Mutualisms involving higher plants and fungi

A wide variety of symbiotic associations are formed between higher plants and fungi. A very remarkable group of Ascomycete fungi, the Clavicipitaceae, grow in the tissues of many species of grass and a few species of sedge. The family includes species that are easily recognized as parasites (e.g. Claviceps, the ergot fungus, and Epichloe, the choke disease of grasses), others that are clearly mutu-alistic, and a large number where the costs and benefits are uncertain. The fungal mycelia characteristically grow as sparsely branched filaments running through intercellular spaces along the axis of leaves and stems, but they are not found in roots. Many of the symbiotic fungi produce powerful toxic alkaloids that another mutualism extending beyond two species

Figure 13.14 Coral acclimation and recovery in coral bleaching. (a) Algal density in western (light bars) and eastern (dark bars) cores of the coral Goniastrea aspera before and after exposure to elevated (34°C) and ambient (27°C) temperatures for 68 h. Mean values are shown; error bars show 1 SD (n = 5). (After Brown et al., 2000.) (b) Symbiont communities in another coral, Montastraea annularis, collected in January 1995 off the coast of Panama. Each symbol represents a sample that contained the algal taxa Symbiodinium A, B or C, or mixtures of taxa summarized according to the code shown below. Columns in the data represent individual coral colonies (depth increases from left to right) and rows represent locations of higher (rows 1 and 2) and lower (rows 3 and 4) irradiance, as defined in the diagram to the left. (After Rowan et al., 1997.) (c) Corresponding symbiont communities from close to the bleaching region of Symbiodinium C before (January 1995) and during (October 1995) an episode of coral bleaching. Densities of A (gray), B (white) and C (orange) before and during bleaching (left and right bars of each pair, respectively) in samples reported in B + C communities (3-10), A + C communities (3-7) and an ABC community. (After Rowan et al., 1997.)

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Figure 13.14 Coral acclimation and recovery in coral bleaching. (a) Algal density in western (light bars) and eastern (dark bars) cores of the coral Goniastrea aspera before and after exposure to elevated (34°C) and ambient (27°C) temperatures for 68 h. Mean values are shown; error bars show 1 SD (n = 5). (After Brown et al., 2000.) (b) Symbiont communities in another coral, Montastraea annularis, collected in January 1995 off the coast of Panama. Each symbol represents a sample that contained the algal taxa Symbiodinium A, B or C, or mixtures of taxa summarized according to the code shown below. Columns in the data represent individual coral colonies (depth increases from left to right) and rows represent locations of higher (rows 1 and 2) and lower (rows 3 and 4) irradiance, as defined in the diagram to the left. (After Rowan et al., 1997.) (c) Corresponding symbiont communities from close to the bleaching region of Symbiodinium C before (January 1995) and during (October 1995) an episode of coral bleaching. Densities of A (gray), B (white) and C (orange) before and during bleaching (left and right bars of each pair, respectively) in samples reported in B + C communities (3-10), A + C communities (3-7) and an ABC community. (After Rowan et al., 1997.)

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confer some protection from grazing animals (the evidence is reviewed in Clay, 1990) and, perhaps even more important, deter seed predators (Knoch et al., 1993).

A quite different mutualism of fungi with higher plants occurs in roots. Most higher plants do not have roots, they have mycorrhizas - intimate mutualisms between fungi and root tissue. Plants of only a few families like the Cruciferae are the exception. Broadly, the fungal networks in mycorrhizas capture nutrients from the soil, which they transport to the plants in exchange for carbon. Many plant species can live without their mycorrhizal fungi in soils where neither nutrients nor water are ever limiting, but in the harsh world of natural plant communities, the symbioses, if not strictly obligate, are none the less 'ecologically obligate'. That is, they are necessary if the individuals are to survive in nature (Buscot et al., 2000). The fossil record suggests that the earliest land plants, too, were heavily infected. These species lacked root hairs, even roots in some cases, and the early colonization of the land may have depended on the presence of the fungi to make the necessary intimate contact between plants and substrates.

Generally, three major types of mycorrhiza are recognized. Arbuscular mycorrhizas are found in up to two-thirds of all plant species, including most nonwoody species and tropical trees. Ectomycorrhizal fungi form symbioses with many trees and shrubs, dominating boreal and temperate forests and also some tropical rainforests. Finally, ericoid mycorrhizas are found in the dominant species of heathlands including the northern hemisphere heaths and heathers (Ericaceae) and the Australian heaths (Epacridaceae).

not roots but mycorrhizas

13.8.1 Ectomycorrhizas

An estimated 5000-6000 species of Basidiomycete and Ascomycete fungi form ectomycorrhizas (ECMs) on the roots of trees (Buscot et al., 2000). Infected roots are usually concentrated in the litter layer of the soil. Fungi form a sheath or mantle of varying thickness around the roots. From there, hyphae radiate into the litter layer, extracting nutrients and water and also producing large fruiting bodies that release enormous numbers of wind-borne spores. The fungal mycelium also extends inwards from the sheath, penetrating between the cells of the root cortex to give intimate cell-to-cell contact with the host and establishing an interface with a large surface area for the exchange of photo-assimilates, soil water and nutrients between the host plant and its fungal partner. The fungus usually induces morphogenetic changes in the host roots, which cease to grow apically and remain stubby (Figure 13.15). Host roots that penetrate into the deeper, less organically rich layers of the soil continue to elongate.

