Introduction to Fungi, Third Edition

PUCCINIA GRAMINIS, THE CAUSE OF BLACK STEM RUST
621
54 genera, and this list is still expanding.
However, no single isolate of P. graminis is able
to infect all these host species. Instead, the
species P. graminis can be separated into several
specialized forms which have become adapted to
one or a few principal host species. These are
termed formae speciales (sing. forma specialis,
abbreviated as ‘f. sp.’) because they cannot be
distinguished reliably from each other on morphological
criteria. A morphologically distinct
form of the same species which can be clearly
identified by microscopy or other means would
be called varietas (abbreviated as ‘var.’).
The most important formae speciales are
P. graminis f. sp. tritici (on wheat), f. sp. avenae
(on oat) and f. sp. secalis (on rye). In addition, there
are several forms on wild grasses, e.g. f. sp. phleipratensis,
f. sp. lolii and f. sp. agrostidis (Wilson &
Henderson, 1966; Anikster, 1984). It is possible to
produce hybrids between some of these formae
speciales, e.g. between f. sp. tritici and f. sp. secalis
(Green, 1971). The hybrid aeciospores are not very
virulent on either principal host, and Green
(1971) has argued that the hybrids resemble a
more primitive form of Puccinia graminis with low
virulence and a wide host range, and that evolution
in stem rust of cereals is progressing from
low virulence and a wide host range to high
virulence and a narrowed host range.
Each forma specialis on cereals in turn forms
hundreds of races distinguished by the infection
responses of differential host cultivars, with
new races continually evolving (see p. 626). This
feature highlights the remarkable genetic and
physiological flexibility of rust fungi.
22.3.1 Puccinia graminis on barberry
The basidiospores are released in spring from
overwintered cereal stubble at about the time
when fresh barberry leaves unfold. Basidiospores
are able to germinate by repetition if they do not
land on a suitable host surface (Fig. 22.10e).
Infection gives rise to a haploid monokaryotic
mycelium which shows inter- and intra-cellular
growth and colonizes the host tissue extensively.
Generally, monokaryotic stages of rust fungi
show more widespread colonization of host
tissue than their dikaryotic counterparts.
Viewed from the surface, the colonized barberry
leaf area appears as a yellowish circular lesion.
On the upper surface of this lesion, several
flask-shaped spermogonia develop whose necks
protrude beyond the epidermal layer. Among
the orange-coloured tapering periphyses surrounding
the opening of each spermogonium
are several thinner, hyaline branched hyphae,
the flexuous (or receptive) hyphae. Lining the
inside surface of the spermogonium are tapering
annellides which give rise to small uninucleate
spermatia. These ooze out through the mouth
of the spermogonium and are held by the periphyses
in a drop of sticky sweet-smelling liquid
(Figs. 22.8a, 22.9a). Within the mesophyll of the
barberry leaf, the haploid mycelium gives rise
to several spherical structures called proto-aecia.
These are mostly made up of large-celled pseudoparenchyma,
but in the upper region is a cap
of smaller, denser cells (Fig. 22.9b).
Single haploid lesions are incapable of
further development unless cross-fertilization
occurs. The sweet-smelling spermatial exudate
contains fructose and several volatile substances
(see p. 629) which attract insects feeding on the
nectar and carrying the spermatia around by
visiting several distinct pustules. The haploid
pustules are of either of the two mating types,
(þ) or( ), and if a (þ) spermatium is brought
close to a flexuous hypha of opposite mating
type, it produces a short germ tube which
anastomoses with the flexuous hypha (Craigie,
1927; Buller, 1950). Nuclear transfer is followed
by repeated division and migration of the
introduced nucleus towards the proto-aecium
(Craigie & Green, 1962). This results in the
dikaryotization of the haploid mycelium until
binucleate cells become visible in the cap region
of the proto-aecium after about 3 days. The
binucleate cells now start to give rise to chains
of alternating long and short cells which are also
binucleate. The longer cells enlarge and become
aeciospores, but the shorter cells disintegrate as
the spore chains develop (Fig. 22.9c). During the
development of the spore chains, the large
pseudoparenchymatous cells of the protoaecium
are also crushed and pushed aside.
Surrounding the chains of spores is a specially
differentiated layer of cells homologous with the