Nutrient Capture

Hyphae absorb sufficient nutrients to support their active vegetative growth and to allow accumulation of reserve materials, which may subsequently be translocated to sites of need, including developing fruit bodies. Fruit body primordia may be fairly uniformly dispersed, but locations of enlarging and maturing fruit bodies may be much less evenly spread. For example, in Coprinus lagopus, certain favourably placed young fruit bodies may initiate a flow of nutrients in their direction, others that are deprived then fail to mature (Madelin, 1956a, 1956b, 1960). When C. lagopus colonies were physically divided in half early in growth, the two halves yielded similar fruit body biomass, whereas the two sides of an intact colony could differ by as much as 10:1, implying that in the latter case the 'minority' half is exporting its nutrients to the 'majority' half (Madelin, 1956b).

Mycelia must have access to sufficient substrates before fruiting is possible. Buller (1931, p. 165) discussed the requirement for a minimum amount of mycelium to support a minimum fruit body in Coprinus sterquilinus, arguing that one of the functions of hyphal fusions between (clonal) germlings is to ensure the rapid formation of that minimal size mycelium encompassing a corresponding minimum quantity of substrate. Obviously, the minimum quantity of substrate required varies between species depending on size of the fruit bodies produced. Fungi producing small fruit bodies are able to do so with only a small amount of resource, e.g. minute Marasmius and Mycena species restricted to leaf petioles, small portions of leaf lamina, beech cupules, etc. (Figure 2). A very large mycelial domain is required to produce the large, perennial brackets of heart-rot fungi (Rayner and Boddy, 1988). It was estimated that all of the nitrogen in 13.6 g of wood would be required to supply 1 g of Ganoderma applanatum basidiome, and

36.1 g wood to supply 1 g of spores, based on mean nitrogen content of fruit bodies (1.13%), spores (3.05%) and Betula sapwood (0.83%; Merrill and Cowling, 1966). Since fruit bodies are commonly 1 kg or more, and several grams of spores are produced each year (Fomes fomentarius produced 1.115 g spores in 20 days (Meyer, 1936)), a mycelium would need to draw upon the entire nitrogen content of more than 14 kg wood.

Culture studies indicate that once the minimum substrate size is reached fruit body distribution is governed by a flow of nutrients towards particular developing fruit bodies, rather than localised nutrient depletion or inhibition of development. The generality of this interpretation is based on two consistent observations. First, that many fruit body primordia are generally formed, but only a comparatively small number of them develop into mature fruit bodies; but if fruit body size is related to local nutrient supply, one would expect that all of the primordia on a colony would develop into mature but small fruit bodies, each using those quantities of materials which are available locally and adjusting its size accordingly. Second, a crop consisting of several fruit bodies will often develop as a group, so that any general inhibitory action is unlikely. The concept that nutrients flow towards a favoured centre would permit several neighbouring primordia to mature in a clump, while still withholding nutrients from unfavourably situated primordia. Clearly, different species emphasise different aspects of this physiology in their fruiting behaviour and some are characteristically solitary, e.g. Phallus impudicus, while others are caespitose, e.g. Hypholoma fasciculare and Psathyrella multipedata (Figure 2). Some Basidiomycota, notably Corticiaceae, form fruit bodies over the entire resource surface that they have access to, e.g. Vuilleminia comedens on branches in the canopy. Large, skin-like fruit bodies of some Corticiaceae may form at individual sites, subsequently coalescing on contact. Detail is, however, lacking as much less research has been done on these species than on Agarics.

