12.13 Comparisons with other tissues and other organisms

So far we have described a particular example in which intermediary metabolism is a major contributor to cell differentiation and fungal morphogenesis. Given that cell inflation and tissue expansion are crucial aspects of fruit body maturation in the majority of fungi, it seems reasonable to ask whether this particular example can be generalised. The key observation in Coprinopsis cinerea was that urea increased by a factor of 2.5 on a dry weight basis but the urea concentration on a fresh weight basis was essentially unchanged during cap development, leading to the inference that urea behaves as an osmoregulator, driving water into hymenial cells and thereby driving expansion of the fruit body cap.

Agaricus bisporus also accumulates substantial amounts of urea in fruit bodies, and content varied with stage of development (Wagemaker et al., 2005). However, in A. bisporus and Lentinula edodes, mannitol (a sugar alcohol, or polyol) is synthesised to serve an analogous osmoregulatory function (Hammond & Nichols, 1976; Tan & Moore, 1994). To support accumulation of large amounts of mannitol, activity of the pentose phosphate pathway (PPP; Fig. 8. in Chapter 10 CLICK HERE for a reminder), though it is always at low activity in mycelium, is specifically elevated by a factor of about 15 times in the fruit body (Tan & Moore, 1995). Elevated PPP has also been noted in Pleurotus pulmonarius, but in this organism it seems that fruit bodies are characterised by elevated levels of both urea and polyols. The genome of the related sclerotium-forming mushroom Pleurotus tuber-regium has been sequenced and used to study the carbohydrate metabolising enzymes involved in the bioconversion of the lignocellulose of the substrate to β-glucan reserves within the hyphae of this white-rot fungus (Lam et al., 2018).

Patyshakuliyeva et al. (2013) studied the expression of genes encoding various carbon metabolism enzymes from different growth stages of Agaricus bisporus, correlating gene expression, enzyme activities and soluble carbohydrates in the hyphae of compost, casing layer and fruit bodies. They found that compost grown vegetative mycelium consumes a wide variety of monosaccharides, however only hexoses or their conversion products are transported from the vegetative mycelium to the fruit body, where only hexoses accumulate and only hexose catabolism occurs. Genes encoding enzymes that degrade plant cell wall polysaccharides were mainly expressed in compost-grown mycelium but were absent from fruit bodies. Whereas, genes encoding fungal cell wall modifying enzymes were expressed in both fruit bodies and vegetative mycelium, but with different gene sets being expressed. In a similar transcriptomic analysis of Pholiota microspora (commonly known as nameko, a small mushroom used as an ingredient in miso soup) revealed significant differences in gene expression between mycelium, primordia and fruit bodies, and suggests that mannitol, trehalose, glycogen and β-glucan play key roles in regulating carbohydrate metabolism and storage in the development of fruit bodies (Zhu, 2018).

The expansion and elongation of cells in the stem are essential aspects of stem elongation in Coprinopsis cinerea, but stem metabolism contrasts dramatically with cap metabolism. Differences between the two (interconnected) tissues are so great as to indicate that the common result is achieved in very different ways. Reported differences between cap and stem include; different patterns of metabolite accumulation, in terms of carbohydrates and amino acids;  different patterns of metabolism of isotopically labelled substrates;  profound differences in the activities of particular enzymes, especially polyol dehydrogenases, chitin synthase, NADP-GDH, alkaline phosphatase, enzymes involved in ornithine metabolism, glucanase, and phenylalanine ammonia-lyase (Moore et al., 1979, and references therein). Nevertheless, elongation of the stem depends on an enormous increase in the volumes of its constituent cells and as the walls remain unthickened and most of the cell interiors are occupied by vacuoles, the stem must be supported by a hydrostatic skeleton.

Uptake of water by the stem during development is dramatic:

  • in developing from about 20 mm to about 100 mm long, the stem of an ‘average’ fruit body doubles its fresh weight with hardly any change in dry weight and absorbs nearly 200 mg of water.

The turgor pressure of stem cells remains constant throughout the period of stem elongation so appropriate osmoregulatory solute(s) must be formed and accumulated in the stem cells in parallel with the absorption of water and synthesis of wall. Low molecular weight carbohydrates are the best candidates as the stem osmoregulatory: trehalose, for example, can account for 18% of the final dry weight. Trehalose is a non-reducing sugar, but alcohol-soluble reducing sugars can account for 12% of the dry weight of mature stems.  Together, therefore, these sugars represent about 30% of the dry weight of the mature stem. Mannitol does not have any role in Coprinopsis cinerea (total polyols never exceed 6% of the dry weight and decline in quantity as the fruit body matures) though it was mentioned above as an osmoregulator in Agaricus bisporus and Lentinula edodes. For comparison, mannitol alone can amount to as much as 50% of the total fruit body dry weight in Agaricus bisporus, and 20 - 30% in Lentinula edodes.

The bulk of the osmotic potential of stem cells must be contributed by compounds of low molecular weight and it is probable that inorganic ions (especially potassium ions) make a very important contribution. So although the sugar content may account for a lesser fraction of the overall osmotic potential of the cell, it is a fraction which is readily adjusted by metabolism of materials already within the cell; something which is not possible with the inorganic components of the cell.

All of these data point to fundamental differences in the ways by which cell inflation and fruit body expansion are achieved in different fungi, and even in different tissues in the same fungus. Cap expansion is due to hyphal inflation in A. bisporus but depends on hyphal proliferation in L. edodes.

Interestingly, Coprinopsis cinerea (which expands by hyphal inflation) and Schizophyllum commune (which expands by hyphal proliferation) show many metabolic similarities despite the fundamental difference between their cellular strategies of expansion. Evidently, totally different tactics can be used to achieve the same strategic end. Presumably, during evolution the ‘choices’ have been made between different metabolic mechanisms which enable a morphogenetic process to be put into effect, and these have been made independently of ‘choices’ between particular cellular processes which might contribute to that morphogenesis.

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Updated July, 2019