16.4.1  Symbiotic associations

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Plants in nature always grow amidst soil microorganisms, and some become intimately associated with plants to form mutualistic symbioses. Examples of such symbiotic micro-organisms include mycorrhizal fungi of various types and N2-fixing prokaryotes, especially rhizobia. Looser symbiotic associations involve bacteria and soil microfauna within the rhizosphere. Their metabolic activities increase nutrient availability (Sections 3.4, 3.5).

All of these symbioses may affect rates of growth and eventually reproduction of plants compared with growth in the absence of such associations. A symbiotic association is therefore a potential selection pressure that can influence the evolutionary success of vascular plants and hence the com-position of plant communities.

(a)  Diversity and ecology of mycorrhizal plants

Mycorrhizas (sometimes called mycorrhizae or mycorrhizal associations) are by far the most common mutualistic symbioses involving vascular plants, and about 90% of higher plant families (both gymnosperms and angiosperms) contain species that can form mycorrhizal associations. Roots of most ferns also form mycorrhizas and similar structures occur in the absorbing organs of many bryophytes (Harley and Smith 1983; Smith and Read 1997). Fossil mycorrhizas occur in rocks formed in the Devonian era, about 400 million years ago, and present-day mycorrhizas are the result of a very long period of worldwide co-evolution between plants and soil fungi.

Mycorrhizas fall into distinct classes, depending on the types of fungi and plant, and on the anatomy of the mycorrhizas themselves (Section 3.4). Each main class shows wide specificity where a given species of mycorrhizal fungus can colonise different host species and one plant species can be colonised by different fungal species. This situation contrasts sharply with the extremely narrow specificity of N2-fixing symbioses (Section 3.5).

There are broad differences between the dominant classes of mycorrhizas that are found in different ecosystems, depending on vegetation type, soil characteristics and growth-limiting nutrients. A walk up a mountain can pass through different mycorrhizal ‘zones’ (Figure 16.11). Ectomycorrhizas (with their distinct external fungal sheath and with fungi penetrating intercellular spaces of the root cortex) occur on forest trees including eucalypts, beech (Fagus and Nothofagus), birch, oak and most conifers such as pine and spruce. Ericoid mycorrhizas (where fungi penetrate root cells) occur in plants of heathlands. They are also common in plants growing on peaty soils (those containing large quantities of organic matter) as on the Siberian tundra.

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Figure 16.11 Representative vertical distribution of mycorrhizal classes on a mountain, showing major types of vegetation and important growth-limiting nutrients. (Based on Read 1984)

Overall, the most common mycorrhizal associations are vesicular-arbuscular (VA) mycorrhizas, where fungi again penetrate root cells and form finely branched arbuscules within those cells. Fungal storage bodies (vesicles) can form as either intercellular or intracellular structures. VA mycorrhizas predominate in understorey plants of woods and forests of all types, in temperate and tropical grasslands, in plants of scrub and desert and in many tropical forests.

Some classes of mycorrhizal fungi can grow in soil in the absence of a host plant and in pure culture, but VA mycorrhizal fungi cannot. A vast but unsuccessful research effort has gone into attempts to culture these fungi. Instant fame will be accorded whoever discovers the right medium!

The broad ecological zonations for different classes of mycorrhizas should not be overemphasised because the different classes can often be found very close together. For example, many trees of tropical rainforests form VA mycorrhizas but there are exceptions. Dipterocarps, which dominate many tropical rainforests, form ectomycorrhizas, while the other plants in the same forest will nearly all have VA mycorrhizas. Mediterranean-type vegetation — which is quite common worldwide — contains very mixed mycorrhizal associations, including ericoid, ecto- and VA mycorrhizas. Only in very inhospitable soils (e.g. saline, anaerobic and highly disturbed soils and those in very cold environments) are plants mostly non-mycorrhizal.

Since mycorrhizal symbioses are so common, research into the growth and nutrition of plants in the field should always take into account their probable occurrence as a
factor that can influence plant growth and competition, especially in soils where levels of essential inorganic nutrients are low. For example, research done in Western Australia has shown that disturbance of soils during surface mining can reduce the levels of mycorrhizal fungi, but survival in stored topsoil is still sufficient to help re-establish native vegetation when the topsoil is replaced after mining operations cease (Jasper 1994).

Mycorrhizas can also improve productivity in cultivated plants even when levels of applied fertilisers are high. An important example in parts of Australia is the ‘long fallow disorder’ that reduces the growth of a wide range of crops when soils are left fallow for long periods (Table 16.6). This effect with sorghum and sunflower grown in Queensland (Thompson 1987) is due to a massive decline in populations of VA mycorrhizal fungi. Better growth of both plants on soils left fallow for shorter periods was associated with greater colonisation of roots by VA mycorrhizal fungi. There were higher levels of P per plant grown after short fallow and in sunflower P was higher even when expressed on the basis of % of dry weight; these effects reflected uptake of soil P via mycorrhizal fungi.

