Symbiotic fungi have a key role in soil ecosystems and inoculating plants with them has been claimed to benefit their growth. But scientific evidence shows a very complex picture; which might surprise you.
If you are a gardener, news might have reached your ear about a supposedly beneficial category of fungi called mycorrhizal. If you are an ecologist, chances are you consider mycorrhizae one of the most successful partnerships of all time. If you are a plant scientist, you know a great deal about them, but perhaps you are perplexed about the sensational claims that home gardeners, some regenerative farmers and most suppliers have been making in the last ten years. Although there is a wide consensus about the extreme importance of healthy mycorrhizal populations in thriving ecosystems and productive soils, their effects as plant growth stimulants constitute a controversial issue, to say the least.
Unfortunately, we are often exposed only to part of the scientific evidence available. In this article, I will try to provide a comprehensive, fully referenced yet non-technical review of:
1. what mycorrhizal fungi are and how they work;
2. how they interact with plants:
3. when and how they are beneficial or detrimental to them;
4. how mycorrhizal fungi can be effectively employed without incurring risks to plant health.
The sections that follow are numbered according to the list above, so that you may jump straight to any one of them, should you wish to.
1. What are mycorrhizae?
The term mycorrhiza (plural mycorrhizae) refers to the close and long-term (or symbiotic) association between a plant and a fungus present in the plant’s root zone (the rhizosphere). Scientists have known about these fascinating relationships for more than a century¹, while agronomists and gardeners have started to become acquainted with mycorrhizal fungi only in the last few decades, thanks to books such as Teaming with microbes, Mycorrhizal Planet and Mycelium Running.
Nearly all plants in the wild rely, for their nutrition, on the exchange of nutrients and other benefits with the complex network of soil microorganisms that is known as the soil microbiome or the soil food web². Within this rich underground ecosystem made up of worms, insects, bacteria, algae, and other microscopic creatures, fungi play two crucial roles: some of them (saprophytic) are unique in their ability to decompose woody material (rich in lignin), while others (mycorrhizal) are the food transportation system of the soil. The body of a fungus is composed by fine and intricately branched threads called hyphae, which form a dense network referred to as mycelium. In seasonal cycles, the mycelium gives rise to the more recognisable mushrooms; these are fruiting structures and contain the spores that allow a fungus to spread far and wide and populate new ground.
A single fungus’ mycelium can extend over a surface of 4 square miles, as in the case of the largest living being on earth — a specimen of Armillaria ostoyae living in Malheur National Forest, Oregon. This gives fungi the ability to populate a vast volume of soil, scouting for nutrients and water, and transporting them over large distances. On the other hand, most plants can’t extend their roots anywhere as far, and thus started to make advantage of their neighbouring fungal networks as early as 400 million years ago³ — as soon as they started colonising land. In its own root zone, a plant can trade the surplus of sugars produced by photosynthesis in exchange for increased access to water, nutrients and protection from pathogens⁴. In some cases, plants which are located far away from each other can exchange nutrients via the fungal network that connects them underground. In temperate forests, young trees benefit from the ability of older (and taller) ones to reach up to sunlight; so much so that up to 40% of their carbon can come from their grown-up neighbours’ photosynthesis⁵ via the fungal wood wide web.
Figure: The wood wide web, mycorrhizal fungi in temperate forests allow the exchange of carbon among trees. From: New Zeland Geographics.
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Are all mycorrhizae the same?
But not all mycorrhizal fungi are the same. First of all, fungi can interact with plants either from within or without their cell walls. Among the ones that colonise the cells of the host plant and from there extend into the soil, the most numerous are arbuscular mycorrhizal (AMF), whereas ectomycorrhizal (EMF) grow on the roots’ surface and form webs around them. EMF are the favourite helpers of conifers and deciduous trees, with which they sometimes form exclusive one-to-one relationships, such that only a specific species of fungus pairs up with a given species of tree⁶.
