Mycorrhiza – Definition, Types, Examples, Importance

Mycorrhiza Definition

• A mycorrhiza is a symbiotic relationship between a fungus and a green plant. The plant produces organic molecules such as sugars through photosynthesis and provides them to the fungus, while the fungus provides the plant with water and soil-derived mineral minerals such as phosphate.
• The name mycorrhiza is derived from two Greek words: mykos, which means fungus, and rhizos, which means roots.
• Mycorrhizas are present in numerous habitats, and their ecological success reflects the genetic and physiological diversity of the endophytic fungi.
• There are around 6,000 mycorrhizal species in the Glomeromycotina, Ascomycotina, and Basidiomycotina, and the introduction of molecular technology is increasing this number.
• The taxonomic position of the plant and fungus partners determines the types of mycorrhiza, with endomycorrhizas and ectomycorrhizas being the primary distinction.
• In ectomycorrhizas (ECMs), which are characteristic of trees and shrubs, hyphae stay extracellular and induce significant alterations in root development, whereas their presence induces relatively mild changes in epidermal or cortical cells.
• In endomycorrhizas, including arbuscular (AMs), ericoid, and orchid mycorrhizas, the hyphae penetrate the root cells to form an intracellular symbiosis, regardless of the plant host.
• Comparatively, ericoid and orchid mycorrhizas are restricted to the order Ericales and family Orchidaceae, respectively, whereas AMs are common throughout numerous plant taxa.
• It is believed that the mycorrhizal state arose as a technique of improving the uptake of inorganic nutrients by plants, as the fungal hyphae issuing from the root surface are able to investigate a wider volume of soil than roots and root hairs alone could.
• To make this a real symbiosis, the fungus must get carbohydrates from the photoassimilates of the host plant in order to sustain its growth.
• There is evidence that the role of mycorrhizae extends beyond nutrient acquisition to include access to less readily labile nutrients (organic nutrient sources), improved root access to water, and protection of roots from pathogenic bacteria and fungi, as well as grazing by soil invertebrates.
• A further characteristic of mycorrhizae is their capacity to protect plants from heavy metals by reducing metal transfer into aboveground plant components.
• The potential of mycorrhizae to increase plant development has been utilised in agriculture and forestry due to mycorrhizae’s nutrient absorption-enhancing characteristics.
• The addition of mycorrhizal fungi at an early stage of plant development has been demonstrated to produce larger plants, particularly under nursery circumstances, compared to uninoculated plants.
• The commercial manufacture of mycorrhizal inocula for use in horticulture, agriculture, forestry, and restoration has resulted from the discovery that mycorrhizal inoculation of plants in polluted soils often promotes plant survival and growth.

Types of Mycorrhizae

Mycorrhizas are often classified as either ectomycorrhizas or endomycorrhizas. The hyphae of ectomycorrhizal fungi do not penetrate individual root cells, but the hyphae of endomycorrhizal fungi invade the cell membrane and pierce the cell wall. Endomycorrhiza consists of arbuscular, ericoid, and orchid mycorrhiza, whereas ectoendomycorrhiza comprises arbutoid mycorrhiza. Monotropoid mycorrhizas constitute a unique category.

1. Ectomycorrhiza
2. Endomycorrhiza

A. Ectomycorrhiza

• An ectomycorrhiza is a type of symbiotic interaction between a mycobiont (fungal symbiont) and the roots of several plant species.
• Mycobionts are typically derived from the phyla Basidiomycota and Ascomycota, and less frequently from Zygomycota.
• Ectomycorrhizas occur on the roots of approximately 2% of plant species, typically woody plants from the families of birch, dipterocarp, myrtle, beech, willow, pine, and rose.
• In fields including ecosystem management and restoration, forestry, and agriculture, ectomycorrhiza research is becoming increasingly significant.
• Unlike arbuscular mycorrhiza and ericoid mycorrhiza, ectomycorrhizal fungi do not invade their host’s cell walls.
• Instead, they produce the Hartig net, which consists of highly branching hyphae forming a latticework between epidermal and cortical root cells.
• Ectomycorrhizas are distinguished from other mycorrhizas by the creation of a dense hyphal sheath enclosing the root surface, known as the mantle.
• This covering mantle can be as thick as 40 m, and its hyphae can reach several centimetres into the surrounding soil.
• The hyphal network aids the plant in absorbing nutrients, such as water and minerals, and often aids the plant’s ability to tolerate difficult conditions. The fungus symbiont receives access to carbohydrates in exchange.
• The economically valuable and edible truffle (Tuber) and the lethal death caps and destroying angels are well-known EcM fruiting bodies (Amanita).

Morphology/Structure of Ectomycorrhiza

The mycosymbiont’s biomass, as the name implies, is located largely outside the plant root. The basic structure of a fungus consists of three parts: The Hartig net, composed of intraradical hyphae; the mantle, a sheath that encircles the root tip; the extraradical hyphae and associated structures, which permeate the soil.

Hartig net

• To create the Hartig net, hyphae (typically from the inner section of the surrounding mantle) grow into the root of the plant host.
• Hyphae establish a network between the outer cells of the root axis by penetrating them and growing in a direction perpendicular to the axis.
• Here is where nutrition and carbon exchange takes place, at the point of contact between fungal and root cells.
• Penetration varies in strength from species to species. The Hartig net in Eucalyptus and Alnus only extends as far as the epidermis, but in most gymnosperms, it travels much deeper, into the cortical cells and even the endodermis.
• Increasing surface contact between fungus and root cells occurs as cells of several epidermal kinds elongate along the epidermis.
• Since this extension is not seen in the vast majority of cortical Hartig nets, it may indicate that various species employ unique methods for maximising surface contact.

Mantle

• The root is covered by a hyphal sheath called the mantle, which often contains more biomass than the Hartig net interface.
• The mantle can have a variety of structures, from a disorganised web of hyphae to a well-organized, layered system of tissue.
• These layers are often called “pseudoparenchymatous” because of their resemblance to parenchyma tissue in plants.
• Mantle enclosing the root can hinder its growth. Usually, the root hair development of the plant symbiont that is host to an EcM fungus is inhibited.
• The plant’s cytokinins are induced, which leads to more root branching.
• These patterns of branching can become so broad that a single consolidated mantle can encase multiple root terminals at once. Tuberculate or coralloid ectomycorrhizas are the names given to these kinds of structures.
• Different EcM pairings can be distinguished from one another by the distinctive characteristics of their mantles, such as colour, branching pattern, and level of complexity, which are utilised in conjunction with molecular investigations to confirm the fungus’ identity.
• Although fruiting bodies can be helpful, they are not always accessible.

