In the study made by Högberg et al. (1999 ), for example, EM fungi connecting overstory pine trees with understory plants of different ages received 87–100% of their C from overstory trees and very little from understory trees. Walder et al. (2012) have shown a similar asymmetric pattern by using 13 C of natural abundances between C 3 and C 4 plants without disturbing the system. The authors found that the C 4 plant, which had the higher biomass, was invested more C to both fungal partner than the C 3 plant but did not have a higher nutritional benefit. In this context, nutritional benefit strongly depended on the fungus involved in the CMN, in which Rhizophagus irregularis allocated nutrients preferentially to the C 3 host plant while the CMN formed by Glomus mosseae were more balanced with respect to the nutrient allocation to both, C 3 and C 4 , host plants. This demonstrate that C investment and nutritional benefit are not necessarily tightly linked and that some plant species can receive disproportional benefits from CMN. It is important to note that these experiments indicate that disproportional C investment by one plant does not necessarily mean a disadvantage for the other plant, especially when the cost of C is negligible for the main C donor.

Mycorrhiza Network as Conduits for Interplant Resources Transfer

The premise of a possible nutrient transfer through a physical connection established by CMN may be of great importance in agricultural, where redistribution of symbiotic costs and benefits between individuals of the same or different plant species could increase growth of connected plants and therefore reduce amounts of chemical fertilizer input ( Pena et al., 2013 ; Jansa et al., 2019 ). However, if a direct transfer of photoassimilates and nutrients between plants occurs via CMN is particularly controversially discussed ( Bever et al., 2010 ; Courty et al., 2010 ). Such transfers have been frequently reported in field and laboratory experiments using labeling compounds to trace the fate of nutrients in plants connect by a CMN, trying to demonstrate belowground resource transfer between plants of same and different species is facilitated by mycorrhizal fungi ( Teste et al., 2009 ; Deslippe and Simard, 2011 ; He et al., 2019 ; Fernandez et al., 2020 ).

In earlier studies, this mechanism was mainly observed in mycoheterotrophic plants, which are partly or entirely non-photosynthetic and indirectly parasitize green plants via CMN. These non-photosynthetic plants, also called epiparasites, associate with AM fungi emanating from the roots of surrounding green plants, therefore having access to C provided by those plants, together with other resources ( Bidartondo et al., 2002 ; Girlanda et al., 2006 ; Selosse and Roy, 2009 ). In addition to mycoheterotrophic plants, some green orchids or small green perennial shrubs from the Ericaceae family have also been shown to receive considerable amounts of C from their mycorrhizal fungi ( Selosse and Roy, 2009 ; Selosse et al., 2016 ). Those studies have raised the attention for the existence of a network where unrelated plants are able to transfer elemental compounds via shared fungal symbionts.

The mycorrhizal fungi which associates with mycoheterotrophic plants and green orchids usually belong to a diverse fungal taxa that also form mycorrhizae association with phototrophic tree roots ( Zimmer et al., 2008 ; Waterman et al., 2013 ; Brundrett and Tedersoo, 2018 ). Since C transfer were observed between mycoheterotrophic and green plants and the same fungi species connecting those plants can also colonize several phototrophic trees, theories were raised regarding the possible C allocation between phototrophic trees as well. If such networks could act as a direct pathway of C and nutrients between green plants, this could play an important role for plant to plant interactions ( Selosse and Roy, 2009 ; Smith and Read, 2010 ). Once C is an important resource for fungi growth, C allocation between plants would go to an opposite direction of the natural C flux commonly accepted in the symbiosis, which is from plant to fungi. In this case, one of the host plants would provide fungi with C and the fungi would not incorporate but channel this C through a neighboring plant. Some researchers believe that it might happen when networking fungus can acquire more C than it is required for its own fitness, therefore it may supply the excess to other plants in need ( Gorzelak et al., 2015 ; Prescott et al., 2020 ). This has been suggested as a mechanism from the fungi to ensure survival of its host plants and therefore its access to multiple C supply, in case of a potential loss of one of the hosts ( Gorzelak et al., 2015 ; Bücking et al., 2016 ). Some authors raised this theorem by using experiments involving high and low quality plants connected into a CMN ( Kiers et al., 2011 ; Fellbaum et al., 2014 ; Bücking et al., 2016 ). In this context, the quality of a host is determined by its C investment into the mycorrhiza, in which low quality hosts have a reduced investment while high quality host can produce and allocate higher amounts of C to fungi partner. In previous studies, shading have been frequently used to reduce the plant's ability to produce C compounds to be exchanged by limiting nutrients. In such experiments, although a discrimination between plants was observed leading to higher resources (such as N and P) allocation to high quality host of the network, the fungi also transferred nutrients for the low quality host and maintained a high colonization rate in these plants ( Kiers et al., 2011 ; Fellbaum et al., 2014 ; Bücking et al., 2016 ). Those mechanisms shows a possible strategy from the fungi in maintaining both high and low quality host into the network, to ensure that the possible loss of a high quality host is not harmful for its survival. This might be an important mechanism for fungi survival, especially under variable environments, as suggested first by Perry et al. (1989) and Wilkinson (1998) .

In this context, Simard et al. (1997a) was one of the first to demonstrate a bi-directional flux of C between two autotrophic plants, Douglas-fir ( P. menziesii ) and paper birch ( Betula papyrifera ) species, sharing an EM network. Here, a great amount of C was observed to be exchanged between the plant species, with no net gain for any one of them in the end. However, in the second year of study, Simard et al. (1997b) observed a net gain of C by one of the species independently of full, partial or deep shade light intensity. However, some methodological issues regarding the experimental design of this study was unraveled later by Robinson and Fitter (1999) , raising doubts regarding the ecological relevance of CMN-facilitated resource transfer. Simard et al. (1997b) used a double labeling technique ( 14 C and 13 C) to track C exchange between plants connected by an EM network in the field and calculate proportions of C received by each individual. However, not only EM connected plants received the applied C, but AM surrounding plants not connected to the network had access to labeled C too. That demonstrate that the movement of C between plants were not necessarily exclusively by mycorrhizal links, but could have reached neighboring plant by different pathways. This is especially likely to occur when no physical barriers are used in the experiments.

Robinson and Fitter (1999) also suggested that C transferred from neighboring photosynthetic active plant to hyphae within the roots of C-stressed plants is probably a strategy of the fungi for its own growth and survival, with minor consequences for plant communities. Teste et al. (2010) using a different experimental design also showed a low net C transfer between Douglas-fir seedlings in the field relative to total C uptake by photosynthesis. The significance of the amounts transferred have been repeatedly questioned in other works ( Teste et al., 2009 ; Philip et al., 2010 ; Pickles et al., 2017 ), raising a center debate on whether the extent of net transfer from one plant to another is sufficiently large to affect significantly plant fitness and predict communities' dynamics. In addition, there are also reports about the accumulation of C partially or entirely in mycorrhizal roots of receiver plants, probably in fungal tissues, and not detected on shoots even under situations where root to shoot C flow is encouraged by clipping or shadding ( Robinson and Fitter, 1999 ; Pfeffer et al., 2004 ; Lekberg et al., 2010 ). However, some authors argue that the movement of C to receiver plant, even without transfer into plant tissues, is still an important subsidy to meet the nutrient requirements of the plant, especially under stress conditions ( Bever et al., 2010 ; Teste et al., 2015 ).

Mycorrhizal networks have also been frequently reported to play an important role for belowground transfer of N among plants, but as for C different studies lead to contradicting results. Patterns of N transfer have been studied using natural abundance (δ 15 N) or 15 N-enriched techniques. For the 15 N-enriched techniques, fertilizer is applied directly to the growth media of the N donor root or directly to the N donor plant by exposure to 15 N 2 (in case of experiments using N-fixing bacteria as an additional symbiont to host plant) or foliar spray or petiole injection of labeled 15 N ( NH 4 + , NO 3 - , or urea). In early studies of several intercropping systems, a substantial one-way N transfer was demonstrated via a source-sink gradient from N 2 fixing plants to non-N 2 fixing plants, within a range of 20–50% ( He et al., 2009 ). However, when a bi-directional flux was considered it was possible to note a greater flux of N from non-fixing plants to N-fixing plants, contradicting the source-sink theory initially proposed by this system ( He et al., 2005 , 2009 ; Pirhofer-Walzl et al., 2012 ).

