Whenever a fungus invades an area of natural veget-
ation it is likely that the fungus has been introduced
from elsewhere, because plants in natural communities
co-evolve with the resident pathogens.
Biotrophic plant pathogens
Biotrophic plant pathogens are characterized by the fact
that they have an extended nutritional relationship
with living host cells, in contrast to necrotrophic
pathogens which kill the plant tissues. The success of
this type of parasitism depends on two essential features:
(i) the ability to avoid eliciting host cell death and
(ii) a means of securing a continuous nutrient supply
from the living host tissues. Thus, biotrophs are in many
ways the epitome of successful parasites – they feed from
the host cells without killing them.
There are many types of biotrophic fungus and
fungus-like organisms, because this mode of parasit-
ism has evolved independently on several occasions.
The major groups of biotrophs include the rust
fungi(Basidiomycota), the powdery mildew fungi
(Ascomycota), the downy mildews (Oomycota), and
the intracellular plasmodiophorids(protists of uncer-
tain taxonomic affinity, but clearly distinct from
fungi). In addition to these, the endophytic fungi
grow essentially as biotrophs. A classic example is the
fungus Fulvia(Cladosporium)fulvumwhich causes blue
mould disease of tomato plants. Unlike the ubiquitous
Cladosporiumspp. that grow as epiphytes on leaves
(Chapter 11), F. fulvumenters the host stomata from
a germinating spore and forms an extensive intercel-
lular network in the leaf, before emerging from the
stomata as conidiophores which release further spores.
It has no obvious means of feeding from the living host
cells except by scavenging leachates; but it might
enhance the rate of leakage and also use some of the
cell wall polymers. A strain of F. fulvumcan only feed
from the host if it avoids inducing a hypersensitive
response, and this is governed by “avirulence” genes
of the pathogen and corresponding resistance genes
in the host. This gene-for-gene relationshipwith the
host plant (Honee et al. 1994) is commonly found in
biotrophic plant pathogens, and is discussed later.
In the following sections we consider several ex-
amples of biotrophic plant pathogens.
Haustorial biotrophs
Many biotrophic fungi initiate infection from spores
that land on the host surface and then germinate and
enter through the stomata. The initial events involve
the precise orientation of germ-tube growth, using
cues such as plant surface topography and nutrient gra-
dients, discussed in Chapter 5. The hyphae then grow
between the host cells, and attach to individual cells
by producing a haustorial mother cell. From this, a
narrow penetration hypha grows through the host cell
wall but it does not penetrate the membrane. Instead,
the host cell membrane invaginates to accommodate
the invading fungus, which develops into a haustorium
that is always separated from the host cytoplasm by
an extrahaustorial membrane(see Fig. 5.7).
As shown in Fig. 14.21, the mature haustorium is sur-
rounded by a fluid matrix, and there is a tight “seal”
in the neck region to prevent the fluid from escaping.
One of the consequences of this in experimental
work is that the whole haustorial complex (envelop-
ing membrane, fluid matrix, and the haustorium itself )
can be isolated by digesting the host cell wall with
enzymes. From studies on these isolated haustorial
complexes of rust and powdery mildew fungi it has been
shown that the extrahaustorial membrane allows the
free passage of sugars and amino acids. The wall and
membrane of the plant cell can also be expected to allow
the passage of nutrients through appropriate membrane
transporters. So, the crucial interface for nutrient
uptake by the fungus is likely to be the haustorial mem-
brane (Fig. 14.21).
In a model proposed by Voegele & Mendgen (2003),
sugars and amino acids are believed to be taken
into the haustorium in association with H+ions by
membrane symporters, using the proton motive force
generated by ATPase. The sugars are then used for
biosynthetic reactions within the haustorium. Fructose
(derived by hydrolysis of sucrose to glucose and fructose
in the extrahaustorial matrix) is converted to mannitol,
which is translocated into the fungal hyphae and ultim-
ately into the developing spores. The net result is that
nutrients are continuously withdrawn from the living
plant cells, to support repeated cycles of sporulation on
the host surface. Much of the economic importance
of rust and powdery mildew fungi stems from this
continuous withdrawal of nutrientsfrom the plant
to support sporulation of the fungus.Rust fungiRust fungi gain their name from the distinctive rust-
colored spores, termed uredospores, which are produced
in abundance for dispersal during the summer months.
Over 4000 rust species have been described on crop or
wild plants. Many rust fungi need two separate hosts
to complete their life cycle. For example, Puccinia
graminis(black stem rust of wheat) requires both a cereal
and an alternate host (barberry). But other rust fungi,
such as mint rust (Puccinia menthae), complete their life
cycle on a single host. Below, we will consider the
life cycle of P. graminisbecause it is one of the most