Extraradical hyphae and linkage

• To make up for the loss of root hairs due to colonisation, the extraradical hyphae of a fungus grow outward from the mantle and into the soil.
• These hyphae can either grow independently or join together to form a rhizomorph.
• Many different types of structures can be made by these composite hyphal organs. Some rhizomorphs consist merely of a linear arrangement of hyphae in parallel orientations.
• Some are more intricately structured than others, with central hyphae that are bigger in diameter than the rest, or hyphae that develop continually at the tip, entering new areas in a manner that apparently resembles meristematic activity.
• The ectomycorrhizal structure known as the extraradical or extramatrical mycelium primarily serves as a transport system.
• It’s not uncommon for them to extend for several yards, keeping a sizable surface area in constant touch with the ground.
• Researchers have found an association between rhizomorph structure and nutrient transfer rates.
• The rhizomorphs of various EcMs can be distinguished by their distinct structures and growth patterns inside the soil, which reflect their unique organisational and discovery techniques. The presence of these distinctions also aids in recognising the symbiotic fungus.
• The ectomycorrhizal fungus can infect neighbouring plants through its hyphae, which spread out into the soil.
• This can result in the development of CMNs, which facilitate the exchange of carbon and nutrients between connected host plants. The addition of the rare isotope carbon-14 to a single tree and its subsequent detection in neighbouring plants and seedlings is just one such case.
• It has been hypothesised that CMNs’ role as a conduit for nutrient transfer plays a role in ecological processes as diverse as seedling establishment, forest succession, and plant-plant interactions. It has been demonstrated that certain arbuscular mycorrhizas transmit signals to plants on the network, alerting them to the presence of pests or pathogens.

Fruiting bodies

• EcM fungi, unlike other arbuscular mycorrhizal fungus, reproduce sexually and develop obvious fruiting bodies.
• The sporocarp, or fruiting body, can be viewed as continuing the work of the hyphae that extend outward from the central mass.
• In addition to a high nitrogen content, complex carbohydrates are a common component of its cell walls and spores.
• In order to create fruiting bodies and finish their life cycles, many EcM fungi require the assistance of another EcM fungus.
• Many species, including epigeous mushrooms and hypogeous truffles, have easily identifiable fruit bodies in the form of these familiar fungi.
• The majority of these generate propagules less than 10 m in size, which are capable of being carried great distances by a variety of vectors, such as wind and mycophagous animals.
• Hypogeous fruiting bodies have been hypothesised to attract animals due to the abundance of nitrogen, phosphate, minerals, and vitamins they contain.
• The availability of food at different periods of the year is argued to be more essential than the specific nutrients by some.
• Many studies have employed fruiting body surveys to evaluate the diversity and abundance of a neighborhood’s inhabitants. However, this approach is not ideal because fruiting bodies often disappear quickly and are difficult to spot.

Arbutoid mycorrhiza

• Mycorrhizae of the subfamily Arbutoideae within the Ericaceae plant family are involved in this particular sort of symbiosis.
• But it’s distinct from ericoid mycorrhiza in both its function and the fungi involved, and more akin to ectomycorrhiza.
• One way in which ectendomycorrhiza is distinct from ectomycorrhiza is that its hyphae actually enter the root cells.

Mechanism of Ectomycorrhiza

1. Presymbiosis

• The fungus’ hyphae must first invade the soil and make their way down to the plant’s roots in order to establish an ectomycorrhizal relationship.
• To finally construct the symbiotic Hartig net and accompanying structures, they must encase and infect the root cap cells.
• For this to work, both parties (the plant and the fungus) must adhere to a strict timetable of gene expression.
• There is evidence that genes involved in secretory, apical growth, and infection processes undergo changes in expression during the early, pre-contact phase of ectomycorrhiza, and that volatile organic compounds produced only during the interaction phase play a role in the initial communication between the partners. As a result, it appears that a complicated series of molecular modifications occurs even before the fungus and host plant make contact.
• Plant hosts secrete compounds into the rhizosphere, which can initiate EcM formation by stimulating basidiospore germination, hyphal growth toward the root, and early stages of EcM formation. Some examples of these are flavonoids, diterpenes, cytokinins, hormones, and a variety of other nutrients.
• There is evidence that metabolites secreted by the host can accelerate Pisolithus fungal growth, alter the hyphal branching angle, and trigger other alterations in the fungus.
• Premature expression of some fungal genes away from the plant suggests that crucial fungal genes are induced by soil signals.

2. Symbiosis

• Root cap cells are only the beginning; the fungal hyphae need to continue growing inward to the epidermal cells and multiplying to generate the layers that will eventually produce the mantle.
• Genes involved in translation, cell proliferation, and membrane synthesis/function (including hydrophobins) are all upregulated during fungal mantle production.
• Some polypeptides, known as ectomycorrhizins, are only present when symbiosis is established between a fungus and a plant.
• The creation of ectomycorrhizins is just one example of the fast alterations that occur in polypeptide and mRNA synthesis following fungal invasion.
• Some genes are upregulated, which may facilitate the formation of new membranes at the symbiotic interface. To further understand the mantle’s role in regulating root growth, root hair production, and dichotomous branching, researchers can look to fungal exudates as a potential proxy for the mantle itself.
• The Hartig net originates in the inner, fully differentiated layer of the mantle and invades perpendicular to the root axis to digest the apoplastic region.
• In response to stress, some plant cells produce defensive proteins such chitinases and peroxidases, which can block Hartig net development.
• Despite this, EcM fungi are still able to colonise extensively in the roots of these plants, and by day 21, the resistance symptoms appear to have subsided, suggesting that EcM fungi can dampen the defence response.
• Whenever a fungus and a plant become mutually dependent on one another, they begin exchanging nutrients. Symbiosis-related genes regulate this process as well. Amanita muscaria, for instance, needs a transporter that is only produced when it is in a mycorrhizal relationship in order to take in monosaccharides.
• The expression of the transporter causes the fungus to import more sugar, which prompts the plant host to make more sugar available. Regulated as well is the transfer of ammonium and amino acids from the fungus to the plant.