Moreover, a transfer between N 2 non-fixing donors and receiver plants of varying amount of N has also been observed. The transfer of N usually was reported to be lower than 5 % of N added by pulse labeling, while the direction of transport was largely found to be correlated with plant size ( Teste et al., 2009 , 2015 ; He et al., 2019 ) or plant physiology ( Meding and Zasoski, 2008 ; Weremijewicz et al., 2018 ). Teste et al. (2009) also suggested that C and N move together in form of amino acids, once the stoichiometry of the relative amounts of C and N transferred was similar of this compound, but they were never identified ( Simard et al., 2015 ).

Interestingly, the idea of plant-to-plant transfer implies that N may flow in the “opposite” direction of what is widely known to occur. In the context of nutrient uptake, the current model suggests that P and N acquired from surrounding soil by the ERM of the fungi are transferred to the intraradical mycelium (IRM) as polyphosphate (polyP) and arginine, respectively, stored later on in vacuoles ( Hijikata et al., 2010 ; Bücking and Kafle, 2015 ). Once in the IRM, polyp, and arginine are catabolized and Pi and ammonium are released and transported to the plants through transporters present in the periarbuscular membrane ( Breuillin-Sessoms et al., 2015 ; Wang et al., 2017 ; Figure 1 ). Therefore, for plant-to-plant transfer, N should be transferred in the opposite direction: from plant to the IRM via transporters in the periarbuscular membrane, from IRM transferred to the ERM of the fungi and then again to the IRM of the receiver plant to be assimilated. Although many studies have been made in order to prove such transfer via connected hyphae (please check Supplementary Table 1 for some of those studies), such fluxes were never described anywhere. In the studies presented in Supplementary Table 1 , it is also possible to observe that amount of N transferred via CMN is quite variable, probably due to differences in the experimental design and the choice of plant and fungi combination. In addition, transfer exclusively via mycelium connection in comparison to other possible are not distinguishable, especially in those studies in which a mesh barrier is not used to prevent roots intermingle and flow of soil solution.

Figure 1 . Mycorrhizal pathways for Pi and N in AM Symbiosis. In the mycorrhizal pathway, Pi is assimilated directly via phosphate importers while ammonium ( NH 4 + ) and/or nitrate ( NO 3 - ) are assimilated into glutamine (Gln) and then into arginine (Arg). Assimilation will generate excess H + or OH − with NH 4 + and NO 3 - , respectively. Phosphate is mainly transported in the form of polyphosphate (Poly-P) granules, which is negatively charged, making possible it association with arginine and metal ions for further transportation to the IRM. Phosphate (Pi) and NH 4 + transporters from the intraradical mycelium (IRM) to the interfacial apoplast are still unknown and therefore marked with a “?,” requiring further study (modified from Wang et al., 2017 ).

Direct Vs. Indirect Transfer

Mechanistically, AM fungi can facilitate the transfer of N between plants by creating direct mycelial connections between donors and receivers ( Høgh-Jensen, 2006 ; Meng et al., 2015 ; He et al., 2019 ). When it comes to resource allocation through CMN, it is easy to notice a disagreement regarding its concept within published papers, even most recent ones. On the one hand some authors report a transport of nutrients via CMN exclusively via connected hyphae, thus describing hyphae as “pipelines” for resources ( Klein et al., 2016 ; Van Der Heijden, 2016 ). On the other hand, other authors describe nutrient transfer to occur at least additionally via an indirect pathway. In such pathway, compounds are exuded or leaked into the soil pool by the roots or associated hyphae of one plant and then picked up by the roots or associated hyphae of a neighboring plant or even by other microorganisms present in the soil ( Jansa et al., 2019 ; Fernandez et al., 2020 ; Fang et al., 2021 ). In this context, it is frequently stated in studies that CMN simply facilitate transfers between plants without further specification of the mode of transport, although this transport may occur by several pathways simultaneously between a single pair of plants ( Wang et al., 2016 ; Fang et al., 2021 ).

For these indirect pathways, resources are vulnerable for potential disruptions, such as adsorption of nutrients to soil particles, immobilization and mineralization by surrounding microorganisms, biochemical transformation, and others ( Philip et al., 2010 ; Simard et al., 2012 ). Thus, a direct pathway genuinely utilizing mycorrhizal hyphae would represent a potential conduit of resource sharing, in which resources would be free of disruption by leakage and re-assimilation by other microorganisms.

In field and laboratory studies, split root designs and root restrictive screening techniques have been used to determine the different pathways in interplant transfers ( Xiao et al., 2004 ; He et al., 2005 ; Meng et al., 2015 ; Muneer et al., 2020 ). These designs can effectively prevent contact between individual host plant root systems, but they do not entirely prevent bulk flow or diffusive chemical movement in the soil water. Therefore, some experimental designs rely on air gaps to avoid diffusion over the soil solution flow while allowing the ingrowth of hyphae but not roots. This assures that all labeled compounds found in the receiver plant using in this system can be attributed to the mycorrhizal transport ( Zhang et al., 2020 ; Andrino et al., 2021 ; Fang et al., 2021 ). However, these measures still do not exclude a transfer over indirect pathways, once transported resources by fungi mycelium can be released on neighboring plant compartment, leading the receiver plant to have access to resources without being connected ( Figure 2 ). Moreover, connections among plants can hardly be directly visualized in soils of traditional pot experiments or even under field conditions.

Figure 2 . Possible movement of resources between networked plants, even when mesh barriers are used to avoid roots intermingle and flow of soil solution between connected plants. (A) Represents disrupted hyphal connections between two mycorrhizal (M+) plants and (B) possible transfer from a mycorrhized (M+) plant to a non-mycorrhized (M−) neighbor plant.

Therefore, due to the technical difficulties to distinguish between transport pathways, it still remains unknown whether transfer occurs preferentially via direct hyphae connections or through indirect pathways. Creation of new experiment set-ups using new technologies to improve previous experiments should be developed for a more accurate idea about resource allocation and plant physiological responses that are truly accountable to CMN. Manipulation of the genes involved in setting up symbiotic associations between plant and fungi partner may help to differentiate the fungal effect in such networks ( Merrild et al., 2013 ; Song et al., 2014 ). Mutant lines where the development of arbuscules is impaired and not functional are a promising starting point, and at least for M. truncatula such a mutant line is already known. Arbuscules are recognized as the main site of exchange, and comparing networks formed by wild type and mutant lines might lead to e better understanding of the effects of arbuscular network on the development of donor and receiver. Unfortunately, to our knowledge there are no such impaired mutant lines for EM fungi, therefore such studies are only possible for AM networks. In addition, some plant genera such Acacia, Alnus, Eucalyptus, Fraxinus, Populus, Salix, Shorea, and Uapaca are recognized to associate with both AM and EM fungi simultaneously ( Teste et al., 2020 ), although frequency of each fungi type might differ along plant life. Much less research have been made in dual-mycorrhizae plants, and how AM and EM networks may affect connected plants differently. Altogether, such experiments could be helpful in order to achieve deeper understanding of mechanisms and processes behind CMN and its impact on plant community.

Nevertheless, it is important to keep in mind that, even if resources exchanges between plants takes place mainly via indirect pathways, receiver plants can still be favored by a facilitation of its access to resource coming from neighboring plants, which may anyway play a role in plant-to-plant interaction ( Høgh-Jensen, 2006 ; Alaux et al., 2021 ).

Role of Transfer for Plant Fitness

The simple movement of elements from one plant to another does not by itself indicate a net transfer able to represent an ecological advantage on plant fitness ( Kytöviita et al., 2003 ; Bücking et al., 2016 ). Quantifying the contribution of each pathway to plant fitness is likewise a matter of discussion in most studies on CMN. However, quantification of nutrient and C fluxes exclusive to the fungal hyphae is difficult. To the best of our knowledge, there are only few quantitative information on the magnitude of C fluxes between plants sharing a CMN. In general, C transfer through CMN is not frequently considered a significant pathway for mobile C transfer among plants, although some authors suggest that even small amounts may be of great importance for receiver plant survival and development ( Wu et al., 2001 ; Deslippe and Simard, 2011 ; Klein et al., 2016 ). This can be especially true if the receiver plants are seedlings ( Nara, 2006 ; Booth and Hoeksema, 2010 ; Burke et al., 2018 ; Liang et al., 2021 ). Reported amounts of C vary from 0 up to 10% in literature ( Teste et al., 2010 ; Lin et al., 2020 ). Simard et al. (1997b) was the first attempting to quantify a bidirectional flux of C between plants connected via EM network, in order to evaluate its ecology significance. The authors concluded that there was no net transfer between the species. However, the study raised debate in the literature due to its difficulty in extrapolating the data from young seedlings to mature tree and the use of relevant controls ( Robinson and Fitter, 1999 ; Simard et al., 2012 ; Tedersoo et al., 2020 ). In addition, Simard et al. (1997b) concluded that it was not possible to distinguish whether the translocation occurred through interconnecting hyphae, soil pathways, or even both simultaneously, and, hence, did not really demonstrate the contribution of the CMN for C transfer.

