The association between fungus and plant delivers nutrients to the host plant via: (a) mobilisation and absorption by fungal mycelia in the soil; (b) translocation to the fungus–root interface within the root and (c) transfer across the fungus–root interface into the cytoplasm of root cells. As shown in Figure 4.31, both roots and mycorrhizas can absorb nutrients such as phosphorus from the soil, so plants with highly branched fine roots and long root hairs are less likely to benefit substantially from mycorrhizal associations.
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Figure 4.31 Diagrammatic summary showing the impact of roots hairs or arbuscular mycorrhizal fungal hyphae on phosphorus uptake from the soil. Compare the upper and lower pairs of drawings to see how soil hyphae increase the size of phosphorus depletion zones in soil much more if plants lack highly branched roots with long root hairs. (Based on Brundrett et al. 1996)
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Figure 4.32 Root hairs of an Australian sundew (Drosera erythrorhiza), a carnivorous plant with nonmycorrhizal roots that have extremely long root hairs (1 mm) in relation to the diameter of the root. (Photograph courtesy M. Brundrett)
(a) Nutrient uptake from the soil by the fungi
In addition to hyphae in direct contact with the root surface, all mycorrhizal fungi produce soil hyphae (extramatrical mycelium) which extend into the surrounding soil. Both arbuscular mycorrhizal and ectomycorrhizal fungi can produce copious soil hyphae, that extends well beyond the nutrient depletion zone for immobile nutrients around individual roots and display a complex architecture that renders them an efficient nutrient-collecting and transport network (Figure 4.33). The soil hyphae of many ectomycorrhizal fungi form hyphal aggregations, known as mycelial strands and rhizomorphs, that play a major role in transport of inorganic nutrients or photoassimilates.
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Figure 4.33 Abundant mycelium (M) of Scleroderma forms a sheath (S) around roots of an eucalypt and explores surrounding soil (E). These ectomycorrhizas benefit the host through enhanced nutrient uptake (especially phosphorus) from surrounding soil. (Photograph courtesy I. Tommerup)
Extramatrical mycelium is also primarily responsible for spread of the association to new roots and translocation of energy from the plants for fungal reproduction. Fungi forming mycorrhizal associations can also spread by germination of wind or animal dispersed spores and, in some cases, from old root pieces.
In arbuscular mycorrhizas, fine highly branched soil hyphae (diameter 1–5 µm) provide surface area for nutrient absorption, while larger diameter hyphae (up to 10 µm) form a transport network in the soil for moving solutes from bulk soil to the root (Figure 4.34). Absorption of phosphate by the fungus is maximised by the action of a high-affinity transporter which is expressed only in the soil hyphae of arbuscular mycorrhizal fungi during symbiosis with the plant. The fungi take up inorganic phosphate and quickly convert it to polyphosphate, a macromolecule where the charge of the phosphate ions is balanced by cations including those of potassium and magnesium. Polyphosphate allows phosphorus to be transported to the plant without affecting hyphal osmotic balance. For instance, within the root, concentrations of phosphorus in hyphae may be up to 350 mM, but plant cell vacuoles generally have < 10 mM. Once the polyphosphate reaches an arbuscule in the plant root it is converted back to phosphate and released into the peri-arbuscular space where it is absorbed by the host plant. Active transporters in the host cell plasma membrane maintain a concentration gradient across the plant-fungus interface.
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Figure 4.34 Soil hyphae of an arbuscular mycorrhizal fungus growing through the surrounding rhizosphere soil and forming spores. Such hyphae ramify through the soil and likely influence soil chemistry and microbial functioning. Root stained with Chlorazol black E. (Photograph courtesy M. Brundrett)
Many experiments have demonstrated a relationship between arbuscular mycorrhizal infection and improved plant phosphorus status, particularly under glasshouse and laboratory conditions (Figure 4.35). Arbuscular mycorrhizal fungi do not appear to have access to sources of soil phosphorus that are otherwise unavailable to nonmycorrhizal roots. Thus, increased plant absorption in the presence of arbuscular mycorrhizal fungi of phosphorus, nitrogen and other macronutrients such as calcium and sulphur, and micronutrients including zinc and copper, seems to primarily reflect the increased absorptive surface of the soil hyphae. However, soil hyphae also provide a conduit for rapid transport of carbon from plants into soil and there is evidence that hyphal exudation may promote breakdown of organic nutrient sources by other microorganisms (see below). Note that the effects of individual species or strains of fungi on plant nutrition will vary, in part due to different morphology of soil hyphae. Under some circumstances, the presence of arbuscular mycorrhizal fungi may decrease plant growth especially in heavily fertilised crop plants.