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Table 16.6

Improved growth of forest trees after inoculation with specific ectomycorrhizal fungi has been demonstrated in a wide range of sites, including eucalyptus forests in Australia and elsewhere (Grove and Malajczuk 1994). These examples confirm an extensive interest in establishing and managing populations of mycorrhizal fungi in soils to increase plant productivity in agricultural and forest ecosystems (Robson et al. 1994).

(b)  Benefits and costs of symbioses

Physiological benefits to a mycorrhizal plant include improved absorption of nutrients such as P and Zn via external fungal hyphae. Plant–water relations might also be improved, which would be important in arid conditions, but this is still a controversial area of research (Smith and Read 1997). Mycorrhizal fungi do not fix atmospheric N2 but can facilitate uptake of both inorganic and organic N and can broaden the range of sources of soil N that are available to plants (Case study 16.3). As shown in Queensland, mycorrhizal seedlings of Eucalyptus species can utilise sources of organic N that cannot be assimilated by non-mycorrhizal seedlings (Turnbull et al. 1995). In addition, external hyphae of mycorrhizal fungi can link plants of the same or (within limits) different species and can allow transfer of inorganic and organic compounds between plants.

The idea that mycorrhizal plants can form linked and mutually beneficial communities is an attractive one but it is not yet established if the amounts of solutes transferred from donor to recipient plants are always physiologically important. Transfer of organic C between linked plants is greatest when the recipient is shaded so that its photosynthesis is reduced. Accordingly, transfer of carbohydrate from parent plants might well assist seedlings to grow in deep shade as on a forest floor before they become exposed to bright sunlight (Smith and Read 1997; Smith and Smith 1996).

Mycorrhizas in heterotrophic angiosperms such as some orchids lacking chlorophyll are physiologically distinctive. Even when mature, the plant drains the fungus of organic C derived from other sources (such as soil or donor plants that are autotrophic). This type of mycorrhizal fungus can also supply inorganic nutrients to the plant, but whether the fungi gain any nutritional benefit remains to be established, so that such symbioses may not be truly mutualistic.

Where mycorrhizal fungi colonise autotrophic (photosynthetic) plants the fungus derives its organic C from the plant (Figure 3.17). This is a physiological cost to the plant but one which is usually not excessive, since mycorrhizal plants often grow faster than non-mycorrhizal plants of the same species under the same conditions. These positive growth effects are largest in shoots. Mycorrhizal plants sometimes grow root systems no larger or even smaller than those in non-mycorrhizal plants, diverting organic C to the fungus. However, there are some physiological conditions in which total growth of mycorrhizal plants is the same as or even slower than that of non-mycorrhizal plants of the same type. One of these conditions is low light intensity and here the cause of the effect is obvious: low light means that photoassimilate may be in short supply and the drain to the fungus may be deleterious to the plant.

The second condition resulting in slower growth of mycorrhizal plants is where levels of available soil P are high. The simplest explanation here is that the supply of soil P is adequate even for non-mycorrhizal plants and the C drain to the fungus (where present) then becomes a limitation on plant growth. Under these last conditions some plants reduce or prevent formation of mycorrhizas in a way that is analogous to the absence of N2 fixation where legumes grow in soils high in nitrate or ammonium.

Finally, some mycorrhizal fungi even ‘cheat’ their hosts by obtaining organic C without supplying P or other inorganic nutrients to their host. Why a plant tolerates being cheated in this way is not known (Smith and Smith 1996). Lack of positive growth responses to colonisation is also sometimes found under a variety of field conditions which are less easy to explain and are the subject of much research.

‘Mycorrhizal responsiveness’ (Table 16.7) summarises the most important factors which influence the extent to which a plant benefits from the symbiosis by improved nutrition and growth. These factors include developmental and anatomical properties of the fungi, including their growth rates in soil, their ability to colonise plants and subsequent growth within roots, and their efficiency in absorbing nutrients from soil and transferring them to the plant. Plants such as some cereals which have long, highly branched roots with long root hairs often show small mycorrhizal responses because the roots themselves are well structured for exploring large volumes of soil. Here, mycorrhizal hyphae confer relatively little extra advantage.

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Table 16.7

The interface between fungus and plant is obviously crucial in determining mycorrhizal responsiveness, a principle that applies equally to both intercellular and intracellular inter-faces. If there is a sufficiently large area of contact between the symbionts, as in a VA mycorrhiza with many arbuscules, then there is the capacity for operation of a large number of transport proteins that catalyse selective transfer of nutrients. However, the rates of transfer are subject to regulation that can determine the relative amounts of C transferred to the fungus per amounts of P (or other essential nutrients) transferred to the plant and hence the nutritional costs and benefits to the partners.

