Growth, Differentiation and Sexuality

358 L.A. Casselton and M.P. Challen
A. Breeding Systems
Historically, heterothallic basidiomycete fungi
were classified as bipolar or tetrapolar, depending
on whether mating type was determined by one
or two loci. Where there is just a single locus in
bipolar mushroom species, this was designated
A and in tetrapolar species with two loci, these
were designated A and B (see Raper 1966 for
a historical account of the discovery of mating type
systems, in particular the pioneering studies of
Kniep and Bensaude). In most species, the two loci
are unlinked. For compatibility, mates must have
different alleles of all genes, and the names bipolar
and tetrapolar derive from the fact that two mating
types segregate at meiosis in the former, and four
inthelatter.Thematingtypelociwererecognised
as being complex long before this was confirmed by
molecular analyses, and the terms A factor and B
factor will be found in older literature. Hence, these
breeding systems are also called unifactorial and
bifactorial. Estimates of the frequencies of the two
types of breeding systems in homobasidiomycetes
are that 49%–65% are tetrapolar, 25% are bipolar
and 10%–15% are homothallic (Whitehouse 1949;
Quintanilha and Pinto-Lopes 1950). Because of
the complex structure and high levels of sequence
dissimilarity at the mating type loci, we no longer
equate different versions of A and B with alleles,
as assumed in the classical literature (Raper 1966),
and the term specificity is now more generally
used to describe their different versions. The more
mating types there are, the greater the chance
of finding a compatible partner – outbreeding
efficiency is high; ten A specificities in bipolar
species are sufficient to generate 90% outbreeding
efficiency whereas it requires 20 specificities of
both A and B to give the same potential in tetrapolar
species (based on the calculation one gene
(nA −1)|nA; two genes (nAnB − nA − nB +1)|nAnB,
Koltin et al. 1972). The numbers of different specificities
are surprisingly high in the species studied
to date; for example, S. commune is estimated to
have 288 A and 81 B specificities (generating more
than 20,000 mating types; Raper 1966), C. cinereus
164 A and 79 B specificities (generating more than
12,000 mating types; Raper 1966), and Pleurotus
populinus 126 A and 354 B specificities (generating
nearly 45,000 mating types; James et al. 2004b). U.
maydis is also a tetrapolar species, the mating type
loci in this fungus are designated a and b, and there
are just two alleles of the a locus and some 25 of the
b locus (Christensen 1931; Rowell and de Vay 1954).
The genes found at the mating type loci of U.
maydis and the tetrapolar homobasidiomycetes are
highly conserved in function. At one locus, there
are genes that encode transcription factors belonging
to the homeodomain family, and at the other,
genes encoding pheromones and receptors (see
Sect. II.A). Locus designations predate a knowledge
of the functions of the genes, and it is now
rather unfortunate to discover that the A locus of
homobasidiomycetes is equivalent to the b locus of
U. maydis, and the B locus of homobasidiomycetes
is equivalent to the a locus of U. maydis! InC. neoformans,
the morphological changes that occur
during mating are very similar to those occurring
in homobasidiomycetes (Kwon Chung 1975) but
remarkably, the organisation at the mating type locus
is totally different (Lengeler et al. 2002; Hull
et al. 2005). There are two versions of the locus,
MATa and MATα; both extend over more than
100 kb and contain some 20 genes, some are relevant
to mating, others are not, and some encode enzymes
normally associated with downstream mating
events (see Sect. II.).
B. Developmental Pathways
To understand the role of the mating type genes,
we need to look at the developmental pathways
they regulate. Relevant stages in the life cycles of
U. maydis, C. cinereus and C. neoformans are illustrated
in Figs. 17.1, 17.2 and 17.3. Life cycles of these
fungi have been reviewed by Banuett (1995), Kües
(2000), and Hull and Heitman (2002) respectively.
One feature of the basidiomycete life cycle that is
crucial to understanding mating type gene function
is the extended period between mating cell
fusion and nuclear fusion. In the model species illustrated,
mating cell fusion generates a specialised
mycelium known as a dikaryon, in which the nuclei
of both mates remain paired in each cell and
divide in synchrony. In many basidiomycetes, the
dikaryon has structures known as clamp connections,
which we can see in both C. cinereus and C.
neoformans, and these are formed every time the
tip cell divides. The paired nuclei in each cell fuse
only in cells that are specialised for meiosis.
U. maydis is a dimorphic fungus that
is pathogenic on Zea mays. The asexual stage is
saprophytic and composed of unicellular, yeast-like
cells that divide by budding. When cells are mating,
they secrete small pheromones that bind receptors
on the surface of compatible mating partners. The