3. Nutrient uptake and exchange

• Chlorophyll and all proteins in plants can’t be made without nitrogen, hence it’s crucial to plant biochemistry. Nitrogen is typically scarce on land because it is bound up in inorganic debris that is difficult to decompose.
• Thus, fungi that live in symbiosis with plants benefit the host plant in two ways: first, their hyphae may spread further than roots, and second, they can more easily draw nitrogen from the organic matter layer of the soil.
• The soil-fungus interface, the fungus-apoplast interface, and the apoplast-root cell interface are the three interfaces that nutrients must pass through in order to be taken up by plants.
• According to some estimates, ectomycorrhizal fungi take in about 15% of the host plant’s food output and return up to 86% of the nitrogen requirements.
• Growing pressure from the hyphae of the Hartig net zone causes the root cells to bulge outward. When the cell walls of fungi and plants interact, they often merge into one another, making it simple to transfer nutrients from one to the other.
• Hartig net hyphae, found in many ectomycorrhizas, lack internal divisions, producing a multinuclear transfer cell-like structure that aids in the flow of materials between hyphae.
• Protein and ATP-generating organelles (mitochondria and rough endoplasmic reticulum) are densely packed near the hyphal terminals.
• Transporters in the plasma membranes of both fungi and plants appear to be functioning, indicating that nutrients are being transferred in both directions.
• The EcM network’s structure is influenced by the nutrients available to it. When soil nutrients are scarce, a greater proportion of a plant’s growth energy goes into establishing a deep root system.
• Another nutrient that might be scarce in many biomes is phosphorus. There is evidence to imply that orthophosphate is the predominant form of phosphorus transfer. Ribonucleases are enzymes found in some mat-forming ectomycorrhizas that can rapidly degrade DNA to extract phosphorus from nuclei.

4. Non-nutritional benefits

• Water can also be transported via the extraradical hyphae of a plant, particularly the rhizomorphs. These often mature into specialised runners that spread far from the host roots, so expanding the plant’s effective watering zone.
• In addition to protecting plant tissues from infections and predators, the hyphal sheath that envelops root tips serves as a physical barrier.
• Moreover, there is mounting data indicating that the fungi’s secondary metabolites serve as biochemical defence mechanisms against pathogenic fungi, worms, and bacteria that may attempt to infiltrate the mycorrhizal root.
• EcM fungi have been shown in numerous studies to increase plant tolerance to high concentrations of heavy metals, salts, radionuclides, and organic contaminants in soil.

5. Ectendomycorrhiza

• The Hartig net typically originates outside of root cells, although it can occasionally penetrate the cortical cells of a plant.
• According to the needs of their host, several species of ectomycorrhizal fungi can act either as ectomycorrhizas or in the penetrative manner typical of arbuscular mycorrhizas.
• Because there are a symbiotic relationship between arbuscular mycorrhizas and ectomycorrhizas, these connections are known as ectendomycorrhizas.

Importance of Ectomycorrhiza

1. Agriculture

• Mycorrhizae and other ecosystem components are severely harmed by common modern agricultural methods like tilling, using excessive amounts of fertiliser, and applying fungicides.
• Agricultural practises may have unintended consequences for local ectomycorrhizal communities and ecosystems. One example is the reduction in sporocarp production due to increased fertilisation.

2. Forestry

• Transplanting crop trees to new areas often necessitates bringing along an ectomycorrhizal companion in commercial forestry.
• This is especially true for trees that are very specialised for their mycobiont, or for trees that are being planted in an area with novel fungal species.
• Obligate ectomycorrhizal trees, such as Eucalyptus and Pinus species, have been proven to benefit from being planted together in plantations. For these trees to thrive after being planted en masse, an inoculum of local EcM fungi is usually applied.
• As a means of mitigating climate change and reducing greenhouse gas emissions, planting ectomycorrhizal plantations like pine and eucalyptus is sometimes advocated for. However, there is debate over this practise because the ectomycorrhizal fungi of these species tend to reduce soil carbon.

3. Restoration

• The significance of ectomycorrhizas in sustaining their host plants has led to the proposal that EcM fungus might be employed in ecosystem restoration operations with the goal of re-establishing native plant species.
• Since the loss of mycorrhizal fungi from a habitat represents a significant soil disturbance, their reintroduction is a crucial aspect in establishing vegetation and restoring ecosystems.

4. Heavy metals Removal

• Heavy metals are hazardous to all forms of life. High soil concentrations of heavy metals like zinc, copper, cadmium, lead, nickel, and chromium disrupt fundamental metabolic processes and can cause cell death.
• Numerous species of ectomycorrhizal fungi are able to colonise contaminated soils and are resistant to heavy metals. There are other communities that have adapted locally to harsh chemical conditions.
• Additionally, ectomycorrhizal fungi can bind substantial amounts of heavy metals.
• Once inside the cell, heavy metals can be immobilised in organo-metal complexes, rendered soluble, turned into metallothioneins, involved in metal sequestration, and/or retained in chemically inactive forms within vacuoles. Antioxidant detoxification mechanisms may also be present, hence decreasing the formation of free radicals and safeguarding the fungal cell.
• Metals can be exported from the cytoplasm to the apoplast by fungi, a process that also occurs in plants.
• The fruiting bodies of ectomycorrhizal fungus can also concentrate heavy metals.

5. Pollution and phytoremediation

EcM fungi have been discovered to have positive impacts in a variety of contaminated situations, including:

• High salt: Numerous studies have demonstrated that particular EcM fungi can aid their hosts in surviving circumstances of excessive soil salinity.
• Radionuclides: Numerous species of ectomycorrhizal fungus, particularly the Cortinariaceae, are capable of hyperaccumulating radionuclides.
• Organic pollutants: Certain EcM species can decompose persistent organic pollutants (POPs) such organochlorides and polychlorinated biphenyls (PCBs). 2,4-dichlorophenol and tetrachloroethylene are two substances that can be detoxified by EcM fungus, either alone or in conjunction with their host plant.

6. Climate change

• Ectomycorrhizal communities can be influenced by rising CO2 and the associated consequences of climate change.
• In certain investigations, increasing CO2 levels boosted fungal mycelium development and increased EcM root colonisation. Other EcM connections exhibited little sensitivity to high CO2.
• Increased temperatures also generate a range of responses, some unpleasant, and others positive.
• The EcM response to drought is complex since many species give protection against root desiccation and boost the ability of the roots to take up water.
• Thus, EcMs defend their host plants during periods of drought, although they may themselves be harmed over time.

