Mycorrhizal Symbiosis: Underground Collaboration

As an endomycorrhizal fungus, AMF colonises the root cells of plants that it forms a symbiosis with, to complete the most efficient exchange of nutrients¹. The initiation of the relationship begins when the AMF spores begin to germinate in nutrient poor soils, close to a plant, typically a herb or grass⁷ in a grassland environment², which is releasing hormones such as strigolactones and auxin into the soil. These are signalling or priming molecules that encourage the germination of the fungal spores and the production of long hyphae. In response to these signalling molecules, the fungus itself releases similar ‘priming’ molecules that signal to the plant to prepare for contact and symbiosis⁴ and may include a signal to reduce defence systems so that the fungus can easily colonise⁵. It should be noted that, at this point, there has been no physical contact between plant and fungus, and all initial communication occurs through the diffusion of signalling molecules through the soil. If a fungus begins to germinate but doesn’t receive the appropriate signalling molecules from a nearby plant, germination and growth will be slow, stunted⁵ or even reversed as AMFs are obligate biotrophs and so rely upon their relationship with plants to grow and reproduce, and growth in the absence of an appropriate plant host would be a great waste of an already limited store of carbon⁹.

As the fungus grows and spreads through the soil it will eventually contact the root of the signalling plant and will form appressoria, which enable the fungus to penetrate the root and the hyphae to spread inside the root cortex. From here, the hyphae will continue to grow and branch, some between root cells and some within them, until they produce the eponymous arbuscules⁴. These highly branched structures are almost tree-like in appearance and are formed at the end of hyphae as they penetrate within the root cells⁵. Likely as a defence mechanism to protect the cytoplasmic contents of the cell from the fungus⁴ and as a way to increase the efficiency of nutrient transfer due to increased surface area⁵, the plant surrounds the arbuscule with a periarbuscular membrane, creating a compartment in which nutrients can be exchanged⁴. The stage is now set for symbiotic nutrient transfer between the fungus, whose hyphae outside of the plant continue to grow and seek nutrients such as phosphorus and nitrogen both in inorganic and organic forms, and the plant, who produces carbon sources in the form of carbohydrates and fatty acids⁹. After approximately 4-10 days of symbiosis, the arbuscules within the root cells will begin to die⁵ and be degraded by the plant and new arbuscules may form if the symbiosis is still required by the plant¹. This may be an effective way to control the amount of time the plant stays in the relationship, especially in highly changeable environments where symbiosis is not necessary all the time.

In addition to arbuscules, the fungus may also produce vesicles within the plant’s roots. These are life-long storage areas that the fungus uses to store excess carbon, typically in the form of fatty acids¹. The purpose of these vesicles may be to allow the fungus to control how much carbon it uses at any given time and to build up a store for times in which plant photosynthesis is less, such as during the night or in winter.

As mentioned previously, the majority of terrestrial plants form relationships with AMF and it is considered the ancestral and most stable type of mycorrhizal relationship between plants and fungi³. The relationship has evolved over many thousands of years as a way for both plants and fungi to survive and thrive in unfavourable environments, such as calcareous, nutrient poor¹⁰, and highly metallic soils⁷, and, as the type of plants that form relationships with AMFs are wide ranging and include economically important plants such as rice and potato⁴, study of this particular relationship is highly important. However, arbuscular mycorrhizae is not the only type of mycorrhizal symbiosis present in our environment. Let us now move on to a different sort of relationship: that between plants and ectomycorrhizal fungi.

