The majority of plant species form mycorrhizal associations. Mycorrhiza means ‘fungus root’ and refers to several specialised associations between fungi and roots (Smith and Read 2008). There are four major types of mycorrhizas: ectomycorrhizas, arbuscular mycorrhizas (also called vesicular arbuscular mycorrhizas), ericoid mycorrhizas and orchid mycorrhizas. These associations are generally beneficial to both the plant and the fungus, with nutrient exchange between the partners. However, under some conditions, at least for arbuscular mycorrhizal, there is no beneficial effect and plant growth can even be reduced.
Orchid mycorrhizal associations are very different from the other three types. The minute orchid seed has no reserves of carbon and is totally dependent on the fungus during the early stages of its growth.
Almost all plant species form one of the four types of mycorrhizal associations. Each plant species usually forms only one type of mycorrhizal association. In the less common situation in which more than one type of mycorrhiza is formed on the same plant, the different mycorrhizas usually occur on different roots or are present at different times during the life cycle of the plant.
One type of mycorrhiza is usually dominant in each ecosystem. For example, plants that form ericoid mycorrhizas often dominate heathland ecosystems. Trees that form ectomycorrhizal associations commonly dominate forests in Europe and North America. Tropical forests may contain more equal proportions of plant species that form arbuscular and ectomycorrhizal associations. The type of mycorrhiza present generally depends on the diversity of plant species that occur there.
The eucalypt trees of Australian forests predominantly form ectomycorrhizal or arbuscular mycorrhizal associations. For example, in a jarrah forest in south-west Australia, seventy two percent of the 93 species of plant studied formed either or both of these two mycorrhizas (Brundrett and Abbott 1991). The 25% found with no mycorrhizal association were mostly members of the family Proteaceae, which does not form mycorrhizas but they can form specialised roots ‘proteoid’ roots which facilitate nutrient uptake.
Most annual agricultural plants form arbuscular mycorrhizas. Ectomycorrhizal associations are less common in disturbed ecosystems and are more frequently observed on perennial plants. Horticultural species form a variety of mycorrhizal associations, depending on whether they are ornamentals (all types of mycorrhizas are represented in this group) or vegetable and orchard plant species (most of these form arbuscular mycorrhizas).
Arbuscular mycorrhizas are the most common type of mycorrhiza and they are formed by a fungal group that occurs in most soils (Smith and Read 2008). The distinctive fungi that form arbuscular mycorrhizas have co-evolved with plants over millions of years (Brundrett 1993). However, worldwide, there are relatively few species of arbuscular mycorrhizal fungi in comparison with other groups of soil organisms. Fewer than 200 species have been described, although many others occur which have not yet been formally named and described. These 200 species all occur within a relatively small number of genera including: Glomus, Acaulospora, Archaeospora, Gigaspora and Scutellospora. The genus of each fungus can be identified from the characteristics of their spores and molecular analysis is now also used to distinguish among species and genera (Rosenhahl 2008).
The most characteristic feature of arbuscular mycorrhizal fungi is the arbuscule. Arbuscules occur within cells of the plant and are key sites for nutrient exchange between the two partners of the association. The distinctive vesicles formed inside roots by some, but not all of these fungi contain high concentrations of lipids and appear to be storage structures.
The roots of most plants are colonised by several species of arbuscular mycorrhizal fungi at the same time. There is little evidence of specificity between particular plants and these fungi, although some plants may be colonised to a greater extent by some of them. The relative abundance of different arbuscular mycorrhizal fungi within roots depends on soil conditions, root development and characteristics of the fungi such as the rapidity of spore germination and growth of hyphae.
Arbuscular mycorrhizal fungi are dependent on the plants they colonise for their survival. The fungi are “biotrophic” which means that they are unable to complete their live cycle without a plant. Because of this unusual characteristic of arbuscular mycorrhizal fungi, it is difficult to grow large quantities of arbuscular mycorrhizal fungi on artificial media in the laboratory without a plant.
