12.15 Degeneration, senescence and death
Death is an important aspect of biology in the other two major eukaryotic kingdoms and in fungi, too. This is another cellular processes that contributes to morphogenesis. Removal of old individuals makes way for the young and allows populations to evolve, and programmed cell death (PCD) has been recognised as a crucial contributor to morphogenesis in both animals and plants. PCD is the removal of tissue in a manner controlled in time and position. There are two types of cell death: traumatic or necrotic death and apoptosis or programmed cell death.
In higher animals PCD involves a sequence of well-regulated processes, including synthetic ones, which lead to internal cell degeneration and eventual removal of the dying cell by phagocytosis. It is important that apoptotic elimination of cells is intracellular in higher animals to avoid escape of antigens and the consequent danger of an immune response to components of the animal’s own cells (autoimmunity). This is not a consideration in plants and fungi. The most obvious example of fungal PCD is the autolysis that occurs in the later stages of development of ink cap mushrooms which was long ago interpreted as an integral part of fruit body development (autolysis removes gill tissue from the bottom of the cap to avoid interference with spore discharge from regions above). Autolysis involves production and organised release of a range of lytic enzymes (Iten, 1970; Iten and Matile, 1970), so autolytic destruction of these tissues is clearly a programmed cell death.
There is only one experimental study of the longevity of fungal fruit bodies. Umar & Van Griensven (1997a) grew the cultivated mushroom in artificial environments which protected the culture from pests and diseases. They found that the life span of fruit bodies of Agaricus bisporus was 36 days. Ageing was first evident in fruit bodies about 18 days old, when localised nuclear and cytoplasmic lysis was seen, and after 36 days most of the cells in the fruit body were severely degenerated and malformed. Nevertheless, a number of basidia and subhymenial cells were alive and cytologically intact even on day 36. So even in severely senescent fruit bodies healthy, living cells were found and these are presumably the origin of an unusual phenomenon known as renewed fruiting.
Field-collected fruit body tissues of a mushroom usually generate abundant vegetative hyphae when inoculated onto nutrient agar plates. Such reversion from the fruiting stage into vegetative stage is not an abrupt process, rather there appears to be some sort of ‘memory’ of the differentiated state. Initial hyphal outgrowth from gill lamellae usually mimics the densely packed branching and intertwined hyphal pattern of the gill tissues at first, being quite unlike the pattern of normal vegetative hyphae in culture. The ‘memory’ need be no more than the residual expression of differentiation-specific genes (such as the hydrophobins, (Wessels, 1994a & b, 1996)) before their products are diluted out by continued vegetative growth.
Renewed fruiting (the formation of fruit bodies directly on fruiting tissue) is not uncommon, and it can occur at various locations (cap, stem and/or gills) in improperly stored excised fruit bodies. Experiments in vitro show that numerous primordia can arise on excised fruit body tissues and can mature into normal, though miniature, fruit bodies. In comparison to vegetative cultures, the excised fruit body tissues form fruit bodies very rapidly. For example, in Coprinopsis cinerea, renewed fruiting occurred within four days, compared with cultures inoculated with vegetative dikaryon which, under the same conditions, formed fruit bodies in 10 to 14 days (Chiu & Moore, 1988a; Brunt & Moore, 1989; Bourne, Chiu & Moore, 1996). Renewed fruiting may have an important role in survival, consuming and immediately recycling the resource in the dying fruit body tissue to disperse further crops of spores.
Umar & Van Griensven (1997b, 1998) found that cell death is a common occurrence in various structures starting to differentiate, for example the formation of gill cavities in Agaricus bisporus. The authors point out that specific timing and positioning imply that cell death is part of the differentiation process. Fungal PCD could play a role at many stages in development of many species (Umar & Van Griensven, 1998). Individual hyphal compartments can be sacrificed to trim hyphae to create particular tissue shaping. PCD is used, therefore, to sculpture the shape of the fruit body from the raw medium provided by the hyphal mass of the fruit body initial and primordium. In several examples detailed by Umar & Van Griensven (1998) the programme leading to cell death involves the sacrificed cells over-producing mucilaginous materials which are released by cell lysis. Remember that in autolysing Ink Cap gills the cell contents released on death contain heightened activities of lytic enzymes. Evidently, in fungal PCD the cell contents released when the sacrificed cells die are specialised to particular functions too.
Updated December 17, 2016