AMF are found in 85% of all plant families and are hosted by most agricultural crops as well as grasses, shrubs, and some trees⁶. For this reason, AMF have been used in agriculture and horticulture as a biofertilizer, and are available commercially to use in home gardens. More than 150 species of AMF are known, and they can associate with over 200,000 plant species⁷. AMF live only for a short period of time (8.5 days on average⁸), acting as perfect guests: they do not mix their cell contents (protoplasm) with the host’s ones, but form either balloon-like or tree-shaped structures (arbuscules — from the latin arbor, “tree”) located within the host cell membrane, where nutrients are stored and the exchange takes place⁷.
Figure: Left: Mycelium in a temperate forest, from Nationalforests.org. Right: Ectomychorrizae in Pinus sylvestris
The challenging life of an arbuscular mycorrhiza
The life span of AMF is strongly correlated with their ability to deliver nutrients to the host plant, and is therefore regulated the plant’s demand⁹. Plants can also remove inefficient partners, thus encouraging another one to come forward¹⁰. Before dying, arbuscular mychorrizal reproduce asexually by means of spores, which can germinate even without the presence of a host, although the speed at which their hypae can spread significantly increases in the presence of root exudates¹¹. Some researchers have suggested arbuscular mycorrhizal might have been asexual for millions of years¹². Once germinated, the spore inoculates the nearest host and a new life cycle begins. In order, to survive, however host plants must be found by the newborn fungus, or else it will starve to death.
As you might have already guessed, mychorrizal fungi are very delicate organisms. After all, many of us have experienced how easy it can be to physically remove the hyphae of molds. Any significant soil disturbance, such as tillage, digging and compaction have been shown to reduce AM fungi’s diversity and lifespan¹³. Other practices, common in conventional agriculture, also have a detrimental impact on mycorrhizal networks. For istance, the application of any fungicide as a disease control measure also kills AMF¹⁴, as we might expect. Furthermore, low pH conditions (acid soil) often induced by chemical fertiliser use¹⁵.
Monocultures also have a negative impact on arbuscular populations; in particular, brassicacae (plants belonging to cabbage family) do not form associations with AMF¹⁶, and therefore can act as a biological gap, thus slowing down their spread across larger areas. Conversely, a large variety of crops does encourage the establishment of symbiotic relationships, because “there may be different strains of mycorrhizae that will like something better than another one” — as suggested by J.C. Cahill of the University of Alberta. Cahill also points out how extreme soil conditions, such as drought, high temperatures, waterlogging, frosts can affect AMF.
Finally, and most importantly, the absence of living vegetation over large areas (fallow ground), starves and in the long term wipes out all mycorrhizal life from the soil¹⁷.
Interestingly, however, recent field experiments suggested that the negative impacts of the agricultural practices discussed above has been overestimated by previous research; in fact, the recovery of mycorrhizal systems through their interaction with other soil microbes is still poorly understood and could be more efficient than we believe¹⁸.
Figure: Arbuscular mycorrhizal fungus in a colonised root system. Fungal hyphae (E) increase the surface area of the root and uptake of key nutrients while the plant supplies the fungi with fixed carbon (A=root cortex, B=root epidermis, C=arbuscle, D=vesicle, F=root hair, G=nuclei). Credit: Amarachukwu Ifeji
2. How they impact plants and ecosystems
The importance of finding the right match
Associations between arbuscular mycorrhizal fungi and plants are not always straightforward. Over a century of research has shown that, similarly to ectomycorrhizae, arbuscular partnerships only develop between certain combinations of plants¹⁹. Some plants are generalists, which means that they can associate with several species of AMF. Similarly, some AMF do not show particular preferences, and pair up with hundreds of plant genera. However, this is not always the case, and research labs around the world have been investigating several combinations of fungi and plants, in diverse soil types and conditions, to test when and where mycorrhizae are formed²⁰.