A more recent approach was developed by Klein et al. (2016) , attempting to evaluate C transfer between trees in a mature forest. They continuously labeled five 40-m-tall Norway spruce trees ( Picea abies ) as part of a 5-year free-air CO 2 enrichment experiment (FACE) with 13 C-depleted CO 2 . Despite the low difference in the δ 13 C ratios of canopy twigs, stems, and fine roots between labeled and unlabeled control (max. 2.6‰), the isotopic signal of neighboring trees belonging to same or different taxa ( Fagus sylvatica, Pinus sylvestris , and Larix decidua ) were than measured to evaluate C allocation. The authors claimed to find evidences that reciprocal C transfer indeed occurred between trees, as δ 13 C of fine roots of neighboring plants followed the same signal from the donor Picea . Most of the label was found in the fine roots, which was concluded to prove the participation of the mycorrhizae in the transfer. It was estimated that C derived from transfer represents 4% of net primary productivity.

Another point usually under discussion regarding C transfer is whether transferred C is taken up by the receiver plant for its own growth or, contrastingly, whether the C is mainly kept in the roots, probably incorporated into fungal structures, therefore not representing a meaningful advantage for the receiver plant. This was evaluated, for example, by Waters and Borowicz (1994) and Fitter et al. (1998) . They assumed that by clipping the aboveground parts of living plants, additional C would be required and translocated from the roots to the re-growing clipped shoots. However, in neither of the experiments labeled C was found in the re-growing shoots of the receiver plants. Thus, the authors concluded that the transferred C remained in fungal structures. The opposite was found by Song et al. (2015) who reported labeled 13 C in the shoots of the receiver plant. Another difference in the mentioned studies is that, in the experiment developed by Song et al. (2015) , C transfer from donor to receiver plant increased by increasing defoliation of donor plant. This has been suggested as an effect of the sink-source strength of the connected plants. The authors concluded authors that defoliation could have stimulated interior Douglas-fir donor to rapidly export labile C from enriched roots to the CMN, while the rapid growth rate of ponderosa pine would created a large sink. Nevertheless, even if it is assumed that mycorrhizae might be able to transfer C from one plant to its neighbors, it remains unclear if the amounts of the transferred elements are of any significance to the receiver plant. If this amount is viable for the receiver plant, a process understanding of the switch between fungal storage and delivery to the plant is still required.

Equally contradictory is the magnitude of N transfer reported in the literature. In grassland ecosystems, N transfer was reported to vary from 0 to 72% under field conditions, while it is less variable in agroforestry ecosystems, ranging from 0 up to 16%, depending of the conditions under which the experiments were performed (e.g., in pots, field, etc.; Marty et al., 2009 ; Chapagain and Riseman, 2014 ; Meng et al., 2015 ; Zhang et al., 2020 ). In general, the high variability in the literature may reflect many different factors that might interfere in plant-to-plant interaction, such as differences in environmental conditions, in the different experimental setups, or plant and fungi combinations, soil nutrient supply, additional stress conditions added (e.g., nutrients deficiency, drought, shading, etc.), and the general experimental design (e.g., field, pot or microcosmos experiments). In addition, like for C, quantification of N transfer via interconnecting hyphae is not distinguishable from other pathways ( Montesinos-Navarro et al., 2016 ; Fang et al., 2021 ). The distinction and relative importance of the different pathways determines the strength, direction, and outcome of interactions among plants and soil organisms, requiring new technologies and ideas to address such issues. Nevertheless, the many researches made on this topic so far developed different hypotheses that could give us some hints on how CMN would affect plant-plant interaction.

Conclusions

Despite of the great progress in understanding the effect of mycorrhiza network for plant-to-plant interactions, and how this might affect mycorrhizal communities, there are still important questions to be answered in future researches. Resource allocation between connected plants thereby drew the largest attention of the scientific community. Many possible effects of such transfers of resources have been described, but contrasting results were frequently found. Labeled experiments using C and N isotopes have revealed that under certain conditions a movement of such resources between donor and receiver plants seem to happen, but none of them could demonstrate unequivocally that the transfer occurred preferentially through the direct mycorrhizal pathway and not over the soil solution or simply over exudates. Moreover, quantification of this transfer demonstrated to be an even bigger challenge. Therefore, the real effect of the CMN in shaping plant communities is still not clear. Further research involving new experiment set-ups and new technologies to improve previous experiments should be developed for a more accurate idea about resource allocation and plant physiological responses that are truly accountable to CMN. The use of mutant lines with manipulation of the genes involved in setting up symbiotic associations between plant and fungi partner together with labeling techniques to track resources translocation between connected plants can be used to differentiate the fungal effect in such networks. Effects exclusively to CMN for plant interactions may help us to understand plant community and ecosystem functioning.

Author Contributions

AF, JB, and GG conceived the idea about the topic reviewed in this manuscript. AF wrote the manuscript. JB and GG contributed with corrections and comments and approved the submitted version. All authors contributed to the article and approved the submitted version.

We want to thank the German Research Foundation (Deutsche Forschungsgemeinschaft) for the funding of this project in the framework of the DFG-GRK 1798 Signaling at the Plant-Soil Interface. The publication of this article was funded by the Open Access fund of Leibniz Universität Hannover.

Conflict of Interest

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

Publisher's Note

All claims expressed in this article are solely those of the authors and do not necessarily represent those of their affiliated organizations, or those of the publisher, the editors and the reviewers. Any product that may be evaluated in this article, or claim that may be made by its manufacturer, is not guaranteed or endorsed by the publisher.

Supplementary Material

The Supplementary Material for this article can be found online at: https://www.frontiersin.org/articles/10.3389/ffunb.2021.735299/full#supplementary-material

Alaux, P. L., Zhang, Y., Gilbert, L., and Johnson, D. (2021). Can common mycorrhizal fungal networks be managed to enhance ecosystem functionality? Plants People Planet . 1–12. doi: 10.1002/ppp3.10178

CrossRef Full Text

Andrino, A., Guggenberger, G., Sauheitl, L., Burkart, S., and Boy, J. (2021). Carbon investment into mobilization of mineral and organic phosphorus by arbuscular mycorrhiza. Biol. Fertil. Soils 57, 47–64. doi: 10.1007/s00374-020-01505-5

CrossRef Full Text | Google Scholar

Babikova, Z., Gilbert, L., Bruce, T. J., Birkett, M., Caulfield, J. C., Woodcock, C., et al. (2013). Underground signals carried through common mycelial networks warn neighbouring plants of aphid attack. Ecol. Lett. 16, 835–843. doi: 10.1111/ele.12115

PubMed Abstract | CrossRef Full Text | Google Scholar

Barreto de Novais, C., Pepe, A., Siqueira, J. O., Giovannetti, M., and Sbrana, C. (2017). Compatibility and incompatibility in hyphal anastomosis of arbuscular mycorrhizal fungi. Sci. Agric. 74, 411–416. doi: 10.1590/1678-992x-2016-0243

Beiler, K. J., Durall, D. M., Simard, S. W., Maxwell, S. A., and Kretzer, A. M. (2010). Architecture of the wood-wide web: Rhizopogon spp. genets link multiple Douglas-fir cohorts. New Phytol. 185, 543–553. doi: 10.1111/j.1469-8137.2009.03069.x

Beiler, K. J., Simard, S. W., and Durall, D. M. (2015). Topology of tree-mycorrhizal fungus interaction networks in xeric and mesic Douglas-fir forests. J. Ecol. 103, 616–628. doi: 10.1111/1365-2745.12387

Bever, J. D., Dickie, I. A., Facelli, E., Facelli, J. M., Klironomos, J., Moora, M., et al. (2010). Rooting theories of plant community ecology in microbial interactions. Trends Ecol. Evol. 25, 468–478. doi: 10.1016/j.tree.2010.05.004

Bezrutczyk, M., Yang, J., Eom, J. S., Prior, M., Sosso, D., Hartwig, T., et al. (2018). Sugar flux and signaling in plant-microbe interactions. Plant J. 93, 675–685. doi: 10.1111/tpj.13775

Bidartondo, M. I., Redecker, D., Hijri, I., Wiemken, A., Bruns, T. D., Domínguez, L., et al. (2002). Epiparasitic plants specialized on arbuscular mycorrhizal fungi. Nature 419, 389–392. doi: 10.1038/nature01054

