Arbuscular mycorrhizal fungi (AMF) are soil fungi that form a symbiosis with the majority of the terrestial plants, penetrating cortical cells of vascular plant to from arbuscule where nutrients are exchanged for carbohydrates. This mutualistic association has been shown to help in production of plant growth hormones, increase nutrient availability and inhibit root pathogens.
The arbuscular mycorrhizal (AM) symbiosis is formed by all members of the Glomeromycota: a fungal phylum that hosts approximately 300 morphospecies (though the numbers and classification of the entire group is under ongoing revision). These fungi are delineated from other phyla by their reproduction cycle, which is essentially the same as the mycorrhization process as these fungi are entirely dependent on forming plants associations to acquire carbon.
The AM symbiosis develops in a somewhat similar manner to other mycorrrhizal fungi (i.e. recognition, attachment, penetration, and establishment with and in the root), but there are several unique structural features that define the AM type, and variations of which are used to delineate species. The key stages to AM formation are:
- A glomeromycotan spore germinates, sending out a germ tube to create a primary mycorrhizal network that can only survive for around 7 days on its own before running out of carbon stores.
- A plant releasing strigolactones to attract the fungus and increase hyphal branching, while the fungus releases “myc factors,” (lipochitooligosaccharides) that trigger structural changes in the root that will help accommodate the fungus.
- The mycelium encounters the root surface, attaches, and produces an appressorium (or hyphopodium) to enter the root through an entry point between epidermal (root surface) cells. The plant allows the fungus to enter, usually when it is need of phosphorus or nitrogen, which the fungus readily provides in exchange for carbon from the plant (“C for P”).
- Intercellular hyphae branch and grow between the root’s cells. Some hyphae may terminate in a vesicle (≥100 μm in diameter) that stores lipids, nuclei, and other cell components, and may also serve as a post-winter propagule (though these are not found in genera in the Gigasporaceae, such as Gigaspora or Scutellospora). Vesicles may grow in the intercellular space, or inside a root cell.
- Some hyphae will penetrate the cell wall of roots and form Paris-type arbusculate coils of hyphae or Arum-type arbuscules that are highly branched and look somewhat like microscopic trees.
- The root cell significantly modifies its cytoskeleton and cell wall to accommodate the growing arbuscule, and eventually forms a periarbuscular membrane around the arbuscule, between which an apoplastic space is filled with a fluid matrix that enables nutrient exchange.
- The fungus travels between cells, rapidly creating arbuscules in adjacent or nearby cells until the colonization percentage plateaus (e.g. 60% in one study with tomatoes). Arbuscules take 2–3 days to form and last for around 4–15 days, after which time they break down and the plant cell returns to normal becomes filled with another arbuscule.
- Extraradical (“outside root”) coenocytic or sparsely septate hyphae will travel in the soil (the mycorrhizosphere) to gather nutrients (most notably nitrogen [as nitrate, ammonium, and amino acids, which are then released to the plant as ammonium] and inorganic phosphorus) sources and water. In one square meter of healthy soil, the surface area of AM mycelium may be as much as 90 m2.
- Some genera (e.g. Gigaspora or Scutellospora) also produce extraradical vesicles in the soil that seem to serve similar functions as vesicles found inside roots.
- Large, thick-walled, and multi-nucleate asexual spores are produced singularly or in clusters (“sporocarps”) along the length of hyphae or at hyphal tips. These are dispersed by animal and insects, though some wind dispersal may also occur.
Some of the best-studied genera are Glomus, Gigaspora, Acaulospora, and Sclerocystis. Glomus is the largest genus, hosting more than 70 morphospecies. Some of the best-studied species include:
- Rhizophagus intraradices
- Funneliformis mosseae
- Gigaspora margarita
AM structures are found among the oldest plant fossils with roots (e.g. Aglaophyton species), dating back to approximately 450 million years ago. As plants evolved and spread around the world over the eons, the AM symbiosis persisted to the point that we now find the relationship among 85–90% of plant species, making it the most ubiquitous and abundant terrestrial symbiosis today. Example AM plants include shrubs, wildflowers, grasses, and many broadleaf and coniferous trees (e.g. redwood [Sequoia], cedar [Thuja], and juniper [Juniperus] species).
The relationship is found on all continents except Antarctica inhabiting grasslands, forests, deserts, aquatic environments, salt marshes, and most other ecosystems. It is common at lower elevations where neutral or slightly alkaline, mineral-rich (alluvial) soils dominate, flora and fauna diversity is rich, and rainfall is less abundant. The AM symbiosis tends to be the dominant mycorrhizal type in ecosystems where decomposition is rapid, creating a good supply of nitrogen relative to phosphorus (e.g. tropical and most temperate systems).
Because these generalist fungi can also associate with many species of plants simultaneously, they can also form an indefinitely large common mycelial network throughout an ecosystem to distribute resources and information amongst all those involved.
The myc factors used to induce AM synthesis are so effective that it is increasingly thought the nod factors used by nitrogen-fixing bacteria were developed to exploit this relationship as the compounds are very similar. Similarly, parasitic plants in the genus Striga use the strigalactones released by plants to trigger germination of their seeds – enabling the Striga plant to grow when a host plant is nearby.
