12.15 Senescence and death

Senescence and death are important aspects of biology in the other two major eukaryotic kingdoms and in fungi, too (Shefferson et al., 2017). This is another cellular process that contributes to morphogenesis, as well as contributing to the evolutionary biology of the organism. Removal of old individuals makes way for the young and allows populations to evolve, and programmed cell death (PCD), which is the removal of tissue in a manner controlled in time and position, has been recognised as a crucial contributor to morphogenesis in both animals and plants. 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’ could be no more than the residual expression of differentiation-specific genes before their products are diluted out by continued vegetative growth, but as we have shown above (Section 12.14), there is considerable scope for epigenetic marks in fungi.

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 (Moore, 2013). 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.

Fungal cultures suffer spontaneous degeneration through successive subculture on artificial media; the culture may stop growing or suffer loss of (or severe reduction of) asexual sporulation, sexuality, ability to fruit, or reduced production of secondary metabolites. Thus, fungal culture degeneration can be a significant economic problem for industrial production processes. Genomic instability is the cause of degeneration in Pleurotus ostreatus. Zhu et al. (2020) found that the DNA damage repair system, especially repair of double-strand breaks (DSBs) via homologous recombination, was impaired in the subcultured mycelium, and gradual accumulation of DSBs lead to strain degeneration after successive subculturing.

It’s a problem that applies as much to yeast cultures as to cultures of filamentous fungi. A budding yeast mother cell can produce a finite number of daughter cells before it stops dividing and dies, whereas filamentous fungal cultures frequently and spontaneously degenerate during ongoing culture maintenance, resulting in formation of sterile and/or weakly-growing sectors in the colony. Senescence seems to result from a progressive decline in physiological function, including mitochondrial dysfunction. This physiological decline is linked to impairments of cellular machines and to the generation of reactive oxygen species (chemically reactive molecules containing oxygen) which arise during normal metabolism (e.g., in the respiratory chain), and serve essential functions, but can cause molecular damage if in excess.

In Neurospora, senescing strains usually contain mitochondrial plasmids, which cause insertional mutagenesis when they integrate into the mitochondrial DNA. The functionally defective mitochondria replicate faster than the wild-type mitochondria and spread between hyphal cells (Maheshwari & Navaraj, 2008).  Senescence can also be due to spontaneous lethal nuclear or mitochondrial gene mutations. Ultimately the growth of a fungal colony ceases due to dysfunctional oxidative phosphorylation (Li et al., 2014; Wiemer et al., 2016). Although the detailed underlying processes may differ from species to species, this situation appears to be basically conserved between organisms and to be a major cause of degenerative diseases in humans (Morales-González, 2013); yet another area of eukaryote biology in which research on fungi can contribute to human health.

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Updated January, 2021