Example

Ectomycorrhizal fungi are largely Basidiomycota and include common woodland mushrooms, such as Amanita spp., Boletus spp. and Tricholoma spp. Ectomycorrhizas can be highly particular (for example Boletus elegans with larch) and non-specific (for example Amanita muscaria with 20 or more tree species) (for example Amanita muscaria with 20 or more tree species).

B. Endomycorrhiza

As the name suggests, endomycorrhiza is a broad term for all mycorrhizal associations when the fungal component is largely internal to the root structure, with fungal penetration into host cortical cell walls.

Types/Classification of Endomycorrhiza

Endomycorrhizas are varied and have been further characterised as arbuscular, ericoid, arbutoid, monotropoid, and orchid mycorrhizas.

1. Arbuscular mycorrhiza

• This group of mycorrhizae is produced by a small number of fungus species (about 150) of the phylum Glomeromycota and a large number of vascular plant species, including grasses, herbs, and trees – especially tropical tree species.
• Fungal hyphae penetrate the epidermal cells through a combination of enzyme activity and hydrostatic force, leaving an appressorium as a hyphal swelling on the surface of the root where pressure rises.
• The hyphae then enter cortical cell walls, push aside the plasma membrane, and branch into tree-like arbuscules to maximise the area of contact between the fungus and the host cell contents.
• This vast surface area allows nutrition and carbon exchange between the symbiotic fungus and plant.
• Traditionally, there are two forms of arbuscule development: Arum and Paris.
• The Arum type forms tree-like arbuscules from multibranched hyphal structures, whereas the Paris type forms arbuscules from vast hyphal coils in the host cells.
• As a result of mycorrhizal fungal colonisation of root tissue, root hair production is inhibited as extraradical hyphae (hyphae extending from the root surface into the soil) effectively assume the job of root hairs to increase the absorptive surface area.
• In several fungal taxa, excluding Gigaspora and Scutellospora, root tissue may include vesicles.
• These are formations of fungi that completely fill the host cell and are stained with lipid stains. The earlier name vesicular-arbuscular mycorrhizae was derived from the presence of vesicles.
• These vesicles are hyphal terminal swellings containing many nuclei and lipid substances. These are believed to involve material storage.
• Spores can be formed either outwardly or internally, within the root.
• Different fungal species produce spores of differing sizes and spore walls with distinctive ornamentation and chitin filament stacking that enable species identification. These spores are spread through the air, water, and grazing animals.

Vesicular Arbuscular Mycorrhizae (VAM)

• Most species of herbaceous angiosperms are infected by vesicular arbuscular mycorrhizal fungi, but unlike ectotrophic mycorrhizae, they do not develop a thick mantle around the roots.
• Their total weight is likewise considerably smaller (approximately 10%) than the weight of the roots they infect.
• Through root hairs and epidermal cells, the mycelium of VAM invades the host’s roots.
• The hyphae spread between the cortical cells and also enter them, where they create vesicles, which are small ellipsoid-shaped oval structures, and arbuscles, which are highly branched tree-like structures.
• In arbuscles, the fungal hyphae branches are enclosed by the plasma membrane or tonoplast of the cortical cells of the host.
• Therefore, only the corti­cal cell walls are penetrated by the hyphae, not the protoplast.
• The cytoplasmic volume of the cortical cells of host roots may rise by 20-25% as a result of VAM infection.
• The arbuscles serve to expand the region of contact between hyphae and cortical cells for nutrition exchange by two to three times.
• In VAM, minerals may diffuse from arbuscles to cortical cells of the host root either I directly or (ii) by disintegrating and releasing their contents into the latter.
• Similar to ectotrophic mycorrhizae, in VAM some of the finer hyphae from the mycelium surrounding the roots extend into the soil beyond nutrient-depleted areas in order to get a fresh supply of minerals.

The VAM derives its name from the presence of two distinctive features, vesicles and arbuscles:

a. The vesicles are intracellularly generated, thin- or thick-walled vesicular structures that store poly­phosphate and other minerals.

b. The arbuscles are repeatedly dichotomously branched intracellular haustoria (Fig. 4.104). After four days, the arbus­cles are lysed, releasing the stored food as oil droplets, primarily polyphosphate.

There is no fungal mantle, only a loose and extremely thin network of septate hyphae that have disseminated throughout the soil. These hyphae contain many types of spores, including chlamydospores, sporocarps, and zygospores. The superficial hyphae have branches that penetrate the epidermis and then only develop intercellularly in the cortex.

Through repetitive dichotomous branching of penetrating hyphae, intercellular hyphae create arbuscles within the parenchyma of cortex. The penetrated cell’s cell membrane is invaginated and covers the arbuscles.

Additionally, hyphae produce both inter- and intracellular vesicles with thick walls. On nutritional agar, chlamydospores can germinate, but the hyphae cease developing when the food inside the spore is depleted, therefore they cannot be subcultured.

This kind of relationship existed quite early on in the history of terrestrial plants. Together with Rhynia and Asteroxylon, Kidston and Lang (1921) identified a VAM-like organism. Later, Pyrozinski and Mallock (1975) hypothesised the mycorrhization/lichenization relationship as a precursor to the emergence of terrestrial plants.

Mechanism of Arbuscular mycorrhiza

1. Presymbiosis

The development of AM fungus prior to root colonisation is referred to as presymbiosis and consists of three stages: spore germination, hyphal growth, host recognition, and appressorium formation.

a. Spore germination

• Spores of AM fungus are multinucleated entities with thick walls. The germination of the spore is independent of the plant, as spores have germinated both in vitro and in soil under experimental conditions in the absence of plants.
• However, host root exudates can boost the rate of germination. Given favourable conditions of the soil matrix, temperature, carbon dioxide concentration, pH, and phosphorus concentration, AM fungal spores germinate.

b. Hyphal growth

• The proliferation of AM hyphae through the soil is governed by the host root exudates known as strigolactones and the concentration of soil phosphorus.
• Low soil phosphorus concentrations stimulate hyphal development and branching, as well as plant exudation of substances that regulate hyphal branching intensity.
• The branching of AM fungal hyphae grown in medium containing 1 mM phosphorus is greatly reduced, while the length of the germ tube and overall hyphal development are unaffected.
• Phosphorus at a concentration of 10 mM decreased both hyphal growth and branching.
• This phosphorus content is found under natural soil conditions and may therefore contribute to decreased mycorrhizal colonisation.