Bingham, M. A., and Simard, S. (2012). Ectomycorrhizal networks of Pseudotsuga menziesii var. glauca trees facilitate establishment of conspecific seedlings under drought. Ecosystems 15, 188–199. doi: 10.1007/s10021-011-9502-2

Bingham, M. A., and Simard, S. W. (2011). Do mycorrhizal network benefits to survival and growth of interior Douglas-fir seedlings increase with soil moisture stress? Ecol. Evol. 1, 306–316. doi: 10.1002/ece3.24

Booth, M. G., and Hoeksema, J. D. (2010). Mycorrhizal networks counteract competitive effects of canopy trees on seedling survival. Ecology 91, 2294–2302. doi: 10.1890/09-1139.1

Bravo, A., Brands, M., Wewer, V., Dörmann, P., and Harrison, M. J. (2017). Arbuscular mycorrhiza-specific enzymes FatM and RAM 2 fine-tune lipid biosynthesis to promote development of arbuscular mycorrhiza. New Phytol. 214, 1631–1645. doi: 10.1111/nph.14533

Breuillin-Sessoms, F., Floss, D. S., Gomez, S. K., Pumplin, N., Ding, Y., Levesque-Tremblay, V., et al. (2015). Suppression of arbuscule degeneration in Medicago truncatula phosphate transporter4 mutants is dependent on the ammonium transporter 2 family protein AMT2; 3. Plant Cell 27, 1352–1366. doi: 10.1105/tpc.114.131144

Brundrett, M. C. (2009). Mycorrhizal associations and other means of nutrition of vascular plants: understanding the global diversity of host plants by resolving conflicting information and developing reliable means of diagnosis. Plant Soil 320, 37–77. doi: 10.1007/s11104-008-9877-9

Brundrett, M. C., and Tedersoo, L. (2018). Evolutionary history of mycorrhizal symbioses and global host plant diversity. New Phytol. 220, 1108–1115. doi: 10.1111/nph.14976

Bücking, H., and Kafle, A. (2015). Role of arbuscular mycorrhizal fungi in the nitrogen uptake of plants: current knowledge and research gaps. Agronomy 5, 587–612. doi: 10.3390/agronomy5040587

Bücking, H., Mensah, J. A., and Fellbaum, C. R. (2016). Common mycorrhizal networks and their effect on the bargaining power of the fungal partner in the arbuscular mycorrhizal symbiosis. Commun. Integr. Biol. 9:e1107684. doi: 10.1080/19420889.2015.1107684

Burke, D. J., Klenkar, M. K., and Medeiros, J. S. (2018). Mycorrhizal network connections, water reduction, and neighboring plant species differentially impact seedling performance of two forest wildflowers. Int. J. Plant Sci. 179, 314–324. doi: 10.1086/696686

Chapagain, T., and Riseman, A. (2014). Barley-pea intercropping: effects on land productivity, carbon and nitrogen transformations. Field Crops Res. 166, 18–25. doi: 10.1016/j.fcr.2014.06.014

Courty, P. E., Buée, M., Diedhiou, A. G., Frey-Klett, P., Le Tacon, F., Rineau, F., et al. (2010). The role of ectomycorrhizal communities in forest ecosystem processes: new perspectives and emerging concepts. Soil Biol. Biochem. 42, 679–698. doi: 10.1016/j.soilbio.2009.12.006

Deslippe, J. R., and Simard, S. W. (2011). Below-ground carbon transfer among Betula nana may increase with warming in Arctic tundra. New Phytol. 192, 689–698. doi: 10.1111/j.1469-8137.2011.03835.x

Diédhiou, A. G., Selosse, M. A., Galiana, A., Diabaté, M., Dreyfus, B., Bâ, A. M., et al. (2010). Multi-host ectomycorrhizal fungi are predominant in a Guinean tropical rainforest and shared between canopy trees and seedlings. Environ. Microbiol. 12, 2219–2232. doi: 10.1111/j.1462-2920.2010.02183.x

Ekblad, A., Wallander, H., Godbold, D. L., Cruz, C., Johnson, D., Baldrian, P., et al. (2013). The production and turnover of extramatrical mycelium of ectomycorrhizal fungi in forest soils: role in carbon cycling. Plant Soil 366, 1–27. doi: 10.1007/s11104-013-1630-3

Fang, L., He, X., Zhang, X., Yang, Y., Liu, R., Shi, S., et al. (2021). A small amount of nitrogen transfer from White Clover to Citrus seedling via common arbuscular mycorrhizal networks. Agronomy 11:32. doi: 10.3390/agronomy11010032

Fellbaum, C. R., Gachomo, E. W., Beesetty, Y., Choudhari, S., Strahan, G. D., Pfeffer, P. E., et al. (2012). Carbon availability triggers fungal nitrogen uptake and transport in arbuscular mycorrhizal symbiosis. Proc. Nat. Acad. Sci. U.S.A. 109, 2666–2671. doi: 10.1073/pnas.1118650109

Fellbaum, C. R., Mensah, J. A., Cloos, A. J., Strahan, G. E., Pfeffer, P. E., Kiers, E. T., et al. (2014). Fungal nutrient allocation in common mycorrhizal networks is regulated by the carbon source strength of individual host plants. New Phytol. 203, 646–656. doi: 10.1111/nph.12827

Fernandez, M., Malagoli, P., Vernay, A., Ameglio, T., and Balandier, P. (2020). Below-ground nitrogen transfer from oak seedlings facilitates Molinia growth: 15 N pulse-chase labelling. Plant Soil 423, 59–85. doi: 10.1007/s11104-020-04473-9

Fitter, A. H., Graves, J. D., Watkins, N. K., Robinson, D., and Scrimgeour, C. (1998). Carbon transfer between plants and its control in networks of arbuscular mycorrhizas. Funct. Ecol. 12, 406–412. doi: 10.1046/j.1365-2435.1998.00206.x

Gilbert, L., and Johnson, D. (2017). Plant-plant communication through common mycorrhizal networks. Adv. Bot. Res. 82, 83–97. doi: 10.1016/bs.abr.2016.09.001

Giovannetti, M., Fortuna, P., Citernesi, A. S., Morini, S., and Nuti, M. P. (2001). The occurrence of anastomosis formation and nuclear exchange in intact arbuscular mycorrhizal networks. New Phytol. 151, 717–724. doi: 10.1046/j.0028-646x.2001.00216.x

Girlanda, M., Selosse, M. A., Cafasso, D., Brilli, F., Delfine, S., Fabbian, R., et al. (2006). Inefficient photosynthesis in the Mediterranean orchid Limodorum abortivum is mirrored by specific association to ectomycorrhizal Russulaceae. Mol. Ecol. 15, 491–504. doi: 10.1111/j.1365-294X.2005.02770.x

Gorzelak, M. A., Asay, A. K., Pickles, B. J., and Simard, S. W. (2015). Inter-plant communication through mycorrhizal networks mediates complex adaptive behaviour in plant communities. AoB Plants 7:plv050. doi: 10.1093/aobpla/plv050

Grove, S., Saarman, N. P., Gilbert, G. S., Faircloth, B., Haubensak, K. A., and Parker, I. M. (2019). Ectomycorrhizas and tree seedling establishment are strongly influenced by forest edge proximity but not soil inoculum. Ecol. Appl. 29:e01867. doi: 10.1002/eap.1867

Gyuricza, V., Thiry, Y., Wannijn, J., Declerck, S., and Dupré de Boulois, H. (2010). Radiocesium transfer between Medicago truncatula plants via a common mycorrhizal network. Environ. Microbiol. 12, 2180–2189. doi: 10.1111/j.1462-2920.2009.02118.x

He, X., Critchley, C., Ng, H., and Bledsoe, C. (2005). Nodulated N2-fixing Casuarina cunninghamiana is the sink for net N transfer from non-N2-fixing Eucalyptus maculata via an ectomycorrhizal fungus Pisolithus sp. using 15NH4+ or 15NO3– supplied as ammonium nitrate. New Phytol. 167, 897–912. doi: 10.1111/j.1469-8137.2005.01437.x

He, X., Xu, M., Qiu, G. Y., and Zhou, J. (2009). Use of 15N stable isotope to quantify nitrogen transfer between mycorrhizal plants. J. Plant Ecol. 2, 107–118. doi: 10.1093/jpe/rtp015