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Figure 16.12 Effects of plant density on growth of mycorrhizal and non-mycorrhizal Trifolium subterraneum. Plants were grown for eight weeks under controlled conditions in pots containing 0.5 kg of soil. The upper diagram (a) shows that growth stimulation of individual plants by VA mycorrhizas is greatest at low plant density. The lower diagram (b) shows that as the density of plants increases, total biomass per pot becomes more similar in mycorrhizal and non-mycorrhizal treatments due to limitations imposed by soil nutrient supply. (Based on unpublished data; E. Facelli, Department of Soil Science, University of Adelaide)

Table 16.7 also shows effects within plant communities that influence mycorrhizal responsiveness. Positive mycorrhizal growth responses decrease as the density of plants increases and competition for soil nutrients intensifies (Sanders et al. 1995). Put another way, where large numbers of roots and mycorrhizal fungal hyphae are close together, mycorrhizal roots appear to compete with each other and with any non-mycorrhizal roots, so that growth of all the individual plants is reduced compared to growth of plants spaced well apart. This effect is shown in Figure 16.12 and may be one reason why intensive mycorrhizal colonisation fails to benefit field growth.

Hyphal links between plants of the same or different species complicates the issue of competition enormously. If nutrients or organic C are transferred via the hyphae between plants growing under similar conditions, what determines whether a plant is a donor or recipient of resources? This important issue awaits resolution.

Finally, mycorrhizal fungi can suppress infection by some pathogenic organisms — an obvious extra benefit of a symbiotic association. Not surprisingly, responses of field plants are more complicated and difficult to understand than in experiments with potted plants under controlled conditions!

(c)  Selection pressures resulting from mycorrhizal symbioses

A successful mycorrhizal symbiosis can act as a selection pressure. Such symbioses can affect growth and reproduction compared to non-mycorrhizal plants under equivalent conditions. This selection pressure can act within a population of a single plant species if the mycorrhizal fungus is present irregularly in the soil. Consider, for example, the potentially faster growth of an individual plant that becomes mycorrhizal compared to one that cannot or can do so only more slowly. The selection pressure can also act within a community of mixed species. Compare here the potentially faster growth of individuals of a species that forms mycorrhizas compared to individuals of a species that cannot. The subtle and complex nature of the selection pressures arises from the various features that can determine mycorrhizal responsiveness (Table 16.7), which is why ‘potentially’ was emphasised. Nutritional benefits in VA mycorrhizal plants can extend from increased vegetative growth to reproductive effects including earlier flower production, increased production of flower buds and increased seed production. In addition to improving plant fecundity, formation of mycorrhizas can improve the quality of plant offspring, for example their weight and nutrient content, and even the nutrient content of their seeds. These
persistent effects are good evidence that formation of mycorrhizas can bring about strong effects on plant populations and on the structure of plant communities (Sanders et al. 1995).

(d)  ‘Non-mycorrhizal’ species

Some terrestrial plants never form mycorrhizas even under growth conditions where colonisation would be expected. These plants belong to diverse families that are not closely related but include many chenopods and most brassicas (unfortunately including Arabidopsis). There are also individual ‘non-mycorrhizal’ genera within families that otherwise form mycorrhizas. One good example is the legume Lupinus (lupin). In such cases, an absence of these symbioses cannot be construed as disadvantage in evolutionary terms, so that mycorrhizal associations are not necessarily a universal advantage to terrestrial plants. A different range of adaptive features allows these plants to grow and reproduce successfully in the absence of mycorrhizas. These include excretion of organic acids that aid solubilisation of P and production of long, relatively fine roots with long root hairs, which exploit soil P and other immobile nutrients in much the same way as do the external hyphae of mycorrhizal fungi, where present. (Such root properties often reduce mycorrhizal responsiveness as mentioned above.)

Notwithstanding alternative adaptations, an important question remains. What prevents colonisation by mycorrhizal fungi in non-mycorrhizal species? The answer is probably not the same for the different families and is still not known for many plants. In some cases, including brassicas, there is production of chemical defences against colonisation by mycorrhizal fungi. This response has similarities to chemical defence reactions in plant roots against pathogenic organisms (Smith and Read 1997).

(e)  Concluding remarks

When considering effects of mycorrhizas on plant growth and the selective advantages of those associations, all levels of organisation from molecular to ecological are relevant.

A molecular aspect as yet unknown is how plants distinguish between a mycorrhizal fungus that is usually beneficial and a fungus which is harmful (pathogenic). Pathogenic organisms can elicit expression of chemical defences by resistant plants, but what exactly is the sequence of recognition signals for a symbiotic association that results in such chemical defence reactions being turned off? Research into this aspect of mycorrhizal associations lags behind work on N2-fixing symbioses.

At an ecological level, mycorrhizal fungi also have beneficial effects on important soil properties — they improve soil structure by binding together soil particles to form water-stable aggregates, and in so doing contribute further to the sustainability of managed ecosystems in agriculture, forestry and horticulture.

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