c. Host recognition

• It has been demonstrated that root exudates from AMF host plants cultivated in liquid media with and without phosphorus alter hyphal development.
• Spores of Gigaspora margarita were developed in the exudates of the host plant.
• Hyphae of fungi cultivated in the exudates of phosphorus-deficient plant roots developed more and formed more tertiary branches than those grown in the exudates of phosphorus-sufficient plant roots.
• AM fungus generated distributed, lengthy branches when growth-promoting root exudates were supplied in low concentration.
• As the concentration of exudates grew, the fungi developed branches that were more densely grouped.
• At the arbuscules with the highest concentration of phosphorus, AMF structures of phosphorus exchange were produced.
• This chemotaxic fungal reaction to the exudates of the host plant is believed to enhance the efficiency of root colonisation in low-phosphorus soils.
• It is an adaptation that allows fungus to efficiently look for a suitable plant host in the soil.

d. Appressorium

• When arbuscular mycorrhizal fungal hyphae come into contact with the root of a host plant, an appressorium or ‘infection structure’ forms on the epidermis of the root.
• From this structure, hyphae can invade the parenchyma cortex of the host.
• AM do not require chemical signals from the plant in order to generate appressoria.
• AM fungi were able to produce appressoria on the cell walls of “ghost” cells in which the protoplast was removed to inhibit signalling between the fungus and its plant host.
• However, the hyphae did not continue to enter the cells and grow into the root cortex, indicating that signalling between symbionts is necessary for ongoing growth once appressoria are produced.

2. Symbiosis

• Once inside the parenchyma, the fungus creates arbuscules, which are highly branched structures facilitating nutrition exchange with the plant.
• These are the structures that distinguish arbuscular mycorrhizal fungi. Arbuscules are where phosphorus, carbon, water, and other nutrients are exchanged.
• There are two variations: The Paris type is distinguished by the growth of hyphae from one plant cell to the next, whereas the Arum type is distinguished by the formation of hyphae between plant cells.
• The decision between Paris type and Arum type is governed mostly by the family of the host plant, but certain families or species are capable of either type.
• The host plant regulates intercellular hyphal growth and arbuscule development.
• Decondensation of the plant’s chromatin suggests an increase in DNA transcription in arbuscule-containing cells.
• To accommodate arbuscules, the plant host cell must undergo extensive alterations. Other cellular organelles multiply while the vacuoles shrink. The cytoskeleton of the plant cell is rearranged around the arbuscules.
• Two other forms of hyphae originate from the colonised root of the host plant. Short-lived runner hyphae emerge from the plant’s root into the soil after colonisation has occurred.
• These are the hyphae that absorb phosphate and micronutrients for the plant’s benefit. AM hyphae have a higher surface-to-volume ratio than plant roots, making their absorption capacity greater.
• Additionally, AMF hyphae are finer than roots and can enter soil pores that are inaccessible to roots.
• The fourth form of AMF hyphae colonises other host plant roots and develops from the roots. The four forms of hyphae have unique morphologies.

3. Nutrient uptake and exchange

• AM fungus are essential symbionts. They have poor saprobic capacity and derive their carbon diet from the plant.
• As hexoses, AM fungus absorb the products of the plant host’s photosynthesis.
• Through the arbuscules or intraradical hyphae, carbon can be transferred from plants to fungi.
• AM performs secondary synthesis from hexoses in the intraradical mycelium. Hexose is metabolised to trehalose and glycogen within the mycelium.
• Trehalose and glycogen are carbon storage forms that can be rapidly generated and destroyed, and they may serve as a buffer for intracellular sugar concentrations.
• The intraradical hexose enters the pentose phosphate oxidation pathway, which generates pentose for nucleic acids.
• In addition, lipid production occurs within the intraradical mycelium. The lipids are subsequently either stored or exported to extraradical hyphae, where they are either stored or digested.
• Gluconeogenesis, the degradation of lipids into hexoses, occurs in the extraradical mycelium.
• The extraradical hyphae store approximately 25% of the carbon transferred from the plant to the fungi. Up to 20% of the carbon in the host plant may be transferred to AM fungus.
• This symbolises the host plant’s substantial carbon investment in the mycorrhizal network and contribution to the organic carbon pool belowground.
• Increasing the plant’s carbon supply to AM fungus enhances phosphorus absorption and transfer from fungi to plant.
• Similarly, phosphorus absorption and transfer are diminished when the photosynthate given to fungus is diminished. The capacity of various AMF species to provide phosphorus to plants varies.
• In some instances, arbuscular mycorrhizae are poor symbionts, contributing little phosphorus while consuming comparatively large quantities of carbon.
• Increased nutrient uptake, notably phosphorus, has been identified as the primary benefit of mycorrhizas for plants.
• This may be the result of a larger surface area in touch with the soil, a greater transfer of nutrients into mycorrhizae, a changing root environment, and an increase in storage capacity.
• Mycorrhizae can absorb phosphorus far more efficiently than plant roots. Phosphorus goes to the root by diffusion or via hyphae, which shortens the distance necessary for diffusion and increases uptake.
• Phosphorus can enter mycorrhizae up to six times faster than it enters root hairs. In extreme instances, the mycorrhizal network might totally assume the role of phosphorus intake, and all of the plant’s phosphorus may originate from hyphae.
• Less is known about the impact of nitrogen feeding on arbuscular mycorrhizal symbiosis and community.
• While substantial progress has been made in unravelling the processes of this intricate connection, there is still more to learn.
• Mycorrhizal activity raises the concentration of accessible phosphorus in the rhizosphere. Mycorrhizae decrease the pH of the root zone by selectively absorbing NH4+ (ammonium ions) and releasing H+ ions.
• The solubility of phosphorus precipitates is increased by a decrease in soil pH. As the inner surfaces of the soil absorb ammonium and disseminate it by diffusion, the hyphal NH4+ uptake also enhances the plant’s nitrogen flow.

Importance of Arbuscular mycorrhiza

1. Phosphorus fertilizer

• The advantages of AMF are greatest in systems with few inputs. Phosphate fertiliser can limit mycorrhizal colonisation and development.
• As the soil’s available phosphorus increases, so does the amount of phosphorus in the plant’s tissues, and the carbon drain on the plant by the AM fungus symbiosis becomes detrimental to the plant.
• A decrease in mycorrhizal colonisation as a result of high soil phosphorus levels might result in copper deficiency in plants, as copper intake is mediated by mycorrhizae.