When newly formed hyphae of AM fungi intercept a root, the fungus enters with no apparent alteration to the root surface. Species, and even strains, of the same fungus colonise roots to different extents, but generally the more hyphae there are in the soil the greater the extent of mycorrhizal root formed (Wilson 1984).
Arbuscular mycorrhizal fungi can survive for long periods in the soil as spores or as pieces of hyphae, even when the soil is dry or frozen. Most species produce spores that have relatively thick walls that are resistant to desiccation and are not easily eaten by organisms in the soil or colonised by pathogens. They have been shown to contain bacteria that appear to be natural inhabitants. Spores of arbuscular mycorrhizal fungi germinate when soil conditions become suitable, providing they are not in a dormant phase. Pieces of hyphae can survive in dead root pieces or directly in the soil.
An important impact of AM fungi on plants is the alleviation of phosphate deficiency. Arbuscular mycorrhizal fungi form a network of hyphae in soil surrounding roots, and in doing so, effectively extend the root system. This can increase uptake of phosphorus from soil into roots. For example, some plants that are well colonised by arbuscular mycorrhizal fungi can grow just as well with only half the amount of phosphorus available in soil as that required by plants that do not have these fungi within their roots (Robson et al. 1981).
The extent to which a plant benefits from its arbuscular mycorrhizal fungi depends on the availability of nutrients and water. In terms of phosphorus nutrition, only plants growing where there is an inadequate supply of phosphorus will receive any benefit from having arbuscular mycorrhizas (this also requires that water and other nutrients are not limiting to growth). In soils where there is very little available phosphorus or where adequate phosphorus is available, there is generally no direct nutritional benefit of arbuscular mycorrhizas. Plant root architecture also influences the ability of a plant to supply itself with phosphorus, and therefore its dependence on an association with arbuscular mycorrhizal fungi. Plants such as grasses have fibrous root systems and are capable of thoroughly exploring soil for phosphorus. As a result, they do not benefit nutritionally from mycorrhizas to the same extent as a plant such as clover which has a coarser root system.
This effect of arbuscular mycorrhizal fungi on plants through increased phosphorus uptake has usually been studied only for young plants or plants grown in controlled conditions. The contribution of arbuscular mycorrhizal fungi to the growth of older plants, especially those growing in field soils, is not well understood.
Obviously the relationship between the way the symbiosis functions and the nutritional status of the plant is complex and the plant does not always benefit. For example, under some conditions, arbuscular mycorrhizal fungi reduce plant growth, possibly because they take a large amount of carbon from the plant. Alternatively, Scutellospora calospora can increase plant growth and phosphate uptake into plants when the level of phosphorus in soil is extremely deficient. But, it can also decrease plant growth when the quantity of phosphorus in the soil is almost sufficient for the plant to reach its maximum potential growth (Thomson et al. 1986). At higher levels of available soil phosphorus, the fungus appears to remove excessive carbon from the plant to an extent that is detrimental to the growth of the plant.
The abundance of arbuscular mycorrhizal fungi within plant roots changes the supply of phosphorus. Very low levels of phosphorus can be insufficient for the growth of the plant as well as the fungus, keeping fungal numbers low. As more phosphorus becomes available, both the plant and the fungus increase in growth. There can be an increase in the length of root colonised by arbuscular mycorrhizal fungi and a corresponding decrease in the proportion of the root colonised. This occurs if the fungus does not grow fast enough to keep up with the growth of the roots. In soil where phosphorus is present at an adequate level for maximum plant growth, the quantity of arbuscular mycorrhizal fungi in roots decreases substantially. This may either be due to a detrimental effect of excessive amounts of phosphorus on the fungi in the soil or to inadequate carbon supply in the roots for fungal growth.