He, Y., Cornelissen, J. H., Wang, P., Dong, M., and Ou, J. (2019). Nitrogen transfer from one plant to another depends on plant biomass production between conspecific and heterospecific species via a common arbuscular mycorrhizal network. Environ. Sci. Pollut. Res. 26, 8828–8837. doi: 10.1007/s11356-019-04385-x

Heaton, L., Obara, B., Grau, V., Jones, N., Nakagaki, T., Boddy, L., et al. (2012). Analysis of fungal networks. Fungal Biol. Rev. 26, 12–29. doi: 10.1016/j.fbr.2012.02.001

Hijikata, N., Murase, M., Tani, C., Ohtomo, R., Osaki, M., and Ezawa, T. (2010). Polyphosphate has a central role in the rapid and massive accumulation of phosphorus in extraradical mycelium of an arbuscular mycorrhizal fungus. New Phytol. 186, 285–289. doi: 10.1111/j.1469-8137.2009.03168.x

Hoeksema, J. D. (2015). “Experimentally testing effects of mycorrhizal networks on plant-plant interactions and distinguishing among mechanisms,” in Mycorrhizal Networks (Dordrecht: Springer), 255–277. doi: 10.1007/978-94-017-7395-9_9

Högberg, P., Högberg, M. N., Quist, M. E., Ekblad, A. L. F., and Näsholm, T. (1999). Nitrogen isotope fractionation during nitrogen uptake by ectomycorrhizal and non-mycorrhizal Pinus sylvestris . New Phytol. 142, 569–576. doi: 10.1046/j.1469-8137.1999.00404.x

Høgh-Jensen, H. (2006). The nitrogen transfer between plants: an important but difficult flux to quantify. Plant Soil 282, 1–5. doi: 10.1007/s11104-005-2613-9

Hu, L., Robert, C. A., Cadot, S., Zhang, X., Ye, M., Li, B., et al. (2018). Root exudate metabolites drive plant-soil feedbacks on growth and defense by shaping the rhizosphere microbiota. Nat. Commun. 9, 1–13. doi: 10.1038/s41467-018-05122-7

Jansa, J., Forczek, S. T., Rozmoš, M., Püschel, D., Bukovská, P., and Hršelová, H. (2019). Arbuscular mycorrhiza and soil organic nitrogen: network of players and interactions. Chem. Biol. Technol. Agric. 6, 1–10. doi: 10.1186/s40538-019-0147-2

Kadowaki, K., Yamamoto, S., Sato, H., Tanabe, A. S., Hidaka, A., and Toju, H. (2018). Mycorrhizal fungi mediate the direction and strength of plant-soil feedbacks differently between arbuscular mycorrhizal and ectomycorrhizal communities. Commun. Biol. 1, 1–11. doi: 10.1038/s42003-018-0201-9

Keymer, A., Pimprikar, P., Wewer, V., Huber, C., Brands, M., Bucerius, S. L., et al. (2017). Lipid transfer from plants to arbuscular mycorrhiza fungi. Elife 6:e29107. doi: 10.7554/eLife.29107.051

Kiers, E. T., Duhamel, M., Beesetty, Y., Mensah, J. A., Franken, O., Verbruggen, E., et al. (2011). Reciprocal rewards stabilize cooperation in the mycorrhizal symbiosis. Science 333, 880–882. doi: 10.1126/science.1208473

Klein, T., Siegwolf, R. T. W., and Körner, C. (2016). Belowground carbon trade among tall trees in a temperate forest. Science 352, 342–344. doi: 10.1126/science.aad6188

Kytöviita, M. M., Vestberg, M., and Tuomi, J. (2003). A test of mutual aid in common mycorrhizal networks: established vegetation negates benefit in seedlings. Ecology 84, 898–906. doi: 10.1890/0012-9658(2003)084[0898:ATOMAI]2.0.CO;2

Lekberg, Y., Hammer, E. C., and Olsson, P. A. (2010). Plants as resource islands and storage units-adopting the mycocentric view of arbuscular mycorrhizal networks. FEMS Microbiol. Ecol. 74, 336–345. doi: 10.1111/j.1574-6941.2010.00956.x

Liang, M., Shi, L., Burslem, D. F., Johnson, D., Fang, M., Zhang, X., et al. (2021). Soil fungal networks moderate density-dependent survival and growth of seedlings. New Phytol . 230, 1688–1689. doi: 10.1111/nph.17237

Lin, C., Wang, Y., Liu, M., Li, Q., Xiao, W., and Song, X. (2020). Effects of nitrogen deposition and phosphorus addition on arbuscular mycorrhizal fungi of Chinese fir ( Cunninghamia lanceolata ). Sci. Rep. 10, 1–8. doi: 10.1038/s41598-020-69213-6

Marty, C., Pornon, A., Escaravage, N., Winterton, P., and Lamaze, T. (2009). Complex interactions between a legume and two grasses in a subalpine meadow. Am. J. Bot. 96, 1814–1820. doi: 10.3732/ajb.0800405

McGuire, K. L. (2007). Common ectomycorrhizal networks may maintain monodominance in a tropical rain forest. Ecology 88, 567–574. doi: 10.1890/05-1173

Meding, S. M., and Zasoski, R. J. (2008). Hyphal-mediated transfer of nitrate, arsenic, cesium, rubidium, and strontium between arbuscular mycorrhizal forbs and grasses from a California oak woodland. Soil Biol. Biochem. 40, 126–134. doi: 10.1016/j.soilbio.2007.07.019

Meng, L., Zhang, A., Wang, F., Han, X., Wang, D., and Li, S. (2015). Arbuscular mycorrhizal fungi and rhizobium facilitate nitrogen uptake and transfer in soybean/maize intercropping system. Front. Plant Sci. 6:339. doi: 10.3389/fpls.2015.00339

Merrild, M. P., Ambus, P., Rosendahl, S., and Jakobsen, I. (2013). Common arbuscular mycorrhizal networks amplify competition for phosphorus between seedlings and established plants. New Phytol. 200, 229–240. doi: 10.1111/nph.12351

Mikkelsen, B. L., Rosendahl, S., and Jakobsen, I. (2008). Underground resource allocation between individual networks of mycorrhizal fungi. New Phytol. 180, 890–898. doi: 10.1111/j.1469-8137.2008.02623.x

Montesinos-Navarro, A., Verd,ú, M., Querejeta, J. I., Sortibrán, L., and Valiente-Banuet, A. (2016). Soil fungi promote nitrogen transfer among plants involved in long-lasting facilitative interactions. Perspect. Plant Ecol. Evol. Syst. 18, 45–51. doi: 10.1016/j.ppees.2016.01.004

Montesinos-Navarro, A., Verdú, M., Querejeta, J. I., and Valiente-Banuet, A. (2017). Nurse plants transfer more nitrogen to distantly related species. Ecology 98, 1300–1310. doi: 10.1002/ecy.1771

Muneer, M. A., Wang, P., Lin, C., and Ji, B. (2020). Potential role of common mycorrhizal networks in improving plant growth and soil physicochemical properties under varying nitrogen levels in a grassland ecosystem. Glob. Ecol. Conserv. 24:e01352. doi: 10.1016/j.gecco.2020.e01352

Nara, K. (2006). Ectomycorrhizal networks and seedling establishment during early primary succession. New Phytol. 169, 169–178. doi: 10.1111/j.1469-8137.2005.01545.x

Ngosong, C., Gabriel, E., and Ruess, L. (2014). Collembola grazing on arbuscular mycorrhiza fungi modulates nutrient allocation in plants. Pedobiologia 57, 171–179. doi: 10.1016/j.pedobi.2014.03.002

Pec, G. J., Simard, S. W., Cahill, J. F., and Karst, J. (2020). The effects of ectomycorrhizal fungal networks on seedling establishment are contingent on species and severity of overstorey mortality. Mycorrhiza 30, 173–183. doi: 10.1007/s00572-020-00940-4

Pena, R., Simon, J., Rennenberg, H., and Polle, A. (2013). Ectomycorrhiza affect architecture and nitrogen partitioning of beech ( Fagus sylvatica L.) seedlings under shade and drought. Environ. Exp. Bot. 87, 207–217. doi: 10.1016/j.envexpbot.2012.11.005

Perry, D. A., Margolis, H., Choquette, C., Molina, R., and Trappe, J. M. (1989). Ectomycorrhizal mediation of competition between coniferous tree species. New Phytol. 112, 501–511. doi: 10.1111/j.1469-8137.1989.tb00344.x

Pfeffer, P. E., Douds Jr, D. D., Bücking, H., Schwartz, D. P., and Shachar-Hill, Y. (2004). The fungus does not transfer carbon to or between roots in an arbuscular mycorrhizal symbiosis. New Phytol. 163, 617–627. doi: 10.1111/j.1469-8137.2004.01152.x

