Growth, Differentiation and Sexuality

376 M. Feldbrügge et al.
different alleles (Kämper et al. 1995). Under natural
conditions, the heterodimeric bE/bW complex
is formed after fusion of compatible cells,
and it is this complex which triggers all subsequent
steps of pathogenic as well as sexual development.
U. maydis was the first basidiomycete
in which the mating type loci were cloned and
their mode of function elucidated. Subsequently,
it was shown that the mating type loci of all basidiomycete
fungi consist of variations of this general
scheme: pheromone and pheromone receptors
on the one hand, and homeodomain gene
pairs on the other. However, the developmental
processes controlled by these loci are quite distinct,
and the structure of these loci in the homobasidiomycete
fungi is much more complex than in U.
maydis. This topic is reviewed elsewhere in this volume
(see Chap. 17, this volume). The filamentous
dikaryon of U. maydis requires the plant for sustained
growth, and this phase is therefore termed
biotrophic. On the plant surface, prior to penetration,
the hyphae have a peculiar growth modus:
while the filament expands at the tip, the cytoplasm
from the rear moves forwards. The distal region of
the tip cell becomes vacuolated and eventually collapses
to leave empty sections behind, which are
sealed off by regularly spaced septa (Fig. 18.1, steps
3 and 4). Stimulated by an unknown signal on the
plant surface, hyphae stop polar growth. Their tips
swell and non-melanized appressoria are formed.
Subsequently, infection hyphae are formed which
penetrate the plant tissue (Fig. 18.1, step 4). Plant
penetration is presumably aided by lytic enzymes.
The penetrating hyphae are never in direct contact
with the host cell cytoplasm but appear surrounded
by invaginated plasma membrane of the
plant. Within the plant, dikaryotic hyphae undergo
anumberofdevelopmentallyregulatedmorphological
transitions which have been described in
detail by earlier workers (Snetselaar 1993; Snetselaar
and Mims 1994; Banuett and Herskowitz
1996). Massive fungal proliferation is a late event
occurring only 5–6 days after infection within the
tumour tissue, and is followed by sporogenesis
(Fig. 18.1, step 5). Except for the induction of anthocyanin
pigmentation, there are no apparent host
responses, suggesting that U. maydis either shields
itself from being recognized or is actively suppressing
plant defence pathways. When the heavily
melanized diploid spores germinate, they produce
a promycelium in which meiosis takes place and
from which haploid sporidia are released by budding
(Fig. 18.1, step 6).
U. maydis is not only a fully developed genetic
system but is also amenable to efficient reverse
genetics. The emphasis in the beginning of the
molecular era has been to unravel the events
triggered by the mating type loci. More recently,
these studies have been extended to the cell
biological level, as it became increasingly apparent
that morphological transitions are a prerequisite
for disease. Publication of the 20.5-Mb genome
sequence ofU. maydis in2003 through the BroadInstitute
and Bayer CropScience (http://www.broad.
mit.edu/annotation/fungi/ustilago_maydis/) has
created a wonderful resource for comparative
genetics and has opened up new avenues for
research. In this review, we will emphasize the
current status of signalling networks underlying
mating and pathogenic development, summarize
our current understanding of the complex morphological
transitions which govern disease, and
indicate which challenges lie ahead.
II. Signalling Networks
Distinct stages of the U. maydis life cycle are regulated
by intricate signalling networks. These not
only trigger fusion of haploid cells during mating
but coordinate all morphological transitions necessary
for pathogenic development.
A. Signalling Network During Mating
The biallelic a locus encodes components of an
intercellular recognition system consisting of
lipopeptide pheromones (mating factor a1 and
a2; Mfa1 and Mfa2) and cognate seven-transmembrane
pheromone receptors (pheromone
receptor a1 and a2; Pra1 and Pra2; Froeliger
and Leong 1991; Bölker et al. 1992). The ability
of cells to fuse is dependent solely on the a
locus. The expression of all mating type genes is
pheromone-inducible, and this is conferred by
pheromone response elements in the regulatory
regions of these genes (Urban et al. 1996b).
The key transcription factor determining basal
as well as pheromone-responsive expression of
mating type genes is the pheromone response
factor (Prf1), a transcription factor which recognizes
pheromone response elements via its
sequence-specific HMG (high mobility group) box
DNA-binding domain (Hartmann et al. 1996).
Comparable to pheromone signalling in other