12.9 Co-ordination of cell inflation throughout the maturing fruit body
As you can see from the descriptions above, most of the changes in shape during fruit body development in basidiomycetes depend on cell inflation; this is typically a slow process in young primordial stages and characteristically more rapid during late maturation. Local cell inflation during fruit body development has often been described and Reijnders (1963) showed that the different zones of fruit bodies enlarge proportionally, so that different tissues mature without being impeded, compressed or distorted by the growth of other parts. Such co-ordination of differentiation of cells in relation to their location is one of the most important general principles of animal and plant morphogenesis. It is thought to be based upon the migration through the developing tissues of pattern-forming morphogenetic factor(s) or signals.
If this is true for fungi, the nature of the signals is obscure, though in the larger fruit body primordia of Ascomycota and Basidiomycota the mechanism would need to operate over distances of many millimetres, a similar scale to animal and plant hormone fields. However, apparent ‘co-ordination’ could also result if developmental events are arranged in a consequential series such that one (secondary) event is only instigated by the initiation or completion of an earlier (primary) event. For any conclusion to be reached on this issue what is needed is an holistic study of inflation over the whole fruit body and an assessment of the correlation between cell behaviour in widely separated locations against an accurate time frame. This was done by Hammad et al. (1993b) for the fruit body of Coprinopsis cinerea.
This study examined a sufficiently large sample of fruit bodies to establish the exact timing of major meiotic and sporulation events, and this provided the basic timeline to which other processes could be referenced simply by microscopic examination of a small piece of cap tissue. Removing small tissue fragments (‘biopsies’) for rapid microscopic examination does not interfere with fruit body development. This timeline is objective in the sense that it depends upon processes which are endogenously controlled. It is reliable because these processes are central to fruit body function and it is versatile since by examining slivers at known (real) time intervals the effects of any change in cultivation conditions or culture genotype become apparent.
In the cultivation conditions described by Hammad et al. (1993b), fruit body primordia were formed 5 d after inoculation of the culture medium and developed into mature fruit bodies within 2-3 days, during which the basidia underwent a sequence of morphologically and physiologically distinctive stages.
- The dikaryotic protobasidia underwent nuclear fusion (karyogamy) and then entered meiosis I, followed immediately by meiosis II.
- After completion of meiosis, four sterigmata emerged
- followed by formation of four basidiospore initials,
- nucleus migration,
- maturation and discharge of the spores.
All these events were completed within 18 h, and the overlap between different stages varied through development.
- In a ‘meiosis I specimen’ about 60% of the basidia had two nuclei;
- at meiosis II about 70% had four nuclei;
- when sterigmata first appeared about 90% of the basidia were at the same stage.
Defining karyogamy as time zero, basidia took 5 h to reach meiosis I and meiosis II was completed after a further hour. From meiosis II to the emergence of sterigmata required 1.5 h, spores emerging 1.5 h after that. Spore formation continued for 1 h and then nuclear migration started. Spore pigmentation commenced 1 h after spore formation and spores matured and were discharged 7 h later.
Co-ordination of cell inflation was studied by measuring cell sizes in microscope sections of fruit bodies of Coprinopsis cinerea whose chronological development was defined by the stage they had reached in meiosis and sporulation.
As far as cell inflation was concerned (measured in terms of cell area in tissue sections), there was only a small increase before meiosis. Presumably, any fruit body expansion occurring in these early stages is due primarily to cell proliferation rather than cell inflation. In contrast, there was a large increase in cell profile area in sections of fruit bodies undergoing meiosis. The average length-to-width ratio of the cells in stems before meiosis (fruit bodies up to about 8 mm tall) was about 2, but this increased greatly after meiosis, to 10 in 48 mm tall fruit bodies, 20 in 55 mm tall fruit bodies and approximately 35 in fruit bodies that were 83 mm tall. The phase of most rapid stem elongation occupied the 5 h prior to spore discharge and started 8 h after karyogamy. Cap expansion started as spores matured, 14 h after karyogamy.
The most remarkable feature of these data was that rapid stem elongation was correlated with the ending of meiosis. Indeed, inflation of all the different cell types in the cap as well as elongation of cells of the stem began immediately after meiosis.
Elongation of the stem is necessary to raise the cap into the air for more effective spore dispersal; inflation of the different cell types in the gill tissue is also necessary for effective spore dispersal so co-ordination of cell inflation across the whole fruit body is clearly advantageous. The co-ordination that is observed may be achieved by some sort of signalling system that ‘reports’ the end of meiosis to spatially distant parts of the fruit body and initiates cell expansion. Indeed, stem elongation was significantly greater when the cap was left attached than when it was removed and leaving half of the cap in place was sufficient to ensure normal elongation.
This effect of surgical removal of cap segments on stem elongation has been observed with several species of mushroom over the years. Generally speaking, the elongating stem curves away from the side with the cap segment left intact (providing it contains gill tissues) and this has been interpreted as indicating that the gills are the source of a ‘growth hormone’. Unfortunately, the information we have about hormonal effects in mushrooms is sparse and unsatisfactory (Moore, 1991; Novak Frazer, 1996) and no definitive fungal growth hormone of any sort has been chemically isolated even now; which is a remarkable statement for a kingdom of organisms which have been known for many years to include pathogenic/parasitic representatives that produce both animal and plant hormones.
Updated December 17, 2016