Unfortunately, a lot of conflicting information has been published, and it is very difficult to determine with certainty whether a specific fungus will associate with a given plant²¹. Most likely, this disagreement is due to different methods used to determine when colonization had happened, and when it was beneficial. Recently, several efforts have been made, and methods proposed, to unify the body of literature and collect all the significant and most up-to-date information available to us. A huge database, MycoDB, has been created, and collates all the information about the effect of specific AMF species on the productivity of single plant species⁷.
One of the latest insights from research shows that plants whose nitrogen (N) content is higher do rely less on mycorrhizal fungi³³.
Figure: Different plant species rely differently onthe same population of AMF. The graph shows the belowground surface area provided by roots (grey) and AMF hyphae (white)³³
From mutualism to parasitism: the full symbiotic spectrum
Knowing what happens when fungus X meets plant Y is extremely important, not only to target specific situations. In fact, although some combinations are destined to result in mutual benefits, others can turn out to be harmful for the host plant, to the advantage of the mycorrhizal fungus.
Symbioses can indeed be mutualistic, commensalistic or parasitic. Mutualistic associations benefit both participants (as is the case for oxpeckers and impalas, or clownfish and sea anemones²²), while in commenalistic ones only one member gains an advantage while the other is neither benefited nor harmed. In the worst case scenario, parasitism takes place, and one organism exploits the other to its own advantage, thus harming it (the obvious example being viruses, which are obligate parasites).
Although most of the research so far has focused on the successful stories typical of mutualist mycorrhizae, in the last few years some research groups around the world have started to explore what happens when the fungus parasitises its host. This information will prove fundamental in order to discern whether introducing arbuscular fungi to a garden or a farm is the right thing to do.
To complicate things, as we will see, what determines whether a fungal symbiosis is beneficial to a plant is not only the combination of species, because some fungus-host pairs can start as mutualist and gradually become parasitic.
Figure: Not all plants establish beneficial partnerships with AMF. The graph shows Mycorrhizal growth dependency (MGD) as calculated from relative biomass differences between AM and non-mycorrhizal plants³³
Mutualist mycorrhizae: a wealth of beneficial effects
It is hardly difficult to explain why so much of the scientific literature, as well as gardening clubs and fertiliser suppliers have been leaning towards over-optimism when talking about mycorrhizal fungi. Indeed, the list of documented impacts of symbiotic fungi range from stimulating plants root growth and crop yields, to ecosystem biodiversity regeneration and greenhouse gases reduction. Here I provide a list of the beneficial effects generally accepted among the scientific community, along with all the references you will need, should you wish to dig a bit deeper.
In numerous studies, agricultural crop yields have been shown to increase where higher densities of arbuscular mycorrhizal were measured²³. However, yields are not directly proportional to the extent of the AMF infection, but to the physiological effect they have on plants⁶
Due to their role in plant nutrition, symbiotic AMF could also have a positive impact on the quality of vegetables, by increasing the concentration of both macro and micronutrients²⁴. One of the most inestimable benefits of mycorrhizae is in fact the facilitation of phosphorous uptake. Phosphrous (P) is critical macronutrient for plant growth, but it is one of the most difficult nutrients for plants to acquire. Even though it might be present in large quantities, often most of it is poorly available because of the very low solubility of phosphates of iron, aluminum, and calcium. Mycorrhizal symbiosis is the most common strategy plants evolved to access phosphorous in its available form, as negatively charged Pi ions²⁵. The uptake of phosphorous in inoculated roots can be three to five times higher than in non-mycorrhizal roots²⁶.
AMF benefit entire ecosystems on many levels, as they improve soil structure and aggregation and drive the structure of plant communities, biodiversity, nutrient capture and productivity²⁷
Mycorrhizal fungi in general are responsible for reducing emissions of nitrogen oxide, which is one of the greenhouse gases that drive climate change²⁸Plants tolerance to stressful soil conditions, such as drought and high salinity, is improved in the presence of AMF²⁹
Arbuscules can reduce the impact of heavy metals in the host plants³⁰. This can also be used for phytoremediation, i.e., the use of plants to clean up soil, water and air in contaminated areas³¹
Increased resistance to soil-borne pathogens, both fungal and bacterial, has been widely observed on plants colonised by AMF, although we still don’t know what the mechanism involved is. Some argue that the beneficial fungi physically inhibit the attack of parasitic ones, other researchers have discovered that plants refine their own defences as a result of the chemical interaction with the mycorrhizal fungi³².