Clearly, it is not always practical to classify a fungus as being either effective or ineffective at enhancing plant growth. The effectiveness of fungi can be altered by changing the amount of fungus in the soil, by changing the amount of phosphorus in the soil or by altering soil conditions that affect the growth of the fungus. In addition, strains of the same fungus may respond differently, so the diversity of fungi present is also significant.
Phosphorus is not the only nutrient taken up by the hyphae of arbuscular mycorrhizal fungi. For example, the supply of Cu (copper) and Zn (zinc) to some plants is improved in the presence of arbuscular mycorrhizal fungi (Timmer and Leyden 1980). However, arbuscular mycorrhizal fungi do not increase the supply of nitrogen to plants. The reason that AM fungi enhance the uptake of some nutrients and not others is related to the way that nutrients interact with soil particles. Nutrients (such as nitrate) that move with water towards plant roots in most soils are not likely to become more available to a plant if it has arbuscular mycorrhizas. In contrast, P, Cu and Zn become adsorbed to soil particles and diffuse through a soil rather than move with water towards roots. Roots need to explore the soil to intercept these nutrients that move slowly by diffusion. By acting as an extension of the root system, the hyphal network of arbuscular mycorrhizal fungi increases the likelihood that roots have access to nutrients that diffuse slowly in soil.
Even if no nutrient benefit is gained from the presence of arbuscular mycorrhizal fungi, there can be a benefit to the physical state of soil if hyphae help to stabilise soil aggregates. Hyphae of arbuscular mycorrhizal fungi may also protect roots from disease.
There is some evidence that arbuscular mycorrhizal fungi assist plants in water uptake, especially under dry conditions. Demonstration and interpretation of such benefits is confounded because the fungi also take up phosphorus. Enhanced growth may be due to increased phosphorus uptake as well as to water uptake if the soil is phosphate deficient. Therefore, increased water uptake may be an additional benefit in some circumstances, but the effects related to water and phosphorus are difficult to separate.
Within soil, arbuscular mycorrhizal fungi form extensive networks of hyphae that connect the roots of many plant species into an integrated system. This provides a pathway for nutrient exchange between different plant species. The extent to which this occurs, and its importance for plant growth needs further investigation. One particularly interesting area is the role of these networks in aiding seedling growth. Seedlings emerging from a soil containing a network of arbuscular mycorrhizal hyphae may gain access to nutrients from existing plants and grow better than might be expected if they are able to connect into this network. In addition, arbuscular mycorrhizal fungi may increase the chance of survival of seedlings in ecosystems where plants compete for nutrients and light. This is especially important for slower growing plants. Therefore, successful establishment of arbuscular mycorrhizas may help maintain or increase plant species diversity in a natural ecosystem.
Ectomycorrhizal fungi are the dominant mycorrhiza in many natural ecosystems, even though they form associations with a smaller number of plant species than do AM fungi. Plants that form ectomycorrhizas include well-known trees and many smaller perennial plants (Smith and Read 2008).
The main features of an ectomycorrhizal association are the hyphal mantle on the root surface, the Hartig net formed between the cells of the root closest to the root surface and the extension of hyphae into the soil. The hyphae of ectomycorrhizal fungi do not enter root cells in the same way as AM fungi. Rather, the Hartig net is formed when the ectomycorrhizal fungi enter roots between epidermal cells and spread out to form a network of hyphae through the root. Ectomycorrhizal fungi are usually clearly visible on the surface of roots. They promote root branching and restrict root extension which results in a great diversity in architecture of ectomycorrhizas. Roots become covered with hyphae to varying degrees.
Ectomycorrhizas are formed by many different species of fungi, in contrast to the relatively small number of species that form arbuscular mycorrhizas. Most belong to families of the basidiomycetes and a number to families of the ascomycetes. Some are clearly visible in forests and other reasonably undisturbed ecosystems because they produce mushrooms and similar fungal spore-containing structures above the soil surface. Others form their reproductive structures below the soil surface. Small mammals dig up and eat these structures. Truffles are a well-known example of fungus-produced underground fruiting structures.
