Introduction to Fungi, Third Edition

644 USTILAGINOMYCETES: SMUT FUNGI AND THEIR ALLIES
at ‘Holliday junctions’ between paired DNA
double helices (see p. 317; Holliday, 1962, 1964).
Areas of ongoing research on U. maydis are
described in subsequent sections. Work on
U. maydis has greatly benefited from the ease
with which the haploid phase of this fungus can
be grown in culture and transformed by molecular
biology tools. The complete genome of this
fungus has now been sequenced, and this should
stimulate further research.
The teliospores of U. maydis are long-lived and
can survive in the environment (e.g. the soil) for
several years. Dikaryotic hyphae resulting from
the fusion of haploid sporidia can infect any
above-ground tissue of its host (wild and cultivated
Zea mays) by entry through stomata or
direct, appressorium-mediated penetration of the
epidermis (Snetselaar & Mims, 1992; Banuett &
Herskowitz, 1996). Infected host organs become
strongly hypertrophied to form galls. This is
in contrast to the small-grain cereal smuts
described above, in which symptom development
is confined to the developing seeds of the host,
and infection usually occurs at the seedling stage
followed by a prolonged symptomless phase. In
U. maydis, the entire process from dikaryon
formation on the plant surface to the release of
mature teliospores may take as little as 2 weeks
(Banuett & Herskowitz, 1996). In the field, infections
by U. maydis are most commonly observed
on the cobs presumably because the stigmata
with their thin epidermal layer are most readily
penetrated by the fungus (Snetselaar & Mims,
1993). As a result of infection, the developing
seeds on the corn cob become replaced by
gall-like outgrowths (‘tumours’) which measure
about 1 5 cm in diameter (Plate 12h). Although
not generally welcomed by farmers, such infected
cobs are prized as a delicacy in the Mexican
cuisine (Pataky & Chandler, 2003).
Monokaryotic yeast cells of U. maydis synthesize
auxins, especially indole-3-acetic acid, in
pure culture (see Basse et al., 1996), and infected
hypertrophied host tissue also shows elevated
concentrations of this plant growth hormone. It
therefore seems likely that the production of
growth hormones by U. maydis in planta contributes
to the development of the striking disease
symptoms, although this has not yet been
formally proven. The mycelium of U. maydis
ramifies in these hypertrophied tissues, followed
by hyphal fragmentation and production of teliospores.
Although the dikaryotic phase is obligately
biotrophic in nature, U. maydis can be
stimulated to complete its life cycle in artificial
conditions if it is grown on living cell cultures of
Zea mays separated from the dikaryotic mycelium
by a membrane permitting the diffusion of
metabolites (Ruiz-Herrera et al., 1999). Deviations
from the life cycle as shown in Fig. 23.1 have
been described by Kahmann et al. (2000).
Mating and dikaryon establishment
Ustilago maydis is heterothallic and has two
mating type loci. A given dikaryon is fully
pathogenic only if it contains different idiomorphs
or alleles at both loci. Since it will
produce haploid progeny of four genetically
distinct types, the mating system is said to
be tetrapolar. Locus a has two idiomorphs,
a1 and a2, each of which encodes a mating
pheromone and the receptor for the pheromone
encoded by the opposite idiomorph. Two haploid
cells will mate if they contain opposite idiomorphs
at locus a, irrespective of their b alleles.
Conjugation can be induced experimentally even
between cells containing the same idiomorph if
the matching pheromones are added. Mating is
therefore purely driven by the pheromones
which are peptides containing 13 (peptide a1)
or 9 (peptide a2) amino acids derivatized with
a lipid (farnesyl) side-chain (Spellig et al., 1994).
A cell whose receptor has bound the pheromone
of the opposite mating type will arrest its
cell cycle in the G2 position and undergo a
morphogenetic change to produce a thin flexible
conjugation tube which grows chemotropically
towards the pheromone source (Snetselaar et al.,
1996).
The ability to infect maize plants and to
complete the life cycle is tightly linked to the
ability of the fusion cell to form dikaryotic
hyphae. This is controlled by the b locus after
conjugation of compatible cells. In contrast to
the a locus which has two idiomorphs with low
sequence homology, the b locus has about 25
alleles which are genetically relatively similar to
each other. Each allele encodes two proteins