21st Century Guidebook to Fungi, SECOND EDITION, by David Moore, Geoffrey D. Robson and Anthony P. J. Trinci

Table of Contents

1. Chapter 11: Exploiting fungi for food
2. Chapter 12: Development and morphogenesis
   1. Development and morphogenesis
   2. The formal terminology of developmental biology
   3. The observational and experimental basis of fungal developmental biology
   4. Ten ways to make a mushroom
   5. Competence and regional patterning
   6. The Coprinopsis fruit body: making hymenia
   7. Coprinopsis and Volvariella making gills (not forgetting how polypores make tubes)
   8. The Coprinopsis fruit body: making stems
   9. Co-ordination of cell inflation throughout the maturing fruit body
   10. Mushroom mechanics
   11. Metabolic regulation in relation to morphogenesis
   12. Developmental commitment
   13. Comparisons with other tissues and other organisms
   14. Genetic approaches to study development: through the classic to genomic systems analysis
   15. Senescence and death
   16. Basic principles of fungal developmental biology
   17. Relevance to commercially cultivated fungi
   18. Chapter 12 References and further reading
   19. Buy a PDF of Chapter 12
3. Chapter 13: Ecosystem mycology: saprotrophs, and mutualisms between plants and fungi

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. Section 9.4, above, describes the genetic circuit leading specifically to competence in Aspergillus conidiophores (Noble & Andrianopoulos, 2013; Lee et al., 2016). Vegetative compatibility systems can also contribute to mycelial interaction (Section 7.5), but it is usually governed by the mating type factors (Chapter 8) and results in formation of a sexually compatible mycelium, which is competent to make fruit bodies.

However, in the higher fungi, even a haploid mycelium can have several alternative developmental pathways open to it: continuation of hyphal growth, production of asexual spores, and/or formation of asexual multihyphal structures (stromata, sclerotia, etc.), so a compatible mating opens up the additional pathways associated with progress into the sexual cycle. 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. Exposure to blue light induces hyphal knot formation in Coprinopsis cinerea mycelia grown on low-glucose media but not in mycelia grown on high-glucose media; on low-glucose media, many hyphal knots are visible near the edge of the colony one day after a 15-minute exposure to blue light. Transcriptome analysis revealed a two-stage response to illumination. Several genes are upregulated by 1 h of blue light exposure in the mycelial region where the hyphal knot will be developed; this upregulation is not influenced by nutrients. These genes are thought to be essential for induction, but not sufficient for development of the hyphal knots. In the second expression stage, genes involved in the architecture of hyphal knots are upregulated after a 10-16 h blue light exposure if the mycelia are cultivated on low-glucose media (Sakamoto, 2018; Sakamoto et al., 2018).

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 et al., 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 the ‘epidermal’ layers of cells that separate adjacent tissues, and evidence is accumulating that these epidermal layers perform specific functions. The pileipellis is the epidermis of the mushroom cap (micrographs in Figs 1 & 11). Mechanically isolated pileipelles (‘skins’) from five genera of Basidiomycota reduced water loss by factors of 10 to 30, and also reduced oxygen permeability (Lendzian & Beck, 2021). Indeed, as such isolated fungal skins are thin flexible sheets of a living homogeneous mycelium made by a filamentous fungus they are being considered as ‘sensing skin components’ for potential living architectures (self-growing/adaptive robots) and for upcycling into paper-like materials for printing, wound dressings, filtration membranes, and specialist coatings (Adamatzky et al., 2021a & b; Gandia et al., 2021).

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 May, 2021