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Figure 4.35 The typical growth response for an Australian Cassia species to inoculation with arbuscular mycorrhizal fungi. The greater shoot dry weight of the inoculated plants is due to the fungi enhancing plant uptake of phosphorus. There is no benefit for the plant from the fungi at the lowest level of phosphorus as the fungi are also likely limited by phosphorus, but benefit is substantial at low-intermediate phosphorus levels. (Based on Brundrett et al. 1996, data courtesy of David Jasper and Karen Clarke)
The soil hyphae of ectomycorrhizal fungi increase the absorptive area of a root system substantially, extending the volume of soil explored by the host plant and consequently the quantity of minerals available. Ectomycorrhizal fungi, however, use additional strategies to enhance nutrient acquisition. Some secrete extracellular proteinases, peptidases, phosphomonoesterases and phosphodiesterases that effectively hydrolyse organic nitrogen and phosphorus sources to liberate some nitrogen and phosphorus compounds which can be absorbed by the fungi. Some ectomycorrhizal fungi produce hydrolytic enzymes within the cellulase, hemicellulase and lignase families that may facilitate hyphal entry to moribund plant material in soil and access to mineral nutrients sequestered therein. In these ways, ectomycorrhizal fungi short-circuit conventional nutrient cycles, releasing nutrients from soil organic matter with little or no involvement of saprotrophic organisms. Ectomycorrhizal fungi also release siderophores capable of complexing iron and oxalate to improve potassium uptake and have also been implicated in promoting weathering of rocks to release mineral nutrients for plants.
(b) Carbon uptake from the plant by the fungi
Arbuscular mycorrhizal fungi depend completely on the host plant for carbon and are unable to grow without being associated with a host plant. This has made the culture of these fungi difficult and proved a significant barrier to development of cheap technologies for inoculation (as might be desirable in land rehabilitation or agriculture) on a large scale. Transfer of carbon from the host to an arbuscular mycorrhizal fungus likely takes place in the arbuscule where the plant releases simple sugars (hexoses) which are absorbed by the fungi. These sugars are rapidly converted into trehalose, glycogen and lipids. The lipids and, to a lesser extent, glycogen are transported to the soil hyphae. Once in the soil hyphae, lipids are progressively broken down into hexoses and trehalose and used to fuel the growth of the fungus. As the lifecycle of the fungus progresses, large amounts of lipid are stored, particularly in vesicles and spores which may be inside or outside of the roots.
In contrast to arbuscular mycorrhizal fungi, ectomycorrhizal fungi can utilise carbon substrates other than those provided by the host plant. It seems that most ectomycorrhizal fungi have some ability to use lignin and cellulose, along with various other substrates including starch, glycogen and sugars such as glucose. Ability to utilise various substrates differs among fungal species. As a result of these abilities, ectomycorrhizal fungi are able to be isolated and grown in culture. For ectomycorrhizal fungi associated with host roots, sucrose is thought to be hydrolysed in root cell walls and glucose to be then absorbed by hyphae from the interface apoplasm.
It has been estimated that 20-50% of plant photosynthate is allocated to mycorrhizal fungi, much of which is allocated to soil hyphae. The soil hyphae of the fungi exude carbon compounds which will influence soil processes including the growth, composition and function of the soil microbial community. Recent research suggests that roots and mycorrhizas may differentially affect soil carbon pools. Thus, overall, the fungi provide a significant pipeline for the movement of carbon from the plant shoot into the soil and may greatly influence soil processes and microbial activity both within and away from the rhizosphere. Indeed, it is now thought that the fungi may significantly influence the global carbon cycle (e.g. their cell walls include some components that are very slow to decompose in soils). In addition, some compounds exuded by the soil hyphae of mycorrhizas, such as glomalin, play an important role in maintenance of soil structure through gluing together soil particles, especially in sandy soils. In addition, colonisation can change the amount and composition of compounds exuded by roots. For instance, the presence of arbuscular mycorrhizal fungi can result in the amount of carboxylates in the rhizosphere being reduced by 50% or more (Figure 4.36). Carboxylates are low molecular weight organic anions which are thought to play a role in release of highly sorbed phosphorus into forms that plant roots or the hyphae of arbuscular mycorrhizal fungi can absorb. Hence, the presence of the fungi enhances the ability of the host to access orthophosphate, but perhaps at the expense of its ability to release phosphorus from sorbed sources.
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Figure 4.36 Amount of carboxylates in the rhizosphere of 12 species of Kennedia grown with and without mycorrhizal fungi. (Adapted from Ryan et al. 2012)