2. Perennialized cropping systems

• Cover crops are cultivated in the fall, winter, and spring, covering the land during times when it would ordinarily be bare of vegetation.
• Mycorrhizal cover crops can enhance the mycorrhizal inoculum potential and hyphal network.
• Since AM fungi are biotrophic, their hyphal networks are dependent on plants for growth. Growing a cover crop extends the growing season for AM into the fall, winter, and spring.
• The expansion of the hyphal network results from the stimulation of hyphal development. The increase in mycorrhizal colonisation observed in cover crop systems can be attributed in large part to an expansion of the extraradical hyphal network that can colonise the roots of the new crop.
• The extraradical mycelia are able to survive the winter, allowing for rapid spring colonisation and symbiosis in the early season.
• This early symbiosis enables plants to tap into the well-established hyphal network and receive appropriate phosphorus nutrition throughout early growth, resulting in a significant increase in crop output.

3. Soil quality

• Restoration of native AM fungus boosts ecological restoration project success and the rate of soil recovery.
• Due to the development of extraradical hyphae and a soil protein known as glomalin, AM fungus increase the aggregate stability of soil.
• Using a monoclonal antibody (Mab32B11) produced against crushed AMF spores, globalin-related soil proteins (GRSP) have been discovered. It is characterised by its extraction conditions and response with Mab32B11 antibody.

4. Phytoremediation

• Soil inoculation with AM fungus before to reinstalling vegetation in ecological restoration projects is a novel method of repairing land (phytoremediation).
• As a result, host plants are now able to thrive in previously unusable soil, restoring its quality and vitality in the process.
• When compared to noninoculated soil and soil inoculated with a single exotic species of AM fungi, the quality parameters of soils that were introduced with a mixture of indigenous arbuscular mycorrhizal fungi species improved dramatically over the long term.
• Higher legume nodulation in the presence of AM fungus led to greater water infiltration and soil aeration, as well as increased plant growth, increased phosphorus uptake, and increased soil nitrogen content.
• The native AM fungus strains are more effective at removing heavy metals from contaminated soils, restoring their health and making them fit for agricultural cultivation.

5. Rhizosphere ecology

• The rhizosphere refers to the soil region right around a plant’s root system.
• The community and diversity of various species in the soil are influenced by arbuscular mycorrhizal symbiosis. This is either immediately noticeable due to the release of exudates or detectable through a shift in the species and quantity of exudates produced by the plants.

6. Glomeromycota and global climate change

• Both AM fungal communities and interactions between AM fungi and their plant hosts are vulnerable to the effects of global climate change.
• While it’s generally agreed that organism interactions will influence how organisms respond to global climate change, our capacity to forecast the outcome of these interactions in future climates remains limited.
• Recent meta-analyses have indicated that AM fungus can improve plant biomass in drought situations while decreasing plant biomass in trials of simulated nitrogen deposition.
• It has been proven that arbuscular mycorrhizal fungi themselves increase their biomass in response to higher levels of CO2 in the air.

Plants lacking arbuscular mycorrhizae

Mustard plants (Brassicaceae) including cabbage, cauliflower, canola, and crambe are unable to colonise their root systems with arbuscular mycorrhizal fungus.

3. Ericoid mycorrhizae

• Members of the Ericaceae plant family form the ericoid mycorrhiza with several different mycorrhizal fungi.
• Ericaceae are generally found in acidic and nutrient-poor soils, such as those found in boggy areas, heathlands, and boreal woods. This symbiosis is a crucial adaptation to these conditions. Based on molecular clock calculations, the symbiosis probably began some 140 million years ago.
• There are only a few plant families—the Ericaceae, the Epacridaceae, and the Empetraceae—that are known to be connected with the ericoid mycorrhizae. The fungus Hymenoscyphus (Pezizella) ericae was the first endosymbiont of ericaceous plants to be discovered.
• On the other hand, several additional fungus genera (Oidiodendron, Myxotrichium, and Gymnascella) have been discovered to form mycorrhizal relationships with ericoid plants in recent years.
• Fungal hyphae infiltrate cortical cells, typically of extremely tiny roots, and form hyphal coils, much like arbuscular mycorrhizae.
• Ericoid plants have fine roots that have a vascular bundle and a single layer of cortical/epidermal cells on their surface.

Structure and function of Ericoid mycorrhizae

• Ericoid mycorrhizas are distinguished by the formation of fungal coils in the epidermal cells of ericaceous species’ fine hair roots.
• Mycorrhizal ericoid fungi develop loose hyphal networks around the outside of hair roots, from which they penetrate the walls of cortical cells to form intercellular coils that can pack plant cells tightly.
• However, the fungi are incapable of penetrating plant cell plasma membranes. According to the available evidence, coils only work for a few weeks before the plant cell and fungal hyphae begin to disintegrate.
• The coil is where fungi exchange nutrients received from the soil for carbohydrates fixed by the plant during photosynthesis.
• It has been demonstrated that ericoid mycorrhizal fungus have the enzyme capacity to degrade complex organic compounds.
• This may allow certain ericoid mycorrhizal fungi to function as saprophytes. However, it is believed that the principal function of these enzymatic capabilities is to access organic forms of minerals, such as nitrogen, whose mineralized forms are in extremely limited supply in settings generally inhabited by ericaceous plants.

Fungal symbionts of Ericoid mycorrhizae

• The majority of study on ericoid mycorrhizal fungal physiology and function has been conducted on fungal isolates morphologically classified as Rhizoscyphus ericae in the Ascomycota order Helotiales, which is now known to be a Pezoloma species.
• In addition to Rhizoscyphus ericae, culturable Ascomycota such as Meliniomyces (closely related to Rhizoscyphus ericae), Cairneyella variabilis, Gamarada debralockiae, and Oidiodendron maius are recognised as producing ericoid mycorrhizas.
• The application of DNA sequencing to fungal isolates and clones from environmental PCR has revealed diverse fungal communities in ericoid roots; nevertheless, the ability of these fungi to form typical ericoid mycorrhizal coils has not been confirmed, and some may be non-mycorrhizal endophytes, saprobes, or parasites.
• Of addition to ascomycetes, Sebacina species in the phylum Basidiomycota are identified as frequent, but non-cultivable, companions of ericoid roots and are capable of forming ericoid mycorrhizas.
• Similarly, basidiomycetes of the order Hymenochaetales have been involved in the production of ericoid mycorrhizas.

Economic significance of Ericoid mycorrhizae

• Several commercial and ornamental plant species, including blueberries, cranberries, and Rhododendron, have symbiotic relationships with ericoid mycorrhizal fungi.
• Inoculation with ericoid mycorrhizal fungus can affect plant development and nutrient absorption.
• However, ericoid mycorrhizal fungi have been the subject of significantly less agricultural and horticultural research than arbuscular and ectomycorrhizal fungi.

