Growth, Differentiation and Sexuality

294 R. Debuchy and B.G. Turgeon
that contains one or the other of two possible
forms of genetic information establishing
mating type. An alternative mating strategy,
called self-compatibility, is less demanding than
self-incompatibility. Homokaryotic cultures of
self-compatible fungi can undergo self-mating.
These fungi (also known as homothallic fungi)
nevertheless perform all steps of meiosis. A special
case of self-compatibility (also known as pseudohomothallism
or secondary homothallism) has
been described for a few genera. These isolates can
be resolved into homokaryotic self-incompatible
cultures, indicating that isolates are heterokaryons,
carrying nuclei of opposite mating type. A survey
of 10,596 Ascomycetes showed that 55% may
reproduce sexually, but evidence of mating is
lacking for the remaining 45% of these species
(Reynolds and Taylor 1993). Whether or not these
apparently asexual species ever undergo sexual
reproduction, or have cryptic or rare sex is often
debated. A decade ago, shortly after mating-type
genes were first identified in filamentous fungi,
finding mating-type genes in asexual fungi was
a novel discovery (first reported by Sharon et al.
1996), but is now commonplace. Whatever the
reason for lack of a sexual stage (cryptic sexuality,
mutations in key genes), absence of the sexual
reproductive machinery is not the answer. This
finding supports the notion that the asexual
lifestyle arises from sexual progenitors.
This chapter emphasizes new developments
in our knowledge of mating-type structure in
self-compatible, self-incompatible, and asexual
Euascomycetes. It presents a possible scenario
for mating evolution among the three different
classes of fungi, as deduced from mating-type
structures, and considers functions attributed to
mating-type genes. Space limitations excluded
consideration of several fields that the reader
can find in other reviews focusing on, for example,
genetic aspects of unstable mating types
(Perkins 1987), theoretical aspects of mating
type (Metzenberg 1990), mating-type functions
(Metzenberg and Glass 1990), vegetative incompatibility
(Glass and Kuldau 1992), genetic
aspects of mating systems (Coppin et al. 1997),
physiology of intercellular recognition (Bistis
1998), evolution and pathology (Turgeon 1998),
mating types and biotechnology (Pöggeler 2001),
commonalities between Ascomycetes and Basidiomycetes
(Casselton 2002), and more general
aspects (Glass and Lorimer 1991; Glass and
Nelson 1994; Kronstad and Staben 1997; Hiscock
and Kes 1999; Shiu and Glass 2000; Souza et al.
2003).
II. Sexual Development
in Mycelial Euascomycetes
The life cycle of Euascomycetes that are used
as model systems, such as Podospora anserina
and Gibberella zeae, is presented in Fig. 15.1.
Self-incompatible homokaryotic strains of either
mating type produce female reproductive structures,
the ascogonia, and male cells, the spermatia.
The spermatia are true differentiated sexual
cells unable to germinate, in contrast to conidia.
Fertilization occurs between an ascogonium of
one mating type and a donor cell of opposite
mating type. The donor cells may be spermatia,
microconidia, macroconidia or hyphae. Ascogonia
are topped by a specialized hypha, the trichogyne,
which is attracted by the donor cell of opposite mating
type and eventually fuses with it (Bistis 1998).
Fertilization is followed by the migration of the
male nucleus down the trichogyne toward the body
of the female organ. During its migration, the male
nucleus passes by female nuclei and when present
in the body of the female organ, it undergoes a series
of mitotic divisions resulting in the formation
of plurinucleate cells containing nuclei of opposite
mating types. Successful production of offspring
depends on internuclear recognition, a process
associated with cellularization whereby two nuclei,
oneofeachmatingtype,migratetoformspecialized
dikaryotic hyphae. These hyphae, called
ascogenous hyphae, maintain a strict ratio of 1:1
of each parental nucleus. Eventually, the tip of this
type of hypha differentiates into a crozier, which
consists of two uninucleate cells and one dikaryotic
cell. Nuclei fuse and meiosis ensues immediately
while the cell is elongating to form the ascus. After
a post-meiotic mitosis, ascospores are delineated
inside the ascus and eventually projected outside
the fruiting body (see Chap. 20, this volume). In
self-compatible species, the male nucleus required
for fertilization is assumed to be provided to
the ascogonium by its basal cell, but outcrossing
indicates that external cells can occasionally be
the source of a male nucleus. Variations to this
description can be found in Euascomycetes, but the
formation of a plurinucleate cell after fertilization
and cellularization associated with internuclear
recognition leading to the formation of ascogenous
hyphae seems to be the common scheme.