In vitro experiments consistently indicate a general correlation between nutrient exhaustion of the medium and the onset of multicellular morphogenesis; however, reproduction is not an alternative to vegetative hyphal growth but an aspect of the differentiation of vegetative hyphae. Continued growth of the vegetative mycelium is necessary to provide sustenance to its developing fruit bodies. Correlation of fruiting with nutrient exhaustion of the medium does not mean that development is prompted by a mycelium that is starving, because the mycelium has accumulated nutrient reserves. Further, the timing of fruiting and the amount of biomass that a fungus commits to fruiting varies with life history

Figure 2 Some fruit bodies of saprotrophic basidiomycota, illustrating a range of sizes and resources: (a) the solitary Macrolepiota rhacodes with a coin size marker (20 mm diameter); (b) a fruit body of Marasmius setosus with the same coin size marker; (c) even smaller Marasmius specimen on the petiole of a beech cupule; (d) Collybia peronata on a pine cone; (e) the decidedly caespitose Psathyrella multipedata; (f) Terence Ingold posing with Fomes fomentarius on a beech tree in Knole Park, Sevenoaks, Kent, 1969 (see Ingold, 2002). Photographs (a)-(e) by David Moore of specimens collected by members of the mid-yorkshire fungus group at Harlow Carr Gardens. (See Colour Section)

strategy (Cooke and Rayner, 1984; Rayner and Boddy, 1988; Chapter 11). Rapid and extensive commitment of mycelial biomass is an R-selected (ruderal) characteristic, typical of fungi that rapidly dominate following disturbance. Such fungi are usually not combative and are often rapidly replaced by later arriving, more combative species. They, therefore, must commit to reproduction before they are killed and replaced. By contrast, slower and intermittent commitment to reproduction is characteristic of fungi in stressful environments and/or that are combative, dominating middle stages of community development. Laboratory studies have largely employed species, e.g. Coprinopsis spp., Pleurotus spp. and Schizophyllum commune, that fruit readily in culture, which is a ruderal characteristic; thus, we must be cautious in extrapolating to fungi with other life history strategies.

As we have discussed above, only preconditioned mycelium is capable of undergoing morphogenesis. The preconditioned mycelium must be beyond a particular minimum size, perhaps be of a particular minimum age, and the underlying nature of both these preconditions is that the mycelium has been able to accumulate sufficient supplies of reserve materials to support development of the minimum reproductive structure. For some fungi, exhaustion of a particular metabolite from the medium or substrate may be a signal that prompts morphogenesis in a mycelium that is not starving, but is healthy and well provisioned. Exhaustion of one or more constituents of the medium changes the balance of nutrient flow. If the medium is no longer fully supportive, the requirements of active hyphal growth can no longer be met by import from outside the hyphae and the balance must shift from 'reserve material accumulation' to 'reserve material mobilisation'. That change from balanced growth to growth under limitation in external nutrient supply is what signals the onset of morphogenesis. Cellular differentiation leading to fruit body morphogenesis is an expression of unbalanced growth which is precipitated by one or more changes in the balance of metabolism, and itself causes further cycles in which cellular components are re-allocated. Even though nutritional dependence on the external substrate may still be demonstrated, the emphasis shifts towards intramycelial regulation.

While this metabolic change is proceeding there is a change in the behaviour of hyphal branches. For some branches, negative autotropism becomes positive autotropism, so that neighbouring hyphae, often those of the surface or more aerial parts of the mycelium, can interact. They form centres of rapid but self-restricting growth and branching which become the hyphal aggregates or mycelial tufts, perhaps 100-200 p.m in diameter, that are the 'initials' of the reproductive structure the organism can produce. Frequently, and especially in culture, these aggregates are formed in great number over the whole surface of the colony. As supplies of nutrients in the medium approach exhaustion repression of the morphogenesis of these hyphal aggregates is lifted and they proceed to develop further. As mentioned above, only a small number of the first-formed hyphal aggregates usually undergo further development and these become the focus for translocation of nutrients, mobilised from the stores in other parts of the colony and transported through the hyphal network to the developing reproductive structures.

Illumination may be required, either to promote further morphogenesis or to direct development into one of a small number of morphogenetic pathways (see below). Particular temperatures may also be required for particular pathways of development. Development usually proceeds in a series of steps that may be coordinated by environmental cues (illumination, temperature, atmosphere) and often involve sweeping re-allocation of cellular components. Within the young fruit body, therefore, new accumulations of 'stored' nutrients arise, and there may be a number of these accumulation-mobilisation-translocation-accumulation cycles during the development of the reproductive structure.

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