4. Orchid mycorrhiza

• Orchid mycorrhizae are symbiotic interactions between the roots of Orchidaceae plants and many fungi.
• Almost every orchid is myco-heterotrophic at some stage in its life cycle.
• Mycorrhizae are essential for orchid germination because orchid seeds have almost limited energy reserves and receive carbon from their fungal symbiont.
• The symbiosis is initiated by a structure known as a protocorm.
• During symbiosis, the fungus produces peloton-like structures within the root cortex of the orchid.
• Numerous mature orchids retain their fungal symbionts for their whole lives, however the benefits to the adult photosynthetic orchid and the fungus are largely unclear.
• There are around 17,000 species of orchids that acquire nutrition from their basidiomycete fungi partners.
• In certain instances, the plant’s dependence on its fungal partner has become so strong that fungal propagules are carried into the seed of the orchid in order to be present during seed germination and enhance nutrient uptake throughout early plant development.
• This is essential when seed size is so small that the nutrient reserve that can be carried without an endosperm is limited.
• Until photosynthetic capacity develops, the first protocorm growth after seed germination is dependent on the symbiotic fungus for carbohydrate supply.
• In certain species, this may take up to a year, whereas in achlorophyllous orchid species, it never develops.
• The fungus produce arbuscules (skeletons) that are tightly coiled within the cortical cells of the host plant. These fungal coils have a short lifespan and deposit cellulose and pectin into the host cell upon their demise.
• These cells may then be “invaded” by new hyphae with access to these glucose and food sources.

5. Monotropoid mycorrhiza

• These mycorrhizal kinds are exclusive to the Monotropoideae of the Ericaceae family, which have lost their photosynthetic ability and exist as achlorophyllous plants on the forest floor.
• Initially believed to be parasitic on forest tree species, it is now understood that they share mycorrhizal symbionts with their neighbours.
• Through mycorrhizal bridges between their root systems, these plants receive carbohydrates from neighbouring trees.
• Tricholoma, Russula, and Rhizopogon are identified as the fungi responsible for these interactions.
• On their monotropoid hosts, these fungi create fungal sheaths and Hartig nets in a way comparable to the ectomycorrhizal state on trees.
• In addition, they create hyphal pegs from the inner sheath of hyphae into the tangential wall of host cortical cells, one peg per cortical cell.
• It appears that the abundance of peg formations is proportional to the growth and development of the host plant, increasing until flowering and then decreasing.
• Using radiotracers, Bjo rkman established in the 1960s that there was transfer of photosynthates from trees into Monotropa.
• Subsequent research has demonstrated that this is the result of mycorrhizal bridges between the shared fungal hyphae developing mycorrhizae with both the Monotropa plant and the neighbouring trees.
• Less research has been conducted on monotropoid mycorrhizal nutrient acquisition, however it may be inferred that it is comparable to ectomycorrhizal conditions.

Other Mycorrhizae

Arbutoid (Ectendomycorrhizae)

• This unique mycorrhizal relationship exists between two Ericaceae species, Arbutus and Arctostaphylos, and many Pyrolaceae genera.
• A number of ectomycorrhizal fungal species have been shown to form these arbutoid relationships, which consist of a very thin fungal sheath surrounding the root, a paraepidermal Hartig net consisting of fungal penetration between the epidermis, and an outer layer of cortical cells into which the hyphae invade and form hyphal coils (intracellular hyphal complexes).
• It is believed that nutrients and photosynthates are exchanged between arbutoid plants and nearby tree species.

Dark septate endophytes

• These root endophytes have been identified in several plant species from nearly all plant families, especially those living in chilly, nutrient-deficient conditions.
• From roots, members of the genera Chloridium, Leptodontidium, Phialocephala, and Phialophora have been identified. However, many fungal species remain unidentified.
• These fungi penetrate the root by root hairs or cortical cells and build runner hyphae between cortical cells, from which dense, multibranched structures known as microsclerotia form within the host cell.
• Initially, hyaline hyphae frequently deposit melanin in their cell walls, producing in the pigmentation that gives these fungi their moniker.
• Although these mycorrhizal types are prevalent, relatively little is known about their function.
• However, given their greater abundance in oligotrophic and climate-restricted habitats, it is likely that they have the enzymatic ability to acquire nutrients from inorganic sources (see “Mycorrhizal Effects on Plant Communities”).

Function of Mycorrhiza/Mycorrhizal Function

The conventional understanding of mycorrhizal function is that they facilitate the uptake of inorganic nutrients from the soil by the host plant. This is accurate, however it may be an oversimplification of their function, as there is evidence that mycorrhizal connection provides various host benefits. However, the majority of these functions have only been demonstrated in laboratory settings, and the significance of these effects in natural ecosystems has recently been questioned.

Nutrient Acquisition

• Numerous studies have demonstrated that plants grown with mycorrhizae are larger than those grown without mycorrhizae.
• In place of root hairs, widespread and dispersed hyphae provide a greater absorptive surface for nutrient uptake at a lower cost to the plant.
• Through photosynthates, carbon is made accessible to fungi. This may account for almost one-third of the plant’s photoassimilates in some ectomycorrhizal connections.
• To effectuate this glucose exchange, both the plant and the fungus boost the activity of their hexose importer genes. Sugar-dependent gene expression has been shown to endow ectomycorrhizae with a variety of physiological activities, such as resistance to herbivory and pathogenic bacterial and fungal attack.
• Phosphate acquisition in arbuscular mycorrhizae is accomplished by membrane integral proteins, including the PHT phosphate transporter and the P-type HATPase.
• Transport within the fungal tissues of both arbuscular and ectomycorrhizae is predominantly in the form of polyphosphates, which may be deposited in cortical cells as nutrient reserves in the form of polyphosphate granules.
• Within arbuscular mycorrhizae, the production of the particular MtPT4 protein is directly linked to arbuscule development and, consequently, phosphorus uptake. Similar genetic regulation exists for nitrogen uptake.
• For inorganic nitrogen uptake in ectomycorrhizal interaction with Hebeloma crustuliniforme, three ammonium transporters and one nitrate transporter have been found.
• For the acquisition of organic nitrogen, both amino acid and polypeptide transporter genes as well as protease and subtilase genes have been found.
• Mycorrhizae’s enhanced nutrient uptake has led to the notion that the growth advantage of mycorrhization is completely nutrient-driven.
• Indeed, experimental, agricultural plant production, and forest nurseries provide abundant evidence of the nutritional advantages of mycorrhizae for enhancing plant development (height and stem diameter), foliar nutrient content and mass, and nutrient content of plant products (peanuts, grain, etc.).
• In a number of instances, it has also been demonstrated that the presence of mycorrhizae promotes plant longevity, particularly during the establishment phase. Mycorrhizae are utilised economically to enhance the growth of agricultural products, forest trees in nurseries, and plants in horticulture as a result of these growth benefits.
• Consequently, the number of companies producing and selling mycorrhizal inoculum for arbuscular mycorrhizae, ectomycorrhizae, and, more recently, ericoid mycorrhizae has increased in recent years.
• Mycorrhizal relationships have a number of non-nutritional benefits, though.