Philip, L., Simard, S., and Jones, M. (2010). Pathways for below-ground carbon transfer between paper birch and Douglas-fir seedlings. Plant Ecol. Divers. 3, 221–233. doi: 10.1080/17550874.2010.502564

Pickles, B. J., Wilhelm, R., Asay, A. K., Hahn, A. S., Simard, S. W., and Mohn, W. W. (2017). Transfer of 13C between paired Douglas-fir seedlings reveals plant kinship effects and uptake of exudates by ectomycorrhizas. New Phytol. 214, 400–411. doi: 10.1111/nph.14325

Pirhofer-Walzl, K., Rasmussen, J., Høgh-Jensen, H., Eriksen, J., Søegaard, K., and Rasmussen, J. (2012). Nitrogen transfer from forage legumes to nine neighbouring plants in a multi-species grassland. Plant Soil 350, 71–84. doi: 10.1007/s11104-011-0882-z

Prescott, C. E., Grayston, S. J., Helmisaari, H. S., Kaštovská, E., Körner, C., Lambers, H., et al. (2020). Surplus carbon drives allocation and plant-soil interactions. Trends Ecol. Evol . 35, 1110–1118. doi: 10.1016/j.tree.2020.08.007

Read, D. J. (1991). Mycorrhizas in ecosystems. Experientia 47, 376–391. doi: 10.1007/BF01972080

Rezáčová, V., Konvalinková, T., and Jansa, J. (2017). “Carbon fluxes in mycorrhizal plants,” in Mycorrhiza-eco-Physiology, Secondary Metabolites, Nanomaterials , ed T. R. Horton (Cham: Springer), 1–21. doi: 10.1007/978-3-319-57849-1_1

Rhodes, C. J. (2017). The whispering world of plants:'the wood wide web'. Sci. Prog. 100, 331–337. doi: 10.3184/003685017X14968299580423

Robinson, D., and Fitter, A. (1999). The magnitude and control of carbon transfer between plants linked by a common mycorrhizal network. J. Exp. Bot. 50, 9–13. doi: 10.1093/jxb/50.330.9

Rotheray, T. D., Jones, T. H., Fricker, M. D., and Boddy, L. (2008). Grazing alters network architecture during interspecific mycelial interactions. Fungal Ecol. 1, 124–132. doi: 10.1016/j.funeco.2008.12.001

Schüßler, A., and Walker, C. (2011). “Evolution of the 'plant-symbiotic' fungal phylum, glomeromycota,” in The Mycota XIV - Evolution of Fungi and Fungal-like Organisms , eds S. Pöggeler and J. Wöstemeyer (Berlin: Springer), 163–185. doi: 10.1007/978-3-642-19974-5_7

Seiwa, K., Negishi, Y., Eto, Y., Hishita, M., Masaka, K., Fukasawa, Y., et al. (2020). Successful seedling establishment of arbuscular mycorrhizal-compared to ectomycorrhizal-associated hardwoods in arbuscular cedar plantations. For. Ecol. Manage. 468:118155. doi: 10.1016/j.foreco.2020.118155

Selosse, M. A., Bocayuva, M. F., Kasuya, M. C. M., and Courty, P. E. (2016). “Mixotrophy in mycorrhizal plants: extracting carbon from mycorrhizal networks”, in Molecular Mycorrhizal Symbiosis , ed F. Martin (Berlin: Springer Verlag), 451–471. doi: 10.1002/9781118951446.ch25

Selosse, M. A., and Roy, M. (2009). Green plants that feed on fungi: facts and questions about mixotrophy. Trends Plant Sci. 14, 64–70. doi: 10.1016/j.tplants.2008.11.004

Simard, S., Asay, A., Beiler, K., Bingham, M., Deslippe, J., He, X., et al. (2015). “Resource transfer between plants through ectomycorrhizal fungal networks,” in Mycorrhizal Networks (Dordrecht: Springer), 133–176. doi: 10.1007/978-94-017-7395-9_5

Simard, S. W., Beiler, K. J., Bingham, M. A., Deslippe, J. R., Philip, L. J., and Teste, F. P. (2012). Mycorrhizal networks: mechanisms, ecology and modelling. Fungal Biol. Rev. 26, 39–60. doi: 10.1016/j.fbr.2012.01.001

Simard, S. W., and Durall, D. M. (2004). Mycorrhizal networks: a review of their extent, function, and importance. Can. J. Bot. 82, 1140–1165. doi: 10.1139/b04-116

Simard, S. W., Jones, M. D., Durall, D. M., Perry, D. A., Myrold, D. D., and Molina, R. (1997a). Reciprocal transfer of carbon isotopes between ectomycorrhizal Betula papyrifera and Pseudotsuga menziesii . New Phytol. 137, 529–542. doi: 10.1046/j.1469-8137.1997.00834.x

Simard, S. W., Perry, D. A., Jones, M. D., Myrold, D. D., Durall, D. M., and Molina, R. (1997b). Net transfer of carbon between ectomycorrhizal tree species in the field. Nature 388, 579–582. doi: 10.1038/41557

Smith, S. E., and Read, D. J. (2010). Mycorrhizal Symbiosis . Oxford: Academic Press.

Google Scholar

Song, Y. Y., Simard, S. W., Carroll, A., Mohn, W. W., and Zeng, R. S. (2015). Defoliation of interior Douglas-fir elicits carbon transfer and stress signalling to ponderosa pine neighbors through ectomycorrhizal networks. Sci. Rep. 5, 1–9. doi: 10.1038/srep08495

Song, Y. Y., Ye, M., Li, C., He, X., Zhu-Salzman, K., Wang, R. L., et al. (2014). Hijacking common mycorrhizal networks for herbivore-induced defence signal transfer between tomato plants. Sci. Rep. 4, 1–8. doi: 10.1038/srep03915

Song, Y. Y., Zeng, R. S., Xu, J. F., Li, J., Shen, X., and Yihdego, W. G. (2010). Interplant communication of tomato plants through underground common mycorrhizal networks. PLoS ONE 5:e13324. doi: 10.1371/journal.pone.0013324

Tedersoo, L., Bahram, M., and Zobel, M. (2020). How mycorrhizal associations drive plant population and community biology. Science 367:6480. doi: 10.1126/science.aba1223

Teste, F. P., Jones, M. D., and Dickie, I. A. (2020). Dual-mycorrhizal plants: their ecology and relevance. New Phytol. 225, 1835–1851. doi: 10.1111/nph.16190

Teste, F. P., Simard, S. W., Durall, D. M., Guy, R. D., and Berch, S. M. (2010). Net carbon transfer between Pseudotsuga menziesii var. glauca seedlings in the field is influenced by soil disturbance. J. Ecol. 98, 429–439. doi: 10.1111/j.1365-2745.2009.01624.x

Teste, F. P., Simard, S. W., Durall, D. M., Guy, R. D., Jones, M. D., and Schoonmaker, A. L. (2009). Access to mycorrhizal networks and roots of trees: importance for seedling survival and resource transfer. Ecology 90, 2808–2822. doi: 10.1890/08-1884.1

Teste, F. P., Veneklaas, E. J., Dixon, K. W., and Lambers, H. (2015). Is nitrogen transfer among plants enhanced by contrasting nutrient-acquisition strategies? Plant Cell Environ. 38, 50–60. doi: 10.1111/pce.12367

Toju, H., Sato, H., Yamamoto, S., Kadowaki, K., Tanabe, A. S., Yazawa, S., et al. (2013). How are plant and fungal communities linked to each other in belowground ecosystems? A massively parallel pyrosequencing analysis of the association specificity of root-associated fungi and their host plants. Ecol. Evol. 3, 3112–3124. doi: 10.1002/ece3.706

Van Der Heijden, M. G. (2016). Underground networking. Science 352, 290–291. doi: 10.1126/science.aaf4694

Van Der Heijden, M. G., and Horton, T. R. (2009). Socialism in soil? The importance of mycorrhizal fungal networks for facilitation in natural ecosystems. J. Ecol. 97, 1139–1150. doi: 10.1111/j.1365-2745.2009.01570.x

Van't Padje, A., Galvez, L. O., Klein, M., Hink, M. A., Postma, M., Shimizu, T., et al. (2021). Temporal tracking of quantum-dot apatite across in vitro mycorrhizal networks shows how host demand can influence fungal nutrient transfer strategies. ISME J. 15, 435–449. doi: 10.1038/s41396-020-00786-w

