12.5 Competence and regional patterning
Some of the processes involved in development of fruit bodies and other multicellular structures by fungal mycelia have been mentioned in earlier Chapters. Production of a multicellular structure is an aspect of mycelial differentiation and the mycelium must have access to the necessary resources. The formal description is that the mycelium must be competent to undertake production of a multicellular structure.
In practical terms this essentially means that the exploratory mycelium has found and captured sufficient of its substratum to have internalised, in the form of accumulated nutritional stores, adequate supplies for all the synthetic processes involved in further development and morphogenesis. The essential point is that nutrients are no longer outside the hyphal system and potentially available, but they are inside the hyphal system and immediately available. This change in balance results in shifts in some of the regulatory circuits that then lead to cell and tissue differentiation.
In Chapter 9 we mentioned differentiation of mycelium in response to environmental and other influences (CLICK HERE to view); and Fig. 16 in Chapter 9 showed a flow chart summarising the processes involved in development of fruit bodies and other multicellular structures in fungi (CLICK HERE to download a PDF version of this chart). The first two paragraphs emphasised physiological aspects, but this flow chart reminds us that there is also a genetic component to competence. Vegetative compatibility systems can make a contribution to mycelial interaction (CLICK HERE to view), but it is usually governed by the mating type factors (CLICK HERE to view) and results in formation of a sexually compatible mycelium. However, in the higher fungi, even a haploid mycelium can have a number of alternative developmental pathways open to it: continuation of hyphal growth, production of asexual spores, and/or formation of asexual multihyphal structures (stromata, sclerotia, etc), whilst a compatible mating permits progress into the sexual cycle and opens up the additional pathways associated with that (Moore, 1998a). Choice between these is often a matter of the impact of sometimes very localised environmental conditions on a mycelium which has become competent to embark on any of several developmental pathways.
As is indicated in this flow chart, the onset of multicellular development is usually signalled by some sort of disturbance that causes a check or restraint to normal (exploratory, invasive) vegetative growth. This restraint might be imposed by a nutritional crisis: perhaps the substrate becomes exhausted of nutrients (of many or even only one or two crucial ones; the preferred carbon source and the preferred nitrogen source, for example). Now, this doesn’t mean that the mycelium is starving, because the mycelium has absorbed and stored many nutrients, but it does mean that the balance of nutrient supply is changed and this will result in a change of regulatory pattern within the hyphae.
Other major signals that have been the subject of numerous laboratory experiments are temperature shocks, light exposure, edge encounters and physical injury, all of which can also be related to natural events in the normal habitat. Many of the Basidiomycota require a drop in temperature to fruit, which may reflect their adaptation to seasonal temperature fluctuations. Response to illumination patterns may reflect response to day light or day length, or even a growth habit in which the mycelium grows through a dark substratum (like a litter layer, pile of plant debris or herbivore dung, etc) to eventually emerge at a light-exposed surface. In the laboratory ‘edge encounter’ usually means that the mycelium has reached the edge of the Petri dish, but in nature it may equate to encountering rocks in the soil or growth through a piece of timber reaching the surface. Physical injury in the wild may be inflicted by adverse weather conditions or disturbance by animals, and may act by resulting in exposure of previously-protected mycelium to any of the other environmental fluctuations (that is, a burrowing animal, say, may separate a mycelium from its food base, or leave it exposed to light or temperature stresses).
Fruit bodies do not arise from single cells, although this was believed to be the case for many years. Rather, initiation of multicellular structures like fruit bodies and sclerotia involves aggregation of cells from different sources as a result of hyphal congregation that is the direct result of the most fundamental change in hyphal growth pattern: namely that in vegetative mycelia hyphae show negative autotropism (hyphal tips grow away from each other) whereas to form a condensed multicellular tissue component hyphal tips must show positive autotropism and grow towards each other (Matthews & Niederpruem, 1972; Waters, Moore & Butler, 1975; Van der Valk & Marchant, 1978).
Unlike animal embryos, fungal multicellular structures evidently do not normally consist of a population of cells which are the progeny of a single progenitor, but are assembled from contributions made by a number of co-operating hyphal systems. Indeed, in a few cases fruit body chimeras have been observed (the word ‘chimera’ comes from the name of a Greek mythological monster, which was made of the parts of several animals; it now means ‘composed of genetically distinct cells’). Kemp (1977) described how fruit bodies of ‘Coprinus’ formed on horse dung collected in the field but incubated in the laboratory could consist of two species (then identified as Coprinus miser and C. pellucidus but now named Parasola misera and Coprinellus pellucidus). The two have distinctively different basidiospore morphologies and the hymenium comprised a mixed population of basidia bearing the two different sorts of spores, so the chimera extended throughout the fruit body.
Generally speaking, the most highly differentiated cells occur on the outside of the tissue blocks that make up fungal multicellular structures (Williams et al., 1985). Thus, major morphogenetic events in fungi, like those in animals and plants, are associated with tissue surfaces and their ‘epidermal’ layers of cells that separate adjacent tissues. As the adult tissues are demarcated in even the earliest fruit body initials (as shown in Fig. 1), fungi are like animals and plants in having a basic ‘body plan’ which is established very early in development. The pattern of tissue distribution that makes up the ‘body plan’ is established sequentially by the processes of regional specification, cell differentiation, and cell co-ordination. It is likely that all of these processes are orchestrated by morphogens and/or growth factors; there is some indirect indication of this, although there is no direct evidence for the existence of morphogens in the differentiating fruit body primordium similar to the growth hormones and growth factors that are so important in animal and plant development. The very young hyphal tufts or initials of vegetative or fruit body structures are simply composed of a mass of tissue which is made up of apparently loosely-interwoven hyphae. Very soon, however, tissue layers involved in rapid cell formation (that is, organised rapid branch formation) become recognisable, which demarcate the major tissue layers of the adult organ. To create such histologically distinct regions (recognisable as the future tissues of the adult organ) some organisation is being imposed on the initially homogeneous interwoven hyphae.
Updated December 17, 2016