Introduction to Fungi, Third Edition

UREDINALES: THE RUST FUNGI
619
formation of the first haustorium (Heath, 1982,
2002). Either way, the hypersensitive response
triggers biochemical events involved in local and
systemic defence against the pathogen (Heath,
2000). One point of difference between penetration
by rust fungi and powdery mildews is that
the host plant mounts some resistance response
against the latter even if the interaction ultimately
turns out to be compatible, whereas no
such recognition occurs if a compatible rust
germ tube penetrates (Heath, 2002). The ultrastructural
consequence is that powdery mildew
haustoria commonly have a callose ring around
their neck, whereas this is absent or reduced in
the case of rust haustoria (Heath & Skalamera,
1997).
The gene-for-gene concept was proposed to
explain the specific interactions between the
rust Melampsora lini and its host, Linum usitatissimum
(flax). It postulates that for every resistance
gene of the host plant there is a matching
virulence gene in the pathogen (see Flor, 1971).
Resistance is usually dominant (R) whereas
virulence is recessive (a). An incompatible interaction
results if a rust fungus with an avirulence
allele (A) attempts to infect a host carrying the
matching resistance (R) allele. The identity of
most molecules interacting in recognition is
still unknown. However, Catanzariti et al. (2006)
have demonstrated that the protein products of
several avirulence genes are secreted by developing
haustoria of M. lini, and that these seem to
enter the cytoplasm of infected host cells where
recognition leading to hypersensitivity occurs.
The localization of proteins of haustorial origin
in host cells, including the host nucleus, was also
demonstrated by Kemen et al. (2005) for Uromyces
spp. on broad bean (Vicia faba). These authors
suggested that fungal avirulence genes might
encode transcription factors involved in manipulating
the host’s metabolism during the
biotrophic interaction. In this theory, avirulence
would result if the host cell managed to detect
the fungal transcription factor as foreign. It is
not yet known how the avirulence proteins are
translocated into the plant cell. The molecular
basis of gene-for-gene interactions involving
rust fungi is therefore fundamentally
different from that, for example, in
Cladosporium fulvum infecting tomato, where
recognition events occur at the host plasma
membrane (see p. 482).
Rusts, like most other fungi, possess an
uncanny ability to overcome major gene resistance
based on gene-for-gene interactions, especially
if a single resistance gene is involved.
Genetic variation is enhanced by the ability to
reproduce sexually in the field if the alternate
host is available. Even in the absence of the
alternate host, however, rust fungi can still
undergo genetic recombination by anastomosis
and nuclear exchange in various other ways (see
p. 625). Different races of a given pathogen can
be distinguished by their ability to infect any
host in a set of cultivars containing defined
resistance genes alone or in combination. Such
tests are routinely employed by plant pathologists
for the identification of races, and for
monitoring their spread (see p. 626).
Major gene resistance against rust fungi was
recognized early in the twentieth century by
Biffen (1905) and others, and extensive breeding
programmes were initiated. Typically a new
cultivar produces excellent results for a few
cropping seasons until resistant races develop
and spread in the field, thereby rendering the
breeders’ efforts futile. This is the ‘boom-andbust’
cycle. The ‘bust’ of a cultivar can be delayed
if it contains a ‘pyramid’ of several resistance
genes which the pathogen may be unable to
overcome. Sometimes the breeding for resistance
against one pathogen can lead to susceptibility
to another, as in the case of the Victoria oat
cultivar which showed good resistance against
P. coronata f. sp. avenae but was devastated by
Cochliobolus victoriae (see p. 471). In addition
to major gene resistance which is commonly
associated with the hypersensitive response,
there are other types of resistance. Some plant
genes do not afford total resistance but give
a moderate degree of resistance. If a combination
of several genes is involved, the resistance
may well be more durable in the field than
single-gene resistance. An example of such ‘field’
or ‘partial’ resistance is the reduced formation
of appressoria over stomata of grasses covered
by a particularly thick wax layer, which seems
to mask the topographic features of the