Varga, S., and Kytöviita, M. M. (2016). Faster acquisition of symbiotic partner by common mycorrhizal networks in early plant life stage. Ecosphere 7:e01222. doi: 10.1002/ecs2.1222

Wagg, C., Jansa, J., Stadler, M., Schmid, B., and Van Der Heijden, M. G. (2011). Mycorrhizal fungal identity and diversity relaxes plant-plant competition. Ecology 92, 1303–1313. doi: 10.1890/10-1915.1

Wagg, C., Veiga, R., and van der Heijden, M. G. (2015). “Facilitation and antagonism in mycorrhizal networks,” in Mycorrhizal Networks eds A. Varma, R. Prasad, and N. Tuteja (Dordrecht: Springer), 203–226. doi: 10.1007/978-94-017-7395-9_7

Wahbi, S., Maghraoui, T., Hafidi, M., Sanguin, H., Oufdou, K., Prin, Y., et al. (2016). Enhanced transfer of biologically fixed N from faba bean to intercropped wheat through mycorrhizal symbiosis. Appl. Soil Ecol. 107, 91–98. doi: 10.1016/j.apsoil.2016.05.008

Walder, F., Niemann, H., Natarajan, M., Lehmann, M. F., Boller, T., and Wiemken, A. (2012). Mycorrhizal networks: common goods of plants shared under unequal terms of trade. Plant Physiol. 159, 789–797. doi: 10.1104/pp.112.195727

Walder, F., and van der Heijden, M. G. (2015). Regulation of resource exchange in the arbuscular mycorrhizal symbiosis. Nat. Plants 1, 1–7. doi: 10.1038/nplants.2015.159

Wang, G., Sheng, L., Zhao, D., Sheng, J., Wang, X., and Liao, H. (2016). Allocation of nitrogen and carbon is regulated by nodulation and mycorrhizal networks in soybean/maize intercropping system. Front. Plant Sci. 7:1901. doi: 10.3389/fpls.2016.01901

Wang, G., Ye, C., Zhang, J., Koziol, L., Bever, J. D., and Li, X. (2019). Asymmetric facilitation induced by inoculation with arbuscular mycorrhizal fungi leads to overyielding in maize/faba bean intercropping. J. Plant Interact. 14, 10–20. doi: 10.1080/17429145.2018.1550218

Wang, W., Shi, J., Xie, Q., Jiang, Y., Yu, N., and Wang, E. (2017). Nutrient exchange and regulation in arbuscular mycorrhizal symbiosis. Mol. Plant 10, 1147–1158. doi: 10.1016/j.molp.2017.07.012

Waterman, R. J., Klooster, M. R., Hentrich, H., Bidartondo, M. I., and Merckx, V. (2013). Mycoheterotrophy: The Biology of Plants Living on Fungi . ed V. Merckx (New York, NY: Springer-Verlag).

Waters, J. R., and Borowicz, V. A. (1994). Effect of clipping, benomyl, and genet on 14C transfer between mycorrhizal plants. Oikos 246–252. doi: 10.2307/3546272

Weremijewicz, J., O'Reilly, L. S. L., and Janos, D. P. (2018). Arbuscular common mycorrhizal networks mediate intra-and interspecific interactions of two prairie grasses. Mycorrhiza 28, 71–83. doi: 10.1007/s00572-017-0801-0

Weremijewicz, J., Sternberg, L. D. S. L. O. R., and Janos, D. P. (2016). Common mycorrhizal networks amplify competition by preferential mineral nutrient allocation to large host plants. New Phytol. 212, 461–471. doi: 10.1111/nph.14041

Werner, G. D., and Kiers, E. T. (2015). Partner selection in the mycorrhizal mutualism. New Phytol. 205, 1437–1442. doi: 10.1111/nph.13113

Wilkinson, D. M. (1998). The evolutionary ecology of mycorrhizal networks. Oikos 407–410. doi: 10.2307/3546985

Wipf, D., Krajinski, F., van Tuinen, D., Recorbet, G., and Courty, P. E. (2019). Trading on the arbuscular mycorrhiza market: from arbuscules to common mycorrhizal networks. New Phytol. 223, 1127–1142. doi: 10.1111/nph.15775

Wu, B., Nara, K., and Hogetsu, T. (2001). Can 14C-labeled photosynthetic products move between Pinus densiflora seedlings linked by ectomycorrhizal mycelia? New Phytol. 149, 137–146. doi: 10.1046/j.1469-8137.2001.00010.x

Wu, B., Nara, K., and Hogetsu, T. (2005). Genetic structure of Cenococcum geophilum populations in primary successional volcanic deserts on Mount Fuji as revealed by microsatellite markers. New Phytol. 165, 285–293. doi: 10.1111/j.1469-8137.2004.01221.x

Xiao, Y., Li, L., and Zhang, F. (2004). Effect of root contact on interspecific competition and N transfer between wheat and fababean using direct and indirect 15N techniques. Plant Soil 262, 45–54. doi: 10.1023/B:PLSO.0000037019.34719.0d

Zhang, H., Wang, X., Gao, Y., and Sun, B. (2020). Short-term N transfer from alfalfa to maize is dependent more on arbuscular mycorrhizal fungi than root exudates in N deficient soil. Plant Soil 446, 23–41. doi: 10.1007/s11104-019-04333-1

Zimmer, K., Meyer, C., and Gebauer, G. (2008). The ectomycorrhizal specialist orchid Corallorhiza trifida is a partial myco-heterotroph. New Phytol. 178, 395–400. doi: 10.1111/j.1469-8137.2007.02362.x

Keywords: resources allocation, plant fitness, mycelium connections, connected plants, direct pathway, indirect pathway

Citation: Figueiredo AF, Boy J and Guggenberger G (2021) Common Mycorrhizae Network: A Review of the Theories and Mechanisms Behind Underground Interactions. Front. Fungal Biol. 2:735299. doi: 10.3389/ffunb.2021.735299

Received: 02 July 2021; Accepted: 23 August 2021; Published: 30 September 2021.

Reviewed by:

Copyright © 2021 Figueiredo, Boy and Guggenberger. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY) . The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

*Correspondence: Aline Fernandes Figueiredo, alinefigueiredo89@gmail.com

Disclaimer: All claims expressed in this article are solely those of the authors and do not necessarily represent those of their affiliated organizations, or those of the publisher, the editors and the reviewers. Any product that may be evaluated in this article or claim that may be made by its manufacturer is not guaranteed or endorsed by the publisher.

