Growth, Differentiation and Sexuality

lar level but two patterns emerge, one exemplified
by Ustilago hordei and the other by Coprinus (Coprinellus)
disseminatus. InU. hordei, a close relative
of U. maydis, there are only two mating types
(MAT1 and MAT2). The alternative loci each contain
genes found at the a and b loci of U. maydis,
apairofbW/bE genes, and a pheromone and receptor
gene. There are only two alleles of the a and b
genes but different allelic versions of these are necessary
for a compatible mating, in the same way
as they are in U. maydis (Bakkeren and Kronstad
1993, 1994; Anderson et al. 1999). A bipolar mating
behaviour arises because the a and b genes of
U. hordei are linked on the same chromosome. Remarkably,
the genes are separated by 430–500 kb
of non-mating type-specific sequence but recombination
suppression means that only two allele
combinations exist in nature (Lee et al. 1999).
In the homobasidiomycetes, bipolar species
are found in all phylogenies, indicating that these
have arisen independently many times (James
et al. 2003). Unlike smuts, however, there is no
evidence that the two classes of mating type genes
have become linked. It appears that the A locus
is sufficient to confer mating type identity, and
the B genes have lost their role as mating type determinants.
Two pairs of closely linked HD1/HD2
genes have been found in C. disseminatus (James,
personal communication) and a single pair in the
commercial mushroom Agaricus bisporus (Li et al.
2004). Receptor and pheromone genes have been
found in C. disseminatus but these are not linked to
the A locus, and they are not polymorphic (James
et al. 2003). It is unlikely that pheromone signalling
is dispensable in bipolar mushrooms, because
the MAPK pathway that it activates plays such an
essential role in dikaryosis. Indeed, nuclear migration
occurs during mating in C. disseminatus,
and the dikaryon has fused clamp connections
(James, personal communication), developmental
steps that are pheromone-dependent in tetrapolar
species. A pheromone or receptor gene mutation
or a recombination event could bring a compatible
receptor/pheromone gene combination together,
and would replace the need for mating to do
this. A compatible combination of genes might
constitutively activate the MAPK pathway; alternatively,
the receptor and pheromone genes may be
induced only once a compatible A gene interaction
is established. The latter is more likely, since
mutation studies (described below) show that
a constitutive pheromone response can severely
disadvantage growth of the monokaryon.
Mating Type Genes in Basidiomycetes 367
C. Homothallic Species
In ascomycete fungi, several homothallic species
have been looked at and found to contain functional
mating type genes. In some species, the genes that
are normally found in the alternative forms of the
MAT locus are combined at a single, complex matingtypelocus,asinSordaria
macrospora (Jacobsen
et al. 2002; see Chap. 15, this volume). In some
cases, compatible genes have become fused and
encode chimeric proteins that are effective in promoting
sexual development (reviewed by Turgeon
1998). It is not surprising that mating type genes
are essential for sexual development in homothallic
species, since we know that they are required to
activate the genes that bring about the same developmental
programme in heterothallic species. At
present, we know little about homothallic basidiomycetes
but preliminary studies with Agaricus
species indicate that the A mating type genes at
least are present (Burrow, Casselton and Challen,
unpublished data). A scan of the recently published
Phanerochaete chrysosporium genome sequence
identified five potential pheromone receptorgenesandanunlinkedpairofHD1-HD2
genes
(Martinez et al. 2004). Assuming this species is homothallic,
as originally reported (Alic et al. 1987),
the finding of all the mating type genes would confirm
our predictions that they are still essential for
sexual development. However, other authors suggest
that this species is heterothallic and has a bipolar
mating system (James et al. 2003).
Mutations that lead to self-compatibility have
long been known in S. commune and C. cinereus,
and one could ask whether these might give clues
to the origin of homothallism. Strong selection was
needed to recover the mutants; incompatible matings
between monokaryons with the same A specificities
or the same B specificities were used to select
for rare mutations that would convert these
mycelia into fertile dikaryons (Parag 1962; Raper
et al. 1965; Day 1963a; Haylock et al. 1980). The
mutations obtained were predominantly dominant
and mapped within the A or the B loci. Mutants
characteristically showed constitutive expression
of the pathway normally induced by a compatible
combination of the corresponding non-mutant
genes. A mutants produce mycelia with unfused
clamp connections and B mutants, at least in S.
commune, produce mycelia in which nuclear migration
is actively occurring (see Raper 1966). Mutant
B strains in S. commune are slow growing and
lack aerial mycelium, a phenotype known as ‘flat’