Some ectomycorrhizal fungi form associations with many different plant species (Horton and Bruns 2001), while others form associations with fewer plants. For example, most species of Amanita have an intermediate or broad host range, whereas most of species of Suillus have a narrow host range (Molina et al. 1992). In contrast, 25% of species of Russula have a narrow host range and 30% have a broad host range.
Compared to AM fungi, many species of ectomycorrhizal fungi can grow in artificial, laboratory media, making them easier to study, although they often grow very slowly. Others are either difficult to grow or have not yet been grown at all under laboratory conditions.
It is not easy to define a simple life cycle for ectomycorrhizal fungi because many genera of fungi are involved. Ectomycorrhizal fungi are commonly associated with perennial host plants that are relatively long-lived. Therefore, ectomycorrhizal fungi within the roots of living plants have the potential to survive for long periods.
Ecological successions of ectomycorrhizal fungi occur on the same root systems leading to a gradual change in dominance of fungi (Mason et al. 1984). Some plants form more than one type of ectomycorrhizal association, either on different roots of the same plant or at different times. In this study, fruiting structures of the fungus Laccaria sp. generally occurred further from the tree base than those of Lactarius. However, the presence of these structures is not a direct measure of the extent of mycorrhizal fungus present in soil or in roots. Recent molecular studies have highlighted the lack of a quantitative relationship between fungi in roots and the number of fruiting structures formed above the ground.
New roots usually become colonised by the hyphae of ectomycorrhizal fungi attached to existing mycorrhizal roots on the same or on a nearby plant. The spores that are formed by these fungi do not appear to be very important for initiation of new mycorrhizas.
Various degrees of specificity exist between ectomycorrhizal fungi and host plants. A process of molecular recognition takes place prior to colonisation of the root by the hyphae. Colonisation of the root by the fungus proceeds only if the fungus and root are compatible. Recognition of compatibility between a root and a fungus involves molecular signalling using genetic information in both the fungus and plant.
It is more difficult to estimate the contribution of ectomycorrhizal fungi to plant growth than for AM fungi, except at early stages in plant development (Onguene and Kuyper 2002). Studies on seedlings clearly illustrate the contribution of ectomycorrhizal fungi in the early stages of tree development, but extrapolation of these benefits to older trees is not reliable.
Ectomycorrhizal associations can improve the phosphate status of plants in soils that are phosphate deficient. Under some circumstances, ectomycorrhizal fungi make nitrogen more available to plants and increase plant resistance to drought and disease. These benefits can lead to a more robust plant that has a greater chance of survival.
There is substantial evidence for benefits of ectomycorrhizal fungi in nitrogen nutrition of plants where nitrogen is deficient. Some ectomycorrhizal fungi can use simple or more complex forms of organic nitrogen (Turnbull et al. 1995). For example, all three fungi in this study were effective at using glutamine as a nitrogen source, but none could use histidine, which is a very complex form of nitrogen. In contrast, Elaphomyces was able to use nitrogen from arginine, but the other two fungi were not. These differences are likely to be important in soils with low levels of inorganic nitrogen and high levels of organic matter. The nitrogen that is taken up by the ectomycorrhizal fungi is passed onto their plant hosts, improving what would otherwise be relatively poor growing conditions for the plant.
Ectomycorrhizal fungi also appear to directly help plants avoid disease and survive periods of drought. Where the hyphal mantle covers the root, it provides protection from pathogenic fungi, which can not penetrate the hyphal layer. In addition to this, due to the presence of the ectomycorrhizal fungi changes occur in root physiology that minimises the susceptibility of the root to infection by pathogenic fungi or bacteria. The hyphal networks around mycorrhizal roots enables water to be taken up from parts of the soil that the roots cannot reach. Protection from both disease and drought are contributions that ectomycorrhizal fungi may make to various degrees at different stages in the growth cycle of the host plant. The contributions depend on the type of fungus and the soil conditions.