As indicated by the name, the main difference between endomycorrhizal fungi, such as AMF, and ectomycorrhizal fungi is their ability to enter plant root cells¹. Just like AM symbiosis, EM symbiosis begins with the release of hormones and other signalling molecules by both the plant, this time flowering plants⁷, conifers and woody trees in forests¹¹, and the fungus to induce and encourage the symbiosis. When the hyphae of the EMF reach the plant roots, however, they will surround the root tip before entering the root cortex instead of the simple penetration seen by AMF. This thick layer surrounding the root gives the plant protection from soil-dwelling microorganisms and perhaps more efficient nutrient transfer so survival, especially of young plants, is generally greater for those involved in symbiosis with EMF compared to AMF. Once the root tip is surrounded by the fungus, hyphae then enter into the root cortex and begin to surround the individual root cells but do not colonise the inside of these cells as AMF does¹². This Hartig net performs the same role as the arbuscles of AMF, namely nutrient exchange¹. Just like AMF, the fungus provides the plant with phosphorus, nitrogen and micro-nutrients while the plant provides the fungus with carbon in the form of carbohydrates. Interestingly, plants in forest environments tend to allocate considerably lower amounts of carbon to their symbiont compared to those in grassland environments¹³. This can be explained by the fact that AMF, the main type of mycorrhizal fungus present in a grassland environment, are obligate symbionts and cannot obtain carbon on their own, while EMF, the major mycorrhizal fungus in forest environments, are typically facultative symbionts as they can decompose organic material². This ability of EMF to obtain carbon from decaying matter within the soil means that their reliance on carbon given from their plant symbiont is less. Carbon is not the only metabolite that can be scavenged from organic material, however, as nitrogen can also be obtained. This means that, especially in soil where soluble nitrogen is limited, EMF provides a greater amount of nitrogen to their plant symbiont than AMF and is therefore more beneficial in environments such as forests^{2, 6, 12}.

Now that both main types of mycorrhizal symbiosis have been examined, it is time to move on to how these symbioses are used more widely than simple nutrient exchange. Both AMF and EMF hyphae can achieve lengths of hundreds of metres¹⁴ and can form relationships with multiple plants at the same time¹¹. This opens the possibility for communication between plants through the fungus; a possibility that is often realised.

Like the mycorrhizal symbiosis between fungus and plant, a major benefit of a plant-to-plant network is the sharing of resources. It has been shown that older trees, or plants with a resource surplus, can redirect resources such as water, carbon, and nitrogen towards their symbiotic fungus which then transfer these to young plants or those that have a resource deficit, increasing the survival of the receiver plants while having limited consequences for the sender plants¹². This phenomenon has been studied in Douglas firs where the selective sharing of resources between related, rather than stranger, plants through EMFs¹³ within forests composed solely of Douglas firs has been noted and linked to an enhanced regenerative ability of the forest¹². This selectivity relates to a second benefit of CMNs: kin recognition.

Being able to discern between individuals of the same and different species and between related and unrelated individuals is of great advantage to a plant, especially one within a diverse forest environment, as the plant may wish to communicate differently depending on this kinship status. As discussed previously, when related individuals are connected to each other via a CMN, they show great communication and resource sharing compared to when unrelated individuals of the same species are connected. This is due to kin selection as enhancing the survival of a close relative benefits the individual through the perpetuation of their own genes, also referred to as inclusive fitness. That being said, it is not unheard of for plants to communicate and share resources with unrelated individuals and even those of different species. Douglas firs have been shown to thrive more when connected to other species such as ponderosa pine as the pine is able to provide excess phosphorus to the fir which would not be the case in a fir-fir relationship. Similarly, when connected to paper birch, the Douglas fir could enjoy a more stable source of carbon year-round as the two species produced peak carbon at different times of the year. This means that when the fir produced surplus carbon it transferred excess to the birch which was not currently producing enough carbon, and vis versa, benefiting both individuals¹¹. Kin recognition is not only used for the transfer of survival-enhancing resources, however. Defence signals can also be shared through the CMN, allowing connected individuals to prepare for attacks.

When a plant is under attack from a herbivore, it can signal to connected individuals of the same or different species¹³ that there is a threat in close proximity and these receiver plants can then produce herbivore repellent chemicals or herbivore-predator attractant chemicals in order to protect themselves from the threat¹². This is an example of kin selection and inclusive fitness when the transfer is between related individuals and may also be considered inclusive fitness when the transfer is between unrelated individuals as, as discussed previously, diverse networks can provide a better environment for individual survival than mono-species networks.