The ECM fungi (see Buscot et al., 2000 for a review) are effective in extracting the sparse and patchy supplies of phosphorus and especially nitrogen from the forest litter layer, and their high species diversity presumably reflects a corresponding diversity of niches in this environment (though this diversity of niches is very far from having been demonstrated). Carbon flows from the plant to the fungus, very largely in the form of the simple hexose sugars: glucose and fructose. Fungal consumption of these may represent up to 30% of the plants' net rate of photosynthate production. The plants, though, are often nitrogen-limited, since in the forest litter there are low rates of nitrogen mineralization (conversion from organic to inorganic forms), and inorganic

Figure 13.15 Mycorrhiza of pine (Pinus sylvestris). The swollen, much branched structure is the modified rootlet enveloped in a thick sheath of fungal tissue. (Courtesy of J. Whiting; photograph by S. Barber.)

nitrogen is itself mostly available as ammonia. It is therefore crucial for forest trees that ECM fungi can access organic nitrogen directly through enzymic degradation, utilize ammonium as a preferred source of inorganic nitrogen, and circumvent ammonium depletion zones through extensive hyphal growth. None the less, the idea that this relationship between the fungi and their host plants is mutually exploitative rather than 'cosy' is emphasized by its responsiveness to changing circumstances. ECM growth is directly related to the rate of flow of hexose sugars from the plant. But when the direct availability of nitrate to the plants is high, either naturally or through artificial supplementation, plant metabolism is directed away from hexose production (and export) and towards amino acid synthesis. As a result the ECM degrades; the plants seem to support just as much ECM as they appear to need.

13.8.2 Arbuscular mycorrhizas

Arbuscular mycorrhizas (AMs) do not form a sheath but penetrate within the roots of the host, though they do not alter the host's root morphology. Roots become infected from mycelium present in the soil or from germ tubes that develop from asexual spores, which are very large and produced in small numbers - a striking contrast with the ECM fungi. Initially, the fungus grows between host cells but then enters them and forms a finely branched intracellular 'arbuscule'. The fungi responsible comprise a distinct phylum, the Glomeromycota (Schüfiler et al., 2001). Although originally divided into only about 150 species, suggesting a lack of host specificity (since there are vastly more species of hosts), modern genetic methods have uncovered a far greater diversity among the AM fungi, and there is increasing evidence of niche differentiation amongst them. For instance, when 89 root samples were taken from three grass species that co-occurred in the same plots in a field experiment, and their AM fungi were characterized using such a method - terminal restriction fragment length polymorphism - there was clear separation amongst the AM strains found on the different hosts (Figure 13.16).

There has been a tendency to a range of benefits? emphasize facilitation of the uptake of phosphorus as the main benefit to plants from AM symbioses (phosphorus is a highly immobile element in the soil, which is therefore frequently limiting to plant growth), but the truth appears to be more complex than this. Benefits have been demonstrated, too, in nitrogen uptake, pathogen and herbivore protection, and resistance to toxic metals (Newsham et al., 1995). Certainly, there are cases where the inflow of phosphorus is strongly related to the degree of colonization of roots by AM fungi. This has been shown for the bluebell, Hyacinthoides non-scripta, as colonization progresses during its phase of subterranean growth from August to February through to its above-ground photosynthetic phase thereafter (Figure 13.17a). Indeed, bluebells cultured without AM fungi are unable to take up phosphorus through their poorly branched system of roots (Merryweather & Fitter, 1995).

On the other hand, a factorial set of experiments examined the growth of the annual grass Vulpia ciliata ssp. ambigua at sites

Figure 13.16 The similarity among 89 arbuscular mycorrhiza (AM) fungal communities taken from the roots of three coexisting grass species, Agrostis capillaris, Poa pratensis and Festuca rubra, assessed by terminal restriction fragment length polymorphism. Each terminal on the 'tree' is a different sample, with the grass species from which it originated shown. More similar samples are closer together on the tree. The similarity within, and the differentiation between, the AM fungal communities associated with different hosts are plainly apparent. (After Vandenkoornhuyse et al., 2003.)

Figure 13.16 The similarity among 89 arbuscular mycorrhiza (AM) fungal communities taken from the roots of three coexisting grass species, Agrostis capillaris, Poa pratensis and Festuca rubra, assessed by terminal restriction fragment length polymorphism. Each terminal on the 'tree' is a different sample, with the grass species from which it originated shown. More similar samples are closer together on the tree. The similarity within, and the differentiation between, the AM fungal communities associated with different hosts are plainly apparent. (After Vandenkoornhuyse et al., 2003.)

