Growth, Differentiation and Sexuality

416 D. Zickler
Third, a large pool of meiotic mutants have
been isolated in A. nidulans, N. crassa, P. anserina,
S. macrospora and C. cinereus, and molecular tools
are now available to characterize them (see below).
Fourth, publication of the genome sequences
of five ascomycetes (A. nidulans, Fusarium graminearum,
N. crassa, Magnaporthe grisea, P. anserina)
and four basiomycetes (C. cinerea, Cryptococcus
neoformans, Phanerochaete chrysosporium,
Ustilago maydis) provides a powerful basis for
genome comparison with other organisms, and
especially with the budding and fission yeasts,
in which a large spectrum of meiotic genes are
already characterized (e.g., Borkovich et al. 2004).
Homologies among genes involved in the meiotic
and sporulation processes establish rapid ways
to identify genes in the fungus of interest (even
when the sexual cycle is unknown, e.g., Pöggeler
2002). They offer also a starting point for the
identification of fungal-specific genes and/or
evolutionary gene requirements.
Fifth, the small chromosomal size of most fungi
was long considered a handicap for the general requirement
for good chromosome morphology to
study meiosis. However, since chromosome organization
can be investigated using tools such as
three-dimensional reconstruction from serial sections,
fluorescence in situ hybridization (FISH) and
green fluorescent protein (GFP) tagging, fungi became
model systems for investigating both meiotic
pairing and segregation (cf. references below, in
corresponding paragraphs).
Finally, everyone who has observed fungal
chromosomes knows that Barbara McClintock was
right when she said in her 1961 conference exposé
“You may think they (chromosomes of N. crassa)
are small when I show you pictures of them. But
when you look at them, they get bigger and bigger
and bigger” (cited in Perkins 1992).
The major purpose of the present review is to
explore similarities and differences in the better
known organisms, in order to identify key conserved
features of the meiotic process. Recent studies
based on genetic, molecular and cytological approaches,
combined with a rapidly growing arsenal
of mutations, have yielded a great deal of new information
about how pairing and synapsis relate to
other processes such as recombination and segregation
in budding and fission yeasts as well as in C.
cinereus and S. macrospora. In fact, the major task
of the prolonged meiotic prophase is orderly recognition
plus juxtaposition of the homologous chromosomes
and establishment of stable connections
via crossing-over. Throughout this period, events
at the DNA level and events at the chromosome
axis level are spatially and temporally coordinated.
Most of the review will therefore be dedicated to
these critical steps. Differences found when mutants
of different organisms are analyzed shed light
on our understanding of meiosis, and although
only few mycelial fungi are used as model organisms,
it is clear that they underline already both the
diversity and the potentiality of these organisms.
A clear example is given by the variety of gene silencing
mechanisms developed by some fungi before
and during meiosis. Differences underline also
thefactthatinthisvastgroupoforganismsthere
may be interesting “obscure” species awaiting the
opportunity to give important clues. Interestingly
also, mycelial fungi have developed a great variety
of methods for separating or bringing together the
pairs of nuclei that are issued from both meiotic divisions
and, when present, the postmeiotic mitosis.
Such movements imply a strict regulation of how
spindles are located, which is also discussed here.
Finally, an understanding of the meiotic process is
not only pivotal to furthering research on fertility
but also has important implications for fungal and
human disease curing.
II. Entering Meiosis: Mycelial Fungi
Devote Significant Resources
to Make Sure that the Two Nuclei
that Will Fuse Before Entering
Meiosis Have Identical Genomes
Mycelial fungi are self-fertile (also called selfcompatible
or homothallic) or self-sterile,
cross-fertile (self-incompatible or heterothallic).
In primary homothallic species, a homokaryotic
mycelium established from a single haploid
nucleus has the potentiality to progress through
both the dikaryotic stage and meiosis to complete
the sexual cycle. In secondary homothallic species
(also called “pseudoheterothallic”), a fertile
dikaryotic mycelium is established from a single
spore carrying two haploid nuclei of different
mating types. In heterothallic species, mating
between homokaryotic mycelia of different mating
types is required to complete the sexual cycle
(Fig. 20.1A; see also Debuchy and Turgeon, and
Casselton and Challen, Chaps. 15 and 17, respectively,
this volume). In all cases, there is a more
(cf. mycelial basidiomycetes) or less (cf. mycelial