See the document in the download section of this lecture for a list of most of the major plant categories that form AM.s are not found in all species.
AM Fungi for Plant Health
Research over the last few decades has helped solidify the importance of AM fungi in plant and soil health, with some of the most striking findings being in the ability of the fungi to increase plant nutrition and health.
For example, in grasslands, AM fungi may increase plant diversity by up to 30%, while in desert environments, they are critical for plant hydration – especially cacti, which have thick fleshy roots and few or no root hairs. The yield and overall health of many crop plants is also improved by AM inoculation, with the growth rates of maize, wheat, barley, and onions being shown to increase by two, three, four, and six times, respectively, when in symbiosis with AM fungi.
Much of this increase in health can be attributed to the increased access to phosphorus and nitrogen, which also helps reduce fertilizer inputs by as much as 40%. In leguminous plants, AM fungi also assist nitrogen-fixing bacteria by providing much of the phosphorus, copper, and zinc needed for nitrogen fixation. Conversely, the bacteria may increase phosphorus uptake in the fungus or plant through bacteria’s own release of phosphatases and organic acids. The nitrogen-fixing bacteria can also influence AM spore germination and growth rates, just as the myc factors of the fungus may increase nodulation.
Beyond nutrient exchange between plant and fungus (and plants sharing the same common mycorrhizal network), AM fungi have also been shown to transmit other types of information or signals between plants connected by a common mycelial network. In one study, when AM plants were attacked by aphids, other plants sharing the CMN (yet not in proximity to the insects) began producing compounds to defend against the aphids.
AM fungi have also been shown to defend against root-infecting pathogens, such as various Fusarium fungal species and Phytophthora water molds. Fusarium species can be 3–10 times less abundant in the roots zones of AM-associated tomato plants when compared to non-mycorrhizal tomato plants. Proposed mechanisms resulting from the AM symbiosis that increase the plant’s defense against pathogens (and which likely work in concert and not isolation) include:
- Direct competition (e.g. for carbon, which the AM would directly get more of from the plant)
- Production of antibiotics or inhibitory compounds by the fungus
- Changes in plant metabolism and exudation patterns
- Improved plant nutrition leading to increased resilience in response to tissue damage
- Alterations in the soil microbiota and development of pathogen antagonism
These fungi have also been shown to reduce the stress of salinity, drought, and heavy metals on plants, making them essential components of habitat revitalization efforts.
Unique AMF Traits
Alongside the uniqueness of glomalin, the Glomeromycota hosts a number of other unusual traits that makes them a fascinating topic of study.
How glomeromycotan adapt and evolve is unclear as they are “ancient asexuals” that have never been shown to go through a “normal” sexual stage of nuclear recombination. With their added dependence on plants and unusual inability to be cultured in isolation (axenicly), the fungi would seem highly susceptible to attack by other organisms or to have developed unstable genetics, yet AM fungi have proven to be among the most successful and widespread eukaryotes in the world.
Two hypotheses for how AM fungi clean up their genome is through interactions with the endosymbiotic bacteria that live inside their hyphae, vesicles, and spores (e.g. the rod-shaped, Gram-negative Candidatus Glomeribacter gigasporarum [found in the Gigasporaceae family], and a coccoid Mollicutes-related bacteria that is widely distributed across different lineages of AMF), and through the wide diversity of nuclei that these fungi host. Each glomeromycotan spore may contain an incredible suite of 800–35,000 genetically distinct nuclei, many of which are from other microorganisms, including fungi of other phyla!
Adding to this is the fact that unlike other filamentous fungi, the mycelium of different species in the Glomeromycota can fuse together and exchange their hundreds of nuclei. This interspecies breeding act has been shown to occur between various Glomus species, which can share their mycelial contents, bidirectionally, at a flow rate of two millimeters per second. During this exchange, the DNA of both species may recombine, forming hybrid nuclei with the combined genetic intelligence of the parent nuclei.
Because of these features, and because glomeromycotan fungi are known to dramatically change their morphology (appearance) and habits based on their growing environment, researchers suggest that these fungi defy the Biological Species Concept and should instead be regarded as “form species” or morphospecies. Other mycologists suggest that the Glomeromycota are so fundamentally different from other fungi and other eukaryotes that they should be considered a completely unique branch on the tree of life.
One of the most unusual of all glomeromycotan fungi is Geosiphon pyriforme. This species (the only one in its genus) does not form root associations, but rather obtains its carbon from endosymbiotic cyanobacteria, Nostoc punctiforme, that it hosts inside swollen hyphal tips. Found in the upper layers of wet soils poor in inorganic nutrients, this association has been suggested by some researchers to represent a step in the evolution of plants. Research suggests that its underlying mechanisms of symbiosis may have even led to the development of the AM symbiosis and that precursors to it may be found in Diskagma and Horodyskia fossils from over 2 billion years ago!
Considering all of the traits of the AM symbiosis, its role in supporting plants and building soil health, and thereafter influencing the health of herbivores and their natural enemies, the widespread and indeterminable ecological effects of these fungi cannot be overstated. More so than any other mycorrhizal type, AM may be major determinants of the plant and animal diversity in the habitats that they fill, arguably making them the most ecologically significant of all fungal phyla.