Growth, Differentiation and Sexuality

182 B.C.K. Lu
be arrested at diffused diplotene under a continuous
light regime (Lu 2000), and no triggering of
apoptosis will occur. When the arrest is released
with a 3-h dark period, meiotic progression will
resume and the timing of apoptosis can be accurately
identified (Lu et al. 2003).
Why is meiosis-specific apoptosis important in
some organisms, and not in others? It occurs in
C. cinereus but not in yeasts, or Neurospora,where
meiosisgoestocompletionirrespectiveofanygenetic
damages (reviewed in Lu 1996). The same dichotomy
is found in higher eukaryotes. It is found
in mammals (e.g., mice) but not in Drosophila, C.
elegans, nor plants. Why evolution has taken a different
path is not clear, and one can only speculate.
As suggested by Money (2003), basidiospores
of C. cinereus are carried to a fertile ground to
competewithothermicrobes,tosustaingrowth,
and then to find a mate. Chances of success are
really quite remote, but particularly critical for C.
cinereus whose sexuality is a tetrapolar mating system,
whereby only one quarter of the progeny will
be compatible. For altruistic reasons, evolution has
selected meiotic apoptosis to ensure that all spores
produced are genetically healthy for the survival of
the species. Apoptosis is basidia-specific, because
if the damage is induced during meiosis, apoptosis
will remove the damaged cells and allow the mushroom
to recover by generating new basidia, such as
the case with diplotene arrest reported earlier (Lu
et al. 2003). As for mammals, this is even more critical,
because the litter size is small; the evolution
of meiotic apoptosis is much more refined than to
have a continuous molecular safety check – hence,
the multiple checkpoint controls. As for yeast, Neurospora,
Drosophila, C. elegans, and plants, they all
producealargenumberofprogenyandtheirmating
system is simple, but it is not at all clear why
they do not have meiotic apoptosis.
VIII. Conclusion
There is no question that programmed cell death
(PCD) operates in fungi, albeit at a prototypal level,
and it includes apoptotic and autophagic pathways.
The hallmarks of apoptosis can be induced
by the expression of heterologous proapoptotic
genes in yeasts. They can also be induced by
exogenous stimuli, genetic defects, pheromones,
oxygen stress, and even by aging, and cell death
inducedbyalloftheabovecanberescuedby
the co-expression of antiapoptotic genes. Most
importantly, the PCD is intimately connected to
mitochondria and to the ubiquitin-proteasome
system, in much the same way as in the metazoans.
It also plays a role in tissue remodeling. The
discovery of caspase-like or metacaspase genes,
a possible homolog of a Bcl-2 family gene, and
a homolog of AIF, BI-1, and IAP genes in yeast
and other fungi makes the story compelling, and
even the skeptics have begun to see the light.
Meiotic apoptosis occurs in some species, and not
in others. This dichotomy is found in fungi as well
as in animals. This intriguing question remains to
be explored.
Acknowledgements. I thank Dr. Stéphen Manon and Dr. K.
Tsurugi for kindly providing the original drawings and EM
photos, and for permission to use them. I am grateful to
the volume editors for editorial suggestions, and to my sons
Albert and Andrew for reading the manuscript.
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