Ericoid mycorrhizas are the specialised mycorrhizal associations formed with members of the plant families Ericaceae (Smith and Read 2008). These mycorrhizas have a different morphology from the mycorrhizas already mentioned and play an important role for their host plants (Perotto et al. 2002). Ericoid mycorrhizal fungi colonise the individual cells of very fine hair-like roots directly from the soil, forming coils of hyphae within the root cells. The hyphal connections to the soil coalesce around the roots as a fine network. The hair roots colonised by ericoid mycorrhizal fungi are short lived. Therefore, ericoid fungi need to continuously re-establish the mycorrhizal associations as the roots grow.
There appears to be a high degree of specificity between the fungi that form ericoid mycorrhizas and their host plants. Details of the nature of the recognition process between the fungus and plant are well understood.
Some ericoid mycorrhizal fungi grow in pure culture, and analysis of these cultures shows that ericoid fungi are very different from each other (Hutton et al. 1994). This was demonstrated by comparing the electrophoretic pattern of enzymes that decompose pectin after they were separated in a gel. The migration of enzymes in the gel indicated differences in the molecular weight of pectic enzymes from some fungi. This is indicative of differences in genetic characteristics among the fungi.
There is evidence that ericoid mycorrhizal fungi have certain characteristics similar to wood degrading fungi that may allow them to degrade complex components of organic matter in the soil. In comparison to a selection of ectomycorrhizal fungi, two ericoid mycorrhizal fungi had greater potential to degrade lignin and soluble phenolic molecules (Bending and Read 1997). This conclusion was based on the response of the fungi in four biochemical tests that measured characteristics of fungi important in degradation of lignin and other complex plant molecules.
Ericoid plants occur in nutrient poor soils and the mycorrhizal associations that they form are likely to be important in providing them with nutrients from the organic matter that would otherwise remain unavailable to the plant. In particular, nitrogen appears to be released from organic matter by the activity of ericoid mycorrhizal fungi. There is also a possibility that organic phosphorus is mineralised from organic matter by these fungi.
Although ericoid mycorrhizal fungi have characteristics that are very different from those of both AM and ectomycorrhizal fungi, all three types of mycorrhizas coexist in many natural ecosystems. This illustrates how plant-microbial associations respond to the nutrient resources in a soil.
The morphology and physiology of orchid mycorrhizas are very different from those of the other three types of mycorrhizas described above (Smith and Read 2008). Orchid seeds are highly dependent on fungi. During the early stages of seedling growth, the fungi supply carbon to the growing orchid seedling. This is the reverse of what occurs in other mycorrhizas (Rasmussen 2002). Some orchid mycorrhizal fungi have been isolated and grown in culture for many years and many belong to the genus Rhizoctonia or to related genera.
• Mycorrhizal fungi are present in all soils, and their abundance depends on the type of plant present. The major types of mycorrhizas are: arbuscular mycorrhizas, ectomycorrhizas, ericoid mycorrhizas and orchid mycorrhizas.
• Mycorrhizas contribute to nutrient uptake by plants. Hyphae associated with arbuscular, ecto- and ericoid mycorrhizas help the plant to explore the soil for nutrients.
• Roots are usually colonised by more than one species of AM fungus that differ in their ability to help in nutrient uptake.
• One root of an ectomycorrhizal plant is usually colonised by only one species of fungus at anytime.
• The fungi that form arbuscular, ecto- and ericoid mycorrhizas contain their carbon and energy supply from the host plant.
• Ectomycorrhizal fungi are a much more diverse and host-specific group than AM fungi.
• Ericoid mycorrhizal fungi are important in nitrogen nutrition of ericaceous plants.
• Orchid mycorrhizal fungi form a type of association with their host plant that is very different from all other types of mycorrhizal associations. Orchid mycorrhizal fungi are essential for the early stages of growth of the plant when the plant is totally dependent on the fungus for carbon.