Plants do not grow alone. From the moment roots develop in soil, they are penetrated
and colonized extensively by filamentous fungi in "fungus-root" associations
called mycorrhizae. These associations are "mutualistic" in that both
host and fungus obtain benefit. The plant receives inorganic nutrients and water
from fungal hyphae foraging far beyond the root zone. The fungus, in turn, obtains
a steady supply of carbon and energy directly from the plant with a minimum
of competition from other soil microbes. The origin of mycorrhizae at least
400 million years ago indicates they are critical to growth and reproduction
of both plant and fungus. As a result of coevolution, mycorrhizae are found
in most habitats worldwide and in approximately 95% of all plant species. Their
universality is one reason below-ground microbial activity is being reevaluated
from the perspective of a "mycorrhizosphere", which includes not only
the root zone but a larger soil volume containing an integrative network of
fungal hyphae, spores and fruiting bodies (Fig. 1).
Seven types of mycorrhizae are known to occur in nature, all of which fit within two broad categories (see figure):
Some fungi combine properties of each category. In "ectoendomycorrhizae", the fungal symbionts form an ectomycorrhizal mantle but hyphae in roots resemble endomycorrhizae by entering cortical cells. "Arbuscular" endomycorrhizae are the most prevalent globally in over 30,000 plant species, but fungal species currently number only 152 in one order Glomales of the phylum Zygomycota. Vegetative structural characters of fungi in roots define two broad groups: those forming finely branched arbuscules and lipid-rich intercellular "vesicles" (see figure) and those with coarser arbuscules and clusters of fragile cells called "auxiliary cells" outside roots. Species are defined by mode of spore formation and differences of microscopic structural characters inside broken spores (see figure). The simplicity of these characters is thought to be the cause of low number of species relative to the high diversity of habitats they coinhabit with plants. Ectomycorrhizae also are widespread, but the range of hosts is limited to gymnosperms and some woody angiosperms. The fungi are much more taxonomically diverse, encompassing over 4,000 species spanning two phyla, Basidiomycota and Ascomycota. Species are classified mainly by structure and organization of fruiting bodies with diverse morphologies such as various mushrooms and puffballs. When sporulation is absent, some species now can be identified by characteristics of the mantle covering roots, such as color and branching patterns of component hyphae.
Less is known about other endomycorrhizal symbioses because they have narrow host ranges and are not as well studied. "Ericoid mycorrhizae" are formed by Ascomycete fungi that associate only the roots of plants in Ericales. Hyphal coils penetrate in cortical cells that emerge and are arranged loosely on root surfaces. "Orchidaceous mycorrhizae", as the name implies, are restricted to orchids (Orchidaceae). The fungal symbionts are mostly Basidiomycetes that otherwise are pathogens, such as root and wood decay fungi. They establish hyphal coils in cells that degenerate and release nutrients during seed germination and early seedling development.
"Arbuscular" fungi have a wide host range, but plants in some families (e.g. Cruciferae, Cyperaceae, and Polygonaceae) do not form mycorrhizae. They appear to have evolved away from the symbiosis, along the way altering their genotypes to actively produce defense reactions against fungal colonization. Chemically-induced mycorrhiza-resistant (myc-) mutants of peas have been obtained to determine defense mechanisms. Myc- plants release phenolic substances, callose, and pathogenesis-related proteins at the onset of fungal penetration into root cells, leading to suppression of colonization. Myc+ plants lack such reactions, indicating that compatibility between host and fungus results from a suppression of genetic defense mechanisms. Myc- plants also do not nodulate (nod-), which suggests the presence of common plant "symbiosis" genes.
Similar mutants have not been obtained in ectomycorrhizal associations, but greater specificity between some fungi and their hosts provides model systems to determine the molecular basis for incompatable reactions. Nonhosts produce defense reactions similar to those observed by myc- legume mutants. However, hosts also produce some enzymes (chitinases, peroxidases) that may inhibit intracellular fungal colonization. Root cells normally undergo marked changes in shape and cell wall structure during mycorrhizal development, indicating strong host involvement. Host-encoded tubulin proteins increase with onset of mycorrhiza formation, and they now are considered important determinants in host-fungus compatability.
The localized sites of nutrient exchange is intracellular in endomycorrhizal associations. The most intensive activity occurs along a narrow interface zone between specialized fungal structures (arbuscules, hyphal coils) and the host cell plasma membrane. An arbuscule (or hyphal coil of Ericaeous and Orchidaceous fungi) develops after an intercellular hypha penetrates a root cell wall, wherepon it then is enveloped by the cell's invaginating plasma membrane. Ultrastructural studies indicate an electron-dense material is sandwiched between host and fungal boundaries, so there is no direct contact. Active bidirectional flow of carbon and inorganic ions in this zone occurs via an H+-ATPase pump. The major nutrient exchanged, phosphorus, is released by the fungus in large amounts, and efficiency of the transfer to host appears to be governed by arbuscule longevity, area of the interface, number of ion channels, and activity of transmembrane carriers. Complex interactions of source-sink relationships between shoots and roots also regulate amount of mycorrhizal development. For example, increases in root soluble carbohydrates tend to increase mycorrhizal colonization. Slight growth suppressions may occur from carbon drain by the mycorrhizal fungus under conditions of high soil nutrients, but they usually disappear as soil nutrients levels decline and dependency on the symbiosis increases.