Water Acquisition

• The capacity of mycorrhizal extraradical hyphae and, in particular, ectomycorrhizal rhizomorphs to translocate nutrients from soil to plant also allows them to translocate water.
• This has also been proven to be crucial for plant growth in arid settings. Plant species determine water uptake and the relationship between water and nutrient intake.
• For instance, the presence of arbuscular mycorrhizae on Acacia did not promote plant development under drought stress whether P fertiliser was added or not.
• In contrast, the presence of mycorrhizae in another tropical tree, Leucaena, greatly increased plant development under dry conditions at both levels of P supply.
• Mycorrhizal connections of Acacia roots at depths of 30 metres in Senegal are likely connected with water acquisition rather than nutrient uptake.

Plant Defense

• The presence of mycorrhizae in the root gives some protection against grazing soil fauna as well as plant diseases. This defence seems to have two components.
• The creation of a physical barrier to root tissue by an ectomycorrhizal sheath is one form of defence.
• The second is a biochemical defence system in which secondary metabolites of fungi protect mycorrhizal roots from harmful fungus and bacteria.
• For instance, the presence of Glomus mosseae arbuscular mycorrhizae boosted peanut plant growth by 28%, pod production by 22%, and seed weight by 12%.
• In the presence of two fungal infections, Fusarium solani and Rhizoctonia solani, the presence of mycorrhizae neutralised the growth inhibition of the pathogens for all parameters and boosted yield by 26% (plant weight), 35% (pods per plant), and 39% (relative to pathogen alone) (seed weight).

Mycorrhizae as Food

• It has been reported that fungi are as good a dietary source as beef due to their high nutrient content, specifically nitrogen, phosphorus, minerals, and vitamins.
• Thus, a range of invertebrates, including mollusks and fly larvae, feed on the fruitbodies of ectomycorrhizal fungus basidiomycete mushrooms.
• Numerous species of fly larvae may tolerate the poisonous component of Amanatia spp., amanitin.
• In addition, numerous mushrooms and, in particular, hypogeous fruitbodies (e.g. truffles) provide a significant source of nutrition for small mammals.
• In Australia, 37 species of native and 4 species of feral mammals exhibit considerable mycophagy, with fungus comprising more than 25% (by volume) of the diet of the brush-tailed potoroo (Potorus longipes) year-round.

Role of Mycorrhizae in Agriculture and Forestry

Role in Agriculture

• The mycorrhizal relationship facilitates the development of dichotomous branching and abundant root growth, hence promoting plant growth.
• Ectotrophic mycorrhiza aids in mineral ion uptake and also serves as a reservoir.
• They also aid with nutrient absorption.
• Mycelial association aids in the absorption of N, Ca, P, Zn, Fe, and others in nutrient-deficient soil.
• Mycorrhizal connection is required for orchid seed germination. Mycorrhizal growth in the tuber tissues of orchids (Rhizoctonia repens and Orchis militaris) results in the synthesis of phytoalexins, orchinol and hirsinol. Both chemicals protect against infection by other pathogens by acting as a barrier.
• Inoculating phosphorus-deficient soil with VAM as a biofertilizer provides a particular opportunity for phosphorus uptake.

Role in Foresty

• Mycorrhiza plays a crucial part in the establishment of forests in unfavourable locations, such as barren land, waste areas, and so on.
• In plant succession, trees with facultative endomycorrhiza operate as the pioneering invaders in degraded areas.
• The introduction of mycorrhizal fungi into a forest bed promotes the establishment of mycorrhizal associations, which limit the entry of fungal root diseases. This approach is quite successful against Phytophthora cinnamoni infection in the roots of Pinus clausa.
• Mycorrhiza makes available to plants nitrogenous compounds such as nitrate, ammonia, etc. Thus, it promotes plant growth, particularly in acidic soil.

Benefits of Mycorrhiza

• It increases the absorption of fluids and nutrients.
• The association decreases the need for watering.
• Reduced demand for artificial fertilisers.
• Plant health flourishes and grows resistant to stress.
• Enhanced transplantation success.
• Improves the plants’ ability to survive.
• It makes the plants more disease- and drought-resistant.
• Mycorrhizal plants produce substances that repel insects.
• This increases the plants’ resistance to environmental contaminants.

References

• Dighton, J. (2009). Mycorrhizae. Encyclopedia of Microbiology, 153–162. doi:10.1016/b978-012373944-5.00327-8
• Egerton-Warburton, L. M., Querejeta, J. I., Allen, M. F., & Finkelman, S. L. (2005). MYCORRHIZAL FUNGI. Encyclopedia of Soils in the Environment, 533–542. doi:10.1016/b0-12-348530-4/00455-0 
• Egerton-Warburton, L. M., Querejeta, J. I., Allen, M. F., & Finkelman, S. L. (2013). Mycorrhizal Fungi. Reference Module in Earth Systems and Environmental Sciences. doi:10.1016/b978-0-12-409548-9.05226-x
• Bonfante, Paola & Anca, Iulia-Andra. (2009). Plants, Mycorrhizal Fungi, and Bacteria: A Network of Interactions. Annual review of microbiology. 63. 363-83. 10.1146/annurev.micro.091208.073504. 
• Devi, S. H. , Bhupenchandra, I., Sinyorita, S., Chongtham, S., & Devi, E. L.  (2021). Mycorrhizal Fungi and Sustainable Agriculture. In T. Ohyama, & K. Inubushi (Eds.), Nitrogen in Agriculture – Physiological, Agricultural and Ecological Aspects. IntechOpen. https://doi.org/10.5772/intechopen.99262
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