Fungal Morphogenesis

Within the developing tissues of a fruit body, cells embark on a particular course of differentiation in response to the interaction of their intrinsic genetic programme with external physical signals (light, temperature, gravity, humidity), and/or chemical signals from other regions of the developing structure. These chemicals may be termed organisers, inducers or morphogens, and may inhibit or stimulate entry to particular states of determination. Chemical signals may contribute to a morphogenetic field around a structure (cell or organ), which permits continued development of that structure but inhibits formation of another structure of the same type within the field. All of these phenomena contribute to the pattern formation that characterises the 'body plan' created by the particular distribution of differentiated tissues in the multicellular structure. Pattern formation depends on positional information, which prompts or allows the cell to differentiate in a way appropriate to its position in the structure and may be conveyed by concentration gradients of one or more morphogens emitted from one or more spatially distinct organisers. Pattern formation thus involves an instructive process, which provides positional information, and a second interpretive process, in which the receiving cell or tissue responds.

Fungi are 'modular organisms' in which growth is repetitive, and a single individual mycelium will have localised regions at very different stages of development (Andrews, 1995). Consideration of developmental regulatory systems is relevant to the current discussion because any effect of the external environment on fruit body development must operate through an influence on the control systems that determine the distribution and growth patterns of the multicellular structure.

The constituent cells of a fungal fruit body are generally considered to be totipotent (able to follow any pathway of differentiation), because a mycelial culture can be produced in vitro from a fragment of a mature, fully differentiated structure, e.g. a fruit body stem. This feature results in a morphogenetic plasticity which surpasses that of other organisms and provides an intellectual challenge in terms of developmental biology, taxonomy and genetics (Watling and Moore, 1994). The only exceptions to totipotency are the meiocytes (the cells within which meiosis occurs), which are committed to sporulation once they have progressed through meiotic prophase (Chiu and Moore, 1988a, 1988b, 1990, 1993; Chiu, 1996). On the other hand, even meiocytes can be 'used' for non-sporulation functions: the hymenium of Agaricus bisporus is packed with basidia held in an arrested meiosis and serving a purely structural function (Allen et al., 1992).

Differentiated fungal cells require reinforcement of their differentiation 'instructions'. This reinforcement is part of the context within which they normally develop, but when removed from their normal environment most differentiated hyphae revert to vegetative hyphae. Hyphal differentiation is consequently an unbalanced process in comparison with vegetative hyphal growth. In most hyphal differentiation pathways the balance must be tipped in the direction of 'differentiation' by the local microenvironment, which is, presumably, mainly defined by the local population of hyphae.

Another common feature is that morphogenesis is compartmentalised into a collection of distinct developmental processes (called 'subroutines'; Figure 1; Moore, 1998a). These separate (or parallel) subroutines can be recognised at the levels of organs (e.g. cap, stem, veil), tissues (e.g. hymenophore, context, pileipellis), cells (e.g. basidium, paraphysis, cystidium) and cellular components (e.g. uniform wall growth, growth in girth, growth in length, growth in wall thickness). They are distinct genetically and physiologically and may run in parallel or in sequence. When they are played out in their correct arrangement the morphology that is normal to the organism results. If some of the subroutines are disabled (genetically or through physiological stress), the rest may still proceed. This partial execution of developmental subroutines produces an abnormal morphology. The main principles that govern fungal development as deduced from observation, experiment and computer modelling are summarised in Table 1 (from Moore, 2005).

Fungal morphogenesis must be totally different from animals, because fungal cells have walls, and from plants (whose cells also have walls) because hyphae grow only at their tips and hyphal cross-walls form only at right angles to the

Figure 1 Flowchart showing a simplified view of the processes involved in development of fruit bodies and other multicellular structures in fungi (from Moore, 1998a).

Table 1 The eleven principles that govern fungal development

Principle 1 The fundamental cell biology of fungi on which development depends is that hyphae extend only at their apex, and cross-walls form only at right angles to the long axis of the hypha Principle 2 Fungal morphogenesis depends on the placement of hyphal branches

Principle 3 The molecular biology of the management of cell-to-cell interactions in fungi is completely different from that found in animals and plants Principle 4 Fungal morphogenetic programmes are organised into developmental subroutines, which are integrated collections of genetic information that contribute to individual isolated features of the whole programme. Execution of all the developmental subroutines at the right time and in the right place results in a normal structure Principle 5 Because hyphae grow only at their apex, global change to tropic reactions of all the hyphal tips in a structure is sufficient to generate basic fruit body shapes Principle 6 Over localised spatial scales coordination is achieved by an inducer hypha regulating the behaviour of a surrounding knot of hyphae and/or branches (these are called Reijnders' hyphal knots)

Principle 7 The response of tissues to tropic signals and the response of

Reijnders' hyphal knots to their inducer hyphae, coupled with the absence of lateral contacts between fungal hyphae analogous to the plasmodesmata, gap junctions and cell processes that interconnect neighbouring cells in plant and animal tissues suggest that development in fungi is regulated by morphogens communicated mainly through the extracellular environment Principle 8 Fungi can show extremes of cell differentiation in adjacent hyphal compartments even when pores in the cross-wall appear to be open (as judged by transmission electron microscopy)

Principle 9 Meiocytes appear to be the only hyphal cells that become committed to their developmental fate. Other highly differentiated cells retain totipotency — the ability to generate vegetative hyphal tips that grow out of the differentiated cell to re-establish a vegetative mycelium Principle 10 In arriving at a morphogenetic structure and/or a state of differentiation, fungi are tolerant of considerable imprecision (= expression of fuzzy logic), which results in even the most abnormal fruit bodies (caused by errors in execution of the developmental subroutines) being still able

Table 1. (Continued)

to distribute viable spores, and poorly (or wrongly) differentiated cells still serving a useful function Principle 11 Mechanical interactions influence the form and shape of the whole fruit body as it inflates and matures, and often generate the shape with which we are most familiar

Source: From Moore (2005).

long axis of the hypha. Consequently, fungal morphogenesis depends on the placement of hyphal branches. A hypha must branch to proliferate. To form a multicellular structure, the position at which the branch emerges and its direction of growth must be controlled. A major aspect of that directional control is an autotropism—a tropism to self—in which growth direction of each hyphal branch is influenced by the position of the rest of the mycelium. Exploratory mycelia experience a negative autotropism, which causes them to grow away from the main mycelium and this maintains the outward exploration of the substratum. On the other hand, to create a multicellular structure like a fruit body, positive autotropism is essential to cause hyphae to grow together for hyphal branches to cooperate and coordinate their activities. Tropic reactions imply a signalling system, a signal sensing system and a reaction system. Mathematical models of these systems can be created very successfully (Stockus and Moore, 1996; Meskauskas et al., 1998, 1999a, 1999b, 2004a, 2004b; Moore et al., 2006), but we know nothing yet about their biochemistry, cell biology or molecular nature. However, it is clear that what mechanisms exist must be different to animals and plants because gene sequences known to regulate development in animals and plants do not occur in fungal genomes (Moore et al., 2005; Moore and Meskauskas, 2006).

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