COMMENTS

feed the soil: my experiment with mycorrhizae
A. Many synthetic plant foods, especially fast-acting liquids, harm microbial activity in the soil and create fertilizer-dependent plants, so we don't recommend using them. We say that the fungi are not an "add-on-" to a chemical-fertilizer routine, but best used "instead of.". We recommend ongoing use of compost, compost tea, cover ...
PDF Mysterious Mycorrhizae? A Field Trip and Classroom Experiment to
Mycorrhizae Symbiosis occurs when individuals of different spe-cies live in a close physical association (Boucher et al., 1982). The word mycorrhiza is Latin for "fungus-root." Mycorrhizal associations involving soil fungi and plant roots are among the most common symbioses on Earth. There are many different types of mycorrhizal symbioses
How do mycorrhizae work? Explained Simply
From here, the mycorrhizae are able to absorb it to sustain themselves. There is very little sunlight underground, and even if there was, the mycorrhizae wouldn't be able to harvest it like plants because they don't have the equipment needed for photosynthesis. The sugar from the plants literally keeps the mycorrhizae fed and alive.
How mycorrhizal associations drive plant population and ...
Associations between plants and symbiotic fungi—mycorrhizas—are ubiquitous in plant communities. Tedersoo et al. review recent developments in mycorrhizal research, revealing the complex and pervasive nature of this largely invisible interaction. Complex networks of mycorrhizal hyphae connect the root systems of individual plants ...
Why You Should Add Mycorrhizae To Your Soil
At the same time, this makes plants more resistant to drought. For you folks in drought-prone areas, you're going to want to experiment with adding mycorrhizae to your soil. 2. Prevents Soil Erosion. Again, because the root system has so much surface area, it really gives your plant some grab. Large root systems keep soil in place.
Mycorrhiza: a natural resource assists plant growth under varied soil
Abstract. In this overview, the authors have discussed the potential advantages of the association between mycorrhizae and plants, their mutual accelerated growth under favorable conditions and their role in nutrient supply. In addition, methods for isolating mycorrhizae are described and spore morphologies and their adaptation to various ...
Farmers of Fungi: Growing Mushrooms and Mycorrhizae
Final Thoughts: "Experiment, Reflect, Experiment Again" As you venture into the exciting world of home mushroom and mycorrhizae cultivation, remember to experiment, reflect on what worked, what didn't, and then experiment again. Things may seem unfamiliar at first, but if you start small and pay attention you'll be sure to succeed in no ...
Mycorrhizae: Nature's Gift to Plant Health
Late in the 19th century, a Polish scientist by the name of Franciszek Kamienski made a remarkable discovery. He found there were soil-borne fungi that formed a mutually beneficial (symbiotic) relationships with the root systems of plants. Today, those fungi carry the common name of mycorrhizae which, literally interpreted, means "fungus-roots".
Mycorrhizae: Fostering Plant Health Through Fungal Symbiosis
Mycorrhizae, a term that refers to the symbiotic relationship between certain soil fungi and plant roots, represent a revolutionary approach to natural gardening and farming. ... Explore our shop and experiment with mycorrhizal inoculants, fostering a community of gardeners committed to sustainability and the well-being of our planet. You may ...
Mycorrhiza
A mycorrhiza (from Ancient Greek μύκης (múkēs) 'fungus', and ῥίζα (rhíza) 'root'; pl. mycorrhizae, mycorrhiza, or mycorrhizas) is a symbiotic association between a fungus and a plant. The term mycorrhiza refers to the role of the fungus in the plant's rhizosphere, its root system. Mycorrhizae play important roles in plant nutrition, soil biology, and soil chemistry.
Mycorrhizae
Mycorrhizae Definition. Mycorrhizae literally translates to "fungus-root.". Mycorrhiza defines a (generally) mutually beneficial relationship between the root of a plant and a fungus that colonizes the plant root. In many plants, mycorrhiza are fungi that grow inside the plant's roots, or on the surfaces of the roots.
Mysterious mycorrhizae? a field trip and classroom experiment to
T1 - Mysterious mycorrhizae? a field trip and classroom experiment to demystify the symbioses formed between plants and fungi. AU - Johnson, Nancy C. AU - Chaudhary, V. Bala. AU - Hoeksema, Jason D. AU - Moore, John C. AU - Pringle, Anne. AU - Umbanhowar, James A. AU - Wilson, Gail W.T. PY - 2009/9. Y1 - 2009/9
Unique and common traits in mycorrhizal symbioses
Abstract. Mycorrhizas are among the most important biological interkingdom interactions, as they involve ~340,000 land plants and ~50,000 taxa of soil fungi. In these mutually beneficial ...
Mycorrhizae
The word "mycorrhiza" means fungal root. To be more specific, mycorrhizae are fungi that have a symbiotic relationship with the roots of many plants. The fungi which commonly form mycorrhizal relationships with plants are ubiquitous in the soil. Many mycorrhizal fungi are obligately symbiotic and therefore are unable to survive in nature ...
Food, Poison, and Espionage: Mycorrhizal Networks in Action
Some 90% of terrestrial plant species around the world engage in symbioses called mycorrhizae—from Greek mykos (fungus) and rhiza (root). Mycorrhizal plants come from all corners of the plant kingdom and include trees, forbs, grasses, ferns, clubmosses, and liverworts. ... Experiments have shown that certain green orchids can convey carbon ...
Mycorrhizae
The associations between roots and fungi are called mycorrhizae. These symbiotic arrangements have been found in about 90% of all land plants, and have been around for approximately 400 million years. Plant roots are hospitable sites for the fungi to anchor and produce their threads (hyphae). The roots provide essential nutrients for the growth ...
Soil microbiome indicators can predict crop growth response to large
On-farm experiments in 54 fields in Switzerland show that inoculation with arbuscular mycorrhizal fungi can promote crop yield, and inoculation success can be predicted using soil microbiome ...
Frontiers
Mycorrhiza Network: Theoretical Background. Mutualistic associations between mycorrhizal fungi and plants are well-known. Within the diverse mycorrihza types, the arbuscular mycorrhizae (AM), from the phylum Glomeromycota, is one of the most common, ancient and widespread, associating with around 80% of all land plant species (Schüßler and Walker, 2011).
Fertilizer quantity and type alter mycorrhizae ...
In both experiments, we used mycorrhizae extracted from soil collected at the Dilmun Hill student organic farm at Cornell University (Ithaca, NY). Diverse, field collected mixtures have been found to be more beneficial to plants than monocultures (Rowe et al., 2007 ; Rúa et al., 2016 ), and are more representative of the conditions crop plants ...
20 Experiments with Ericoid Mycorrhiza
Publisher Summary. This chapter discusses experiments with ericoid mycorrhiza. There is a description of the procedures for isolation, culture, and re-inoculation of the mycorrhizal endophyte. The extent to which systematic experimental analysis of the response of host plants to infection has enabled justifiably to apply the term "mycorrhizal ...
Effects of mycorrhizae, plants, and soils on phosphorus leaching and
However, in their experiment, there was an effect of mycorrhizae on P content in stems which was due to increased biomass production. Reasons for a lack of response in our experiment may include root morphology (Figure 8 ), mesocosm size, lack of multiple symbiotic microbe, and plant partners for the mycorrhizae in the mesocosms, the commercial ...
Tree diversity effects on productivity depend on mycorrhizae and life
The experiment consists of eighty 11 × 11-m plots covered with a water-permeable weed tarp (minimization of weed interference), with a core area of 8 × 8 m (64 m 2). In March 2015, 140 2-year-old tree seedlings (nursery plants, bare-rooted, 50-80 cm height, no mycorrhizae inoculation) were planted in a 1 × 1-m grid in each plot (64 trees ...
Inoculation of Native Arbuscular Mycorrhizae and Bacillus subtilis Can
The same authors conducted an open greenhouse pot experiment, based on the evaluation of potentiality of wheat inoculation with native and non-native bacteria alone or in co-inoculation with AMF. ... Allium species has a coarse root structure without root hairs, the studied species showed to be highly responsive to mycorrhizae formation . There ...

feed the soil: my experiment with mycorrhizae

mycorrhizae 101, the basics

Leave a Reply Cancel reply

Related Posts

How do mycorrhizae work?

What are mycorrhizae?

How do plants help mycorrhizae?

How do mycorrhizae help plants?

Putting It All Together

Related Topics

Ecology-boo

Science Newsletter:

Teaching Biology?

How to Make Science Films

Read our Wildlife Guide

New From Untamed Science

Mycorrhiza: a natural resource assists plant growth under varied soil conditions

Subash C. B. Gopinath

M. N. A. Uda

Ahmad Radi Wan Yaakub

Introduction

Mycorrhizal fungi

Information on fungi

Wet sieving and decanting method

Analysis of fungal morphology

Spore morphology

Types of mycorrhizae

Arbuscular mycorrhizae

Ectomycorrhizae (EM)

Formation of mycorrhizae

Mycorrhizal plant interactions

Phosphate uptake

Plant growth under physiological conditions

Plant growth under greenhouse conditions

Study lines with greenhouses

Enhanced mycorrhizal associations under controlled greenhouse conditions

Prospective uses

Acknowledgements

Author contributions

Compliance with ethical standards

Farmers of Fungi: Growing Mushrooms and Mycorrhizae in Your Vegetable Patch

Soil Mycorrhizae

Do I Need Mycorrhizae?

How do I cultivate mycorrhizae?

Myco-Gardening: A Gourmet Mushroom Bed in Your Own Backyard!

Myco-gardening Techniques

Growing Mushrooms in Direct Substrate

Growing Mushrooms in Wood Chips

Growing Mushrooms in Straw

Growing Mushroomson Bur ied Logs

Mushroom Species overview:

Mushroom Preservation Techniques

Final Thoughts: “Experiment, Reflect, Experiment Again”

Mushroom Growing Sources and More Info

Leave a Reply Cancel reply

Useful Links

Top Categories

Subscribe Now

Integrated Pest Management

Missouri Produce Growers

Mycorrhizae: Nature's Gift to Plant Health

Published: February 10, 2020

Mycorrhizae

Mycorrhizae Introduction

Mycorrhizae Key Benefits

Mycorrhizae Nutritional Profile

How to Use Mycorrhizae

Ideal Plants and Soil Types

Sustainability and Environmental Impact

Mycorrhizae Tips and Tricks

Mycorrhizae Conclusion

You may also be interested in...

Mycorrhizae

Mycorrhizae Definition

Types of Mycorrhizae

Ectomycorrhiza

Endomycorrhiza

Examples of Mycorrhiza

Arbuscular Mycorrhiza

Ericaceous Mycorrhiza