Introduction to Fungi, Third Edition

THE ‘TRUE’ SMUT FUNGI (USTILAGINOMYCETES)
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Ustilago hordei
This is the type species of Ustilago, causing
covered smut of barley and oats. Crop losses
are usually less than 1% in well-managed
agrosystems (Thomas & Menzies, 1997). The
infection cycle has been described in detail by
Hu et al. (2002). The term ‘covered smut’ implies
that the teliospores produced in the cereal grains
replace the internal tissues but remain covered
by the outer layer (pericarp) of the grains and
are released only during threshing. Teliospores
attached to the outer surface of seeds will
germinate at the time of host germination.
The fusion of compatible monokaryotic yeast
cells results in a dikaryotic hypha which infects
the young seedling. The epidermal cells are
penetrated directly from slightly swollen
hyphal tips, which may be regarded as rudimentary
appressoria. There then follows an extended
phase of systemic growth without outward
symptoms of infection. Colonization of the host
is chiefly intracellular but also intercellular.
Differentiated haustoria are not produced.
Instead, hyphae grow through host cells, invaginating
the plasmalemma in the process. A thick
sheath is deposited between the plasma membranes
of the host and the pathogen (Fig. 23.6).
By the time the mycelium reaches the apical
meristem (about 40 55 days post infection),
the host has usually formed the inflorescence
initials, and massive proliferation of the mycelium
occurs from that stage onwards. The
developing spike tissue becomes filled with
hyphae which then branch profusely and form
teliospores. This infection sequence of a prolonged
symptomless colonization followed by
symptom development in the reproductive structures
of the host is typical of the small-grain
cereal smuts but differs from the infection of
maize by U. maydis (see below).
Ustilago avenae, U. nuda and U. tritici
These species cause loose smut of their cereal
hosts, i.e. the kernels are replaced by sori
producing teliospores, with entire glumes
usually destroyed. Ustilago avenae infects oats
(Fig. 23.7a) and false oat-grass, Arrhenatherum
elatius. There are numerous races which are
specific to different oat cultivars. The disease
cycle is complex. Teliospores have been shown to
survive for 13 years and thus the fungus can
infect seedlings from teliospores dusted onto the
outer surface of seeds. Additionally, it is capable
of limited systemic infection of the seed pericarp
which is initiated during flowering (Neergaard,
1977), and such infections are genuinely seedborne.
Either way, the fungus systemically
colonizes the growing host plant and proliferates
during flowering to produce a crop of teliospores.
Systemically infected hosts flower slightly
earlier than healthy plants, and they release
their teliospores at the time when healthy plants
flower. Teliospores released at that point can
germinate on healthy flowers (Mills, 1967),
leading to systemic infections which may be
carried over to the next growing season within
viable seeds.
Ustilago nuda and U. tritici cause loose smut on
barley and wheat, respectively (Fig. 23.7b). Their
disease cycles are very similar to each other.
Systemic infection of the host plant gives rise
to smutted heads and, as in the case of U. avenae,
flowering of smutted plants occurs slightly
earlier than that of healthy plants, so that the
disease can spread to uninfected flowers by
means of teliospores. The normal entry point of
dikaryotic mycelium was formerly thought to be
the stigma of healthy flowers, but Batts (1955)
showed that it is, in fact, the young tissue at
the base of the ovary. The mycelium survives
systemically in infected embryos. In spring,
systemic infections spread when these embryos
germinate. In contrast to U. avenae, teliospores of
U. nuda and U. tritici are short-lived, rarely surviving
for more than a few days under normal
conditions. Hence, infection from teliospore dust
on the surface of seeds does not seem to be an
important infection route.
23.2.5 Ustilago maydis
This species is the cause of corn smut and is by
far the most thoroughly researched member of
the Ustilaginomycetes (reviewed by Kahmann
et al., 2000). One of the early research highlights
using U. maydis was on mitotic recombination,
leading to the development of the ‘Holliday
model’ to explain the exchange of DNA strands