Figure: The benefits of AM-partnerships from Jacott et al, Agronomy 2017, 7(4)
Parasitism: the dark side of the fungus
Already in the 1980’s, plant scientists knew very well that mycorrhizal fungi could not only be parasitic, but also start as friendly allies and end up as deadly enemies. Studies have shown parasitic behaviour in various vegetable crops, and in most cases the culpable fungus was one that is also known to form mutualistic partnerships, even with the same plants. So, when do mycorrhizal fungi turn their backs to plant needs and start to exploit them?
As pointed out by Johnson et al.³⁶,
Mycorrhizal fungi might be considered to be parasitic on plants when net cost of the symbiosis exceeds net benefits. Parasitism can be developmentally induced, environmentally induced, or possibly genotypically induced.
In practice, this means that there are many ways in which the amount of plant resources allocated to an AMF (the costs) might end up exceeding the benefits it gains from associating with it.
To begin with, environmental factors are extremely important. For instance, a mycorrhiza might become parasitic in a chemically fertilised soil, where the plant already has enough phosphorous and water, and ends up providing carbon to the fungus for free. Similarly, in reduced light conditions, a plant host might be unable photosynthesise quickly enough to provide carbon both for its own growth and to satisfy the fungus needs; often, this means that the plant will slow down its growth or general productivity. Costly and detrimental partnerships can also occur where plant densities are low, and AMF enter in competition with each other and the hosts’ roots.
Furthermore, at different stages of the development of a plant, things can look differently. As a seedling, plants’ needs for nutrients are very low (as most of them are drawn from the seed’s store), and therefore the costs are higher; however, this short-term disadvantage is usually compensated by the long-term advantages of having easier access to soil resources.
To complicate things even further, genetics play an important role, as we already know from the fact that not all matches are successful. Genetic predispositions interact with environmental factors, as well as complex ecosystemic dynamics that result from the interaction of several types of plants and life in the soil.
3. Applications
Before we explore how mycorrhizal fungi can be used in agricultural and horticultural situations, it is important to notice that, contrary to what is commonly believed, where a mutually beneficial mycorrhizal symbiosis is present, the host plant has fewer roots, because it can make advantage of the fungus foraging ability, thus economising on root tissue³³. Let’s pause on this idea for a moment. Perhaps some of you have come accross the comparative photographs that mycorrhizal suppliers use to reinforce their claim that inoculated plants have healthier roots systems (an example has been included below). These can be interpreted in two ways:
if the supplier is trying to tell us that the roots of the inoculated plant are more numerous, they probably have a limited comprehension of how mycorrhizae work;
if the intent is to show the overall biomass of roots plus mycorrhizal hyphae, rather than roots alone, then the supplier is just diplaying how a mycorrhizal and a non-mycorrhizal specimen look. However, having AMF hyphae around its own roots, as you now know, does not mean that a plant is benefiting from them²³, and even if it was, it would not ensure that its productivity will be increased⁶.
Figure: A comparison of the roots of inoculated and uninoculated barley plants, from Teaming with Fungi (J.Lowenfels)
A growth stimulant?
As discussed in the previous section, when mycorrhiza is mutualistic, the productivity and general health (sometimes grouped under the term fitness²⁵) of the inoculated plant are increased, alongside the biodiversity of microorganisms in the soil.