Until this point, CMNs between different species of plants have been depicted as relatively harmonious and mutually beneficial. However, the transfer of signal molecules can be used for more nefarious reasons. Just as helpful molecules such as nutrients and defence signals can be transferred through fungal networks, so can harmful molecules such as herbicides and negative plant-produced chemicals¹². This can initiate a form of ‘biochemical warfare’¹¹ so participating in common mycorrhizal networks can lend a competitive advantage to plants, especially those in environments with limited nutrients.

In conclusion, plants can benefit from engaging in CMNs through the transfer of nutrients, water, defence signals, and herbicides, and through the recognition of related individuals, as these factors can enhance growth, survival, and fitness, both individual and inclusive.

It may be tempting to assume that, as Common Mycorrhizal Networks appear to serve the purpose of connecting plants and transferring resources between them, the mycorrhizal fungus that allows this connection may not receive the same benefits as when the relationship is exclusively between plant and fungus, due to the increased competition for resources between fungus and the receiver plants. This appears not to be the case, however, as carbon is the most limiting resource for a fungus while other nutrients, such as nitrogen, are typically the most limiting resource for plants. This means that the competition between fungus and plant is unlikely to be direct and so all individuals within the network can typically work in harmony with each other. That being said, as has been discussed previously, carbon has been shown to pass through the fungal network which indicates that the fungus is not keeping all of the resource that is so precious to it. The question still remains, therefore, why would a relationship evolve between fungus and plant which appears to directly decrease the amount of a highly limited resource accessible to the fungus?

As the fungus acts as a mediator between the connected plants, the fungus can take as much carbon as it needs before passing on any surplus to the receiver plant, so the fungus will not be at any direct disadvantage when engaging in a CMN compared to an exclusive plant-fungus relationship¹³. However, it still appears to be unusual for an individual to pass on surplus resources to another species instead of storing them for use when resources become more limited. This is made more understandable when considering that CMNs typically work in both directions. If a fungus can increase the survival of a seedling by passing on surplus carbon, it can secure a future carbon-source as that seedling will grow to become an adult plant which will pass carbon through the CMN¹¹. Compared to a single plant-fungus relationship or even to a relationship between a fungus and multiple plants which does not incorporate a CMN between the plants, a fungus will have increased carbon security if it sacrifices surplus carbon, hence a CMN is beneficial for the fungus long-term.

A point that was discussed briefly in the previous section was that two plants of different species can be connected via a CMN and transfer substances such as water, nutrients, and defence signals to each other. From an evolutionary standpoint, enhancing the survival of a direct competitor should not occur. It was mentioned that different species can produce resources at different times of the year so the transfer of surplus resources to a competitor can be beneficial, however, this element of CMNs may become clearer when considering the benefit of the network to the fungus symbiont. Different species require and supply different resources at different levels and at different times of the year, which secures the carbon-supply for the fungus year-round. Additionally, if one species rapidly decreases in abundance, the fungus, being connected and engaging in relationships with other species, will continue to survive and evolve¹². Furthermore, passing on defence signals produced by damaged plants to unrelated individuals of different species may be a way for the fungus to prioritise and secure their future carbon-source¹¹. It may, therefore, not be a ‘conscious’ decision on the part of the plant to exchange resources and defence signals with another species, but the fungus ‘hijacking’ the network, passing on resources that were transferred to it, consciously or not, by one plant to another to ensure the survival of the receiver and therefore the survival of the network and security of the carbon-source.

In conclusion, the fungus may act as a passive ‘mediator’ between plants or an active ‘hijacker’ prioritising one over another, but either way it benefits from the CMN by receiving a more secure carbon-supply that resists annual seasonal changes and more drastic environmental changes to ensure the continued survival of the fungus.