Figure 13.17 (a) Curves fitted to rates of phosphorus inflow (-----, left axis) and root colonization by arbuscular mycorrhiza (AM) fungi

(-, right axis) in the bluebell, Hyacinthoides non-scripta, over a single growing season. (After Merryweather & Fitter, 1995; Newsham et al., 1995.) (b) The effects of a factorial combination of Fusarium oxysporum (Fus) and an AM fungus, Glomus sp. (Glm), on the growth (root length) of Vulpia plants. Values are means of 16 replicates per treatment; bars show standard errors; the asterisk signifies a significant difference at P < 0.05 in a Fisher's pairwise comparison. (After Newsham et al., 1994, 1995.)

Figure 13.17 (a) Curves fitted to rates of phosphorus inflow (-----, left axis) and root colonization by arbuscular mycorrhiza (AM) fungi

(-, right axis) in the bluebell, Hyacinthoides non-scripta, over a single growing season. (After Merryweather & Fitter, 1995; Newsham et al., 1995.) (b) The effects of a factorial combination of Fusarium oxysporum (Fus) and an AM fungus, Glomus sp. (Glm), on the growth (root length) of Vulpia plants. Values are means of 16 replicates per treatment; bars show standard errors; the asterisk signifies a significant difference at P < 0.05 in a Fisher's pairwise comparison. (After Newsham et al., 1994, 1995.)

in eastern England where there were large differences in the intensity of natural mycorrhizal infection (West et al., 1993). In one treatment phosphate was applied, and in another the fungicide benomyl was used to control the fungal infection. Fecundity of the grass was scarcely affected by any of the treatments. An explanation was provided by a further set of experiments (Figure 13.17b) in which seedlings of Vulpia were grown with an AM fungus (Glomus sp.), with the pathogenic fungus Fusarium oxys-porum, with both, and with neither. Growth was not enhanced by Glomus alone, but growth was harmed by Fusarium in the absence of Glomus. When both were present, growth returned to normal levels. Clearly, the mycorrhiza did not benefit the phosphorus-economy of the Vulpia, but it did protect it from the harmful effects of the pathogen. (In the previous experiment, benomyl presumably had no effect on performance because it controlled both mycorrhizal and pathogenic fungi.)

The key difference appears to be that Vulpia, unlike the bluebell, has a highly branched system of roots, and Newsham et al. (1995) go so far as to propose a continuum of AM function in relation to root architecture, with Vulpia and Hyacinthoides sitting towards the two extremes. Plants with finely branched roots have little need for supplementary phosphorus capture, but development of that same root architecture provides multiple points of entry for plant pathogens. In such cases AM symbioses are therefore likely to have evolved with an emphasis on plant protection. By contrast, root systems with few lateral and actively growing meristems are relatively invulnerable to pathogen attack, but these root systems are poor foragers for phosphorus. Here, AM symbioses are likely to have evolved with an emphasis on phosphorus capture. Of course, even this more sophisticated view of AM function is unlikely to be the whole story: other aspects of AM ecology, such as protection from herbivores and toxic metals, may well vary in ways unrelated to root architecture.

13.8.3 Ericoid mycorrhizas

Heathlands exist in environments characterized by soils with low levels of available plant nutrients, often as a result of regular fires in which, for example, up to 80% of the nitrogen that has accumulated between fires may be lost. It is unsurprising, therefore, that heathlands are dominated by many plants that have evolved an association with ericoid mycorrhizal fungi (Read, 1996). This enables them to facilitate the extraction of nitrogen and phosphorus from the superficial layers of detrital material generated by the plants. Indeed, the conservation of natural heathlands is threatened by nitrogen supplementation and fire control, which allow colonization and domination by grasses that would otherwise be unable to exist in these impoverished environments.

The ericoid mycorrhizal root itself is anatomically simple compared to other mycorrhizas, characterized by a reduction of its vascular and cortical tissues, by the absence of root hairs, and by the presence of swollen epidermal cells occupied by mycorrhizal fungi. As a result, the individual roots are delicate structures, often referred to as 'hair-roots'; collectively the hair-roots form a dense fibrous root system, the bulk of which is concentrated towards the surface of the soil profile (Pate, 1994). The fungi are effective, unlike the plants alone, in absorbing nitrate, ammonium and phosphate ions that have been mobilized by other decomposers in the soil (see Chapter 11), but crucially they are also 'saprotrophic'. They are therefore able to compete directly with the other decomposers in liberating nitrogen and phosphorus from the organic residues in which most of these elements are locked up in heathland ecosystems (Read, 1996). A mutualism can thus be seen, again, to be woven into a larger web of interactions: the symbiont enhances its contribution to the host by making a preemptive competitive strike for scarce inorganic resources, and its own competitive ability is presumably enhanced in turn by the physiological support provided by its host.

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