However, researchers have started to point out that mycorrhizae can be parasitic more often than we originally thought. J. Cahill goes as far as saying the interaction between plants and soil life is so complex that if we introduce a diverse mix of mycorrhizal fungi in a generic soil, 50% of the AMF are potential parasites³⁴. Therefore, if we are mainly interested in the performance of individual plants, rather than the ecosystem’s diversity and the other potential benefits of mycorrhizae, we should take some precautions before spreading them indiscriminately over our garden or field. A few considerations to make, in the light of the previous sections, are the following:
Verify that your soil is not already rich in available (soluble) phosphorous, as this might cause mycorrhizal fungi to be parasitic;
Although mycorrhizae improve nutrient uptake, these nutrients need to be present in the soil in the first place. Therefore, especially if plant performance is a priority, it is worth ensuring that soil is chemically balanced³⁵
Avoid introducing non-native species of AMF, as these are less likely to establish readily and healthily in a foreign soil food web;
If possible, you should always test mychorrizal action on some individual plants first, and compare their subsequent performance with other individuals of the same species or family. This will give you an indication of whether any beneficial effects are observed in your soil ecosystem;
Notice that AMF don’t associate with Brassicas and plants that thrive on acidic soils (low pH), such as Rhododendrons, Azaleas, Heathers, Cranberries and Blueberries;
In vegetable gardens or farm operations, increase the crop diversity and rotate brassicas often, as to encourage permanent establishment of a diverse community of AMF;
Avoid tillage and digging, as these destroy fungal hyphae;
If want mycorrhizae to establish permanently in a vegetable or flower bed, whenever plants are removed to make room to another crop, their roots should be left in the soil. This might be easier said than done, especially on plants with strong and branched taproots. However, what is crucial is to leave the finer roots in the soil, as these have a higher density of mycorrhizal fungi; this can be achieved by pulling plants up carefully or cutting their stem below ground;
Do not leave soil uncultivated over winter or at any given time for long periods, because mycorrhizal fungi need hosts to survive (incidently, weeds as fixing agents in disturbed soil do, among other things, provide a home for stranded mycorrhizal fungi.
Commercial inoculants: are they effective?
Although we may legitimately expect that inoculants contain viable spores, some research has shown that more than 50% of the products available to home gardeners are not viable³⁷. This is especially true of mixes that are made up of spores only. Products consisting a clay inert substrate (white granules) inoculated with living mycelium may be more effective.
A Regenerative tool
The soil is the great connector of lives, the source and destination of all. It is the healer and restorer and resurrector, by which disease passes into health, age into youth, death into life. Without proper care for it we can have no community, because without proper care for it we can have no life. (Wendel Berry³⁷)
Despite their potential side effects on individual plant productivity, the benefits of mycorrhizal symbioses to ecosystems, the soil food web, plant biodiversity and the earth’s climate cannot be stressed enough.
All those gardeners, landscapers, farmers and policy-makers who are interested not only in a sustainable way of maintaning and managing ecosystems, but in regenerating the biological balance that centuries of naive human action have seriously impaired, have long found in mycorrhizal fungi an invaluable ally. Regenerative agricultural and gardening practices, such as no-dig gardening, organic no-till crop production, agroforestry and others are heavily dependent on the fungal network that connects plants and soil microbiology, redistrubuting nutrients and enhancing synergistic dynamics.
In this sense, mycorrhizal fungi are a tool of the future, and we need to understand them better in order to avoid using them improperly or ineffectively.
Further (non-technical) reading
Mycelium running: How Mushrooms Can Help Save the World, Paul Stamets If you are after an intriguing book on fungi, Paul Stamets’ book won’t disappoint you.
Mycorrhizal planet M. Phillips For those interested in understanding mycorrhizal, with particular attention to their use in permaculture and regenerative agriculture, this is a rich and pleasant read.
References
The scientific articles and all the other references corresponding to the numbered footnotes can be opened by clicking on the link below. They are in a google doc format. I suggest that you open them in a separate tab (by pressing CTRL+left-click) so that you might refer back to them while you read the article, without the need to scroll back and forth.