In ectomycorrhizal associations, host and fungal cell walls are in direct contact with each other. The fungal symbiont enzymatically induces cleavage of the middle lamella between root cells, followed by fusion of host and fungal cell walls into a common interfacial matrix. Elevated ATPase activity in fungal and host plasma membranes have been interpreted as indicators of bidirectional nutrient exchange. Role of external hyphae. Arbuscular fungi produce a diverse range of external hyphae with different functions: (a) "runner" hyphae along roots establish new sites of colonization to coincide with new root growth, (b) "fertile" hyphae in soil for production of spores individually, in aggregates, or in sporocarps, and (c) "absorptive" hyphae beyond the root zone for uptake of nutrients and as a pipeline for translocation of nutrients back to host roots. External hyphae alter soil structure by increasing particle aggregation (important in sand dunes and disturbed soils) and by stimulating or inhibiting growth of other soil microbes. Ericoid endomycorrhizae in acidic heath soils produce external hyphae with a more active function: enzymatic release of nitrogen from predominant organic compounds that otherwise is unavailable to roots.
External hyphae of ectomycorrhizal fungi on tree species also excrete proteinases and phosphatases to break down organic matter and increase mineralization (and nutrient availability) of litter on the forest floor. Rhizomorphs greatly enhance the foraging potential of a fungus in organic matter and soil. Some fungi produce large mats of hyphae in litter to accelerate this process and also provide unique habitats for other soil microbes.
The capacity of plant communities to support a diverse fungal community is regulated partly by genetics and physiology of the host plant and aggressiveness of each fungal symbiont. Fungal colonization often is reduced under conditions of high soil nutrients (especially phosphorus) or foliar stresses on photosynthesis such as low light conditions. Some plant groups, such as alder and poplars, are able to support either arbuscular or ectomycorrhizal associations, depending on environmental conditions and the kinds of fungal inoculum present. Arbuscular fungi have low host specificity, so as many as 8-10 species can coexist in the same plant root system. Species diversity seems to be similar in a wide range of habitats, from arid to mesic conditions. Higher degrees of host specificity regulate fungal species composition in ectomycorrhizal, ericoid, and orchidaceous associations.
Heterogeneous plant communities consist of plants with varying levels of dependency on the mycorrhizal association, which in turn impact on plant succession and other dynamic processes. Plants may be obligately dependent (association required in all environments), facultatively dependent (associations required under some conditions such as low soil), or independent (associations not required). Some groups, such as ferns, range from total dependence (e.g. Psilotopsida) to independence (e.g. aquatic Azollaceae) from mycorrhizae. Orchids rely completely on their fungal endophytes for seedling germination and establishment. In arid habitats, glacial moraines, and lava flows, early successional plants generally are mycorrhiza-independent and fungal communities are slow to develop. With the influx of mycorrhizal fungi, dependent hosts become more prevalent. In some tropical communities, plant diversity appears to increase when they are mycorrhizal.
Recent evidence indicates mycorrhizal fungi promote inter-plant communication, even among unrelated plants. Hyphal linkages have been found between roots of legumes and grasses by arbuscular fungi. "Monotropoid" mycorrhizae consist of hyphal linkages by ectomycorrhizal fungi between achlorophyllous parasitic plants and their tree hosts for nutrient exchange and other processes. The mycorrhizosphere includes many other organisms impacting on mycorrhizal processes or vice versa. "Helper" bacteria appear to selectively promote establishment and development of some ectomycorrhizal associations. Symbiotic nitrogen-fixation by bacteria in legumes is strongly dependent on arbuscular mycorrhizae to meet a high demand for soil phosphorus. Soil pathogens may be inhibited or stimulated with changes in mycorrhizal root exudates, barriers created by ectomycorrhizal mantles, and many other processes.
Many efforts have been made over the past 15 years to tap the benefits of mycorrhizae for agricultural and horticultural purposes. Test results have not been consistently positive because of complications by many variables in fluctuating field situations. Success with inoculation of introduced organisms appears to be greatest in disturbed or polluted soils and in locations where the proper fungi for a given type of host association are absent.
Production of mass inoculum varies with mycorrhizal type because methods for culturing the fungal symbionts differ greatly. For example, arbuscular fungi must associate with living roots to grow and reproduce. Batch cultures are produced by growing whole plants in soil mixes, a soilless growth media such as sand, or in closed chambers where roots are bathed in a nutrient mist. Ericaceous or orchidaceous endomycorrhizal fungi can be cultured on synthetic media, but batch cultures are uneconomical because growth is too slow. Most ectomycorrhizal fungi also can be cultured rapidly on synthetic media in large. Commercial inoculum generally consists of fungal material grown or mixed with sterile vermiculite, expanded clay, or other inert and light-weight carriers.
In natural ecosystems, introduced fungi do not appear to offer much superior advantage to native species. Research has focused on developing strategies to optimize the ability of native fungi to colonize hosts in their natural habitat or to minimize loss of these fungi with disturbance. Practical efforts have been limited thus far to agroecosystems. As one example, highly dependent crop hosts are selected over mycorrhizal independent hosts in crop rotations or in multiple cropping systems. Research evidence suggests that traditional methods of breeding and producing crop plants in soils with high nutrients may select against the most efficient fungal communities or even against the mycorrhizal association, but preventive strategies have yet to be implemented.
In summary, mycorrhizal interactions between plants, fungi, and the environment are complex, interdependent, and often inseparable. Although much has yet to be learned about the dynamics of each association, it is clear that mycorrrhizae are an essential below-ground component in establishment and sustainability of plant communities as the earth's geography and climate undergoes continual flux and change.