Download BOTANICAL BRIEFING. Signalling between Pathogenic Rust Fungi

Annals of Botany 80 : 713–720, 1997
BOTANICAL BRIEFING
Signalling between Pathogenic Rust Fungi and Resistant or
Susceptible Host Plants
M I C H E L E C. H E A T H
Botany Department, UniŠersity of Toronto, Toronto, Ontario, Canada M5S 1A1
Received : 22 May 1997
Returned for revision : 29 June 1997
Accepted : 27 July 1997
Rust fungi are obligately biotrophic plant parasites that obtain their nutrients from living host cells. The initiation
of the two parasitic phases of these fungi generally requires topographic signals from the plant surface followed, for
the dikaryotic phase, by a successive sequence of signals to control further fungal development within the plant.
During the fungal life cycle, three types of intracellular structures (invasion hyphae, M-, and D-haustoria) are formed
and each may differently affect the host membrane that surrounds it, as well as affecting other cellular components.
Each intracellular structure also prevents non-specific plant defences triggered by fungal activities, possibly by
interfering with the signalling system rather than defence expression. In resistant host cultivars, cellular invasion
triggers a rapid cell death (the hypersensitive response) that shares some features with developmentally programmed
cell death in animal and plant tissues, and is controlled by parasite-specific resistance genes that resemble those that
defend plants against other types of pathogens. Evidence from one system suggests that this response is specifically
elicited by a fungal peptide and does not involve the oxidative burst typical of resistance expression in other plantpathogen interactions. However, overall, few of the molecules involved in any of these plant-rust fungi interactions
have been completely characterized and much is left to be discovered, particularly with respect to how cellular
susceptibility to rust fungi is conditioned.
# 1997 Annals of Botany Company
Key words : Apoptosis, biotrophy, elicitor, hypersensitive response, oxidative burst, suppressor, Uromyces Šignae.
INTRODUCTION
Despite their role as major food sources for microbes when
they are dead, plants are food for relatively few microorganisms when they are alive. This observation implies
that living plants have antimicrobial features that dead cells
lack, a conclusion supported by recent revelations of the
huge variety of potentially defensive responses that can be
triggered in plants by microbes, their products, and other
stresses (for references see Heath, 1996). Therefore, successful parasites must find ways of coping with these
responses. Most commonly, fungal pathogens employ a
combination of strategies, such as killing cells quickly to
reduce the degree to which defences can be induced, and
possessing attributes (such as enzymes that detoxify antimicrobial compounds) that mitigate the effects of those
defence responses that take place. However, a few pathogenic fungi are biotrophs, feeding off living plant cells and
apparently negating, or not triggering, any obvious adverse
plant response. The advantage of this type of parasitism is
the almost limitless access, through altered plant translocation patterns, to the plant’s nutrients (Lewis, 1973).
However, current evidence suggests that biotrophy requires
an impressive degree of cellular interaction between plant
and parasite, perhaps explaining why so few fungal
pathogens exploit this type of parasitism. Some of the beststudied pathogenic fungal biotrophs belong to the group of
obligate parasites known as the rust fungi (division
Basidiomycota, order Uredinales) and this review will
0305-7364}97}060713­08 $25.00}0
summarize the current state of knowledge of inter-organismal signalling that takes place in rust-infected host plants.
Because the exact molecular interactions are generally
unknown, ‘ signalling ’ is defined fairly loosely as any activity
of one organism that results in a response of the other. A
comparison of rust fungi with other biotrophs can be found
in Heath and Skalamera (1997).
SIGNALLING PRIOR TO CELL
PENETRATION
Rust fungi are generally foliar pathogens with a complex
life cycle that involves two parasitic stages, dikaryotic and
monokaryotic. To initiate the dikaryotic stage, the urediospore germ tube of many rust fungi responds to topographical features of the leaf surface (Read et al., 1992) so that it
grows towards a stoma and recognizes its presence by
responding to the ridges around the stomatal lips (Terhune
et al., 1991). Adhesion to the leaf surface is mandatory for
this contact-sensing (Read et al., 1992), but how the signal
is perceived and transduced is still poorly understood. So
far, there is evidence for the involvement of stretch-activated
calcium channels in the fungal plasma membrane (Zhou et
al., 1991), integrin-mediated signalling across this membrane
(Corre# a, Staples and Hoch, 1996), and alterations to the
fungal cytoskeleton (Read et al., 1992). In response to the
stomatal lips, the fungus sequentially forms an appressorium
over the stomatal opening, an infection peg that grows
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# 1997 Annals of Botany Company
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Heath—Plant-fungal Signalling in Rust Infections
F. 1. Diagrammatic representation of the fungal and plant signals that are involved in the early development of the dikaryotic stage of a rust
fungus, from the germination of the urediospore to the formation of the first haustorium (adapted from Heath, 1995).
between the guard cells, a spherical substomatal vesicle in
the substomatal space, and an infection hypha that grows
intercellularly between mesophyll cells (Fig. 1). This
morphological differentiation is accompanied by changes in
fungal wall composition (Littlefield and Heath, 1979 ;
Kaminskyj and Heath, 1983), the induction of mitosis,
changes in protein synthesis (Staples and Macko, 1984), the
initiation of ribosome synthesis (Heath and Heath, 1978),
and the secretion of a variety of hydrolases (Mendgen,
Hahn and Deising, 1996). Without differentiation, the germ
tube continues to grow on the leaf surface until its
endogenous reserves are depleted and it dies. On non-host
plants with surface topographies that differ significantly
from that of the host leaf, germ tubes commonly make
‘ mistakes ’ in locating or recognizing stomata, considerably
reducing the number of fungal individuals that enter the
plant (Heath, 1977).
During the other, monokaryotic, parasitic stage, rust
fungi usually penetrate directly into epidermal cells and the
only pre-penetration infection structure is the appressorium
produced by the basidiospore germ tube (Fig. 2). Little is
known about the signals required for appressorium formation, but surface hardness is important (Freytag et al.,
1988). It seems, therefore, that basidiospore germ tubes, like
urediospore germ tubes, require signals from the plant
surface to trigger the formation of structures necessary for
further pathogenic development.
In resistant or susceptible cultivars of host species, the
infection hypha formed during the initiation of the
dikaryotic phase grows between mesophyll cells, often
without any obvious response of the plant. Yet the same
rust fungus will elicit a variety of defensive responses (such
as the deposition of silica, callose, or phenolic materials on
and in the plant wall) when it forms an infection hypha
within non-host species. These responses are the same
(although sometimes lower in intensity) to those elicited in
the same plant by incompatible, non-biotrophic, microbes
(Fernandez and Heath, 1989 ; Fink et al., 1991). It seems,
therefore, that intercellular hyphae of rust fungi do not fail
to trigger defences in host plant cells because they lack
Heath—Plant-fungal Signalling in Rust Infections
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F. 2. Diagrammatic representation of the events that take place during the entry of Uromyces Šignae into a cowpea epidermal cell during the
development of the monokaryotic stage of the fungus from a germinating basidiospore (b). A, Events in both resistant and susceptible host
cultivars that accompany the sequential formation, from the fungal appressorium (a), of a penetration peg in the plant wall and a spherical
intraepidermal vesicle (v) within the cell. B, Subsequent events seen in susceptible cultivars prior to the fungal invasion hypha (h) growing into
neighbouring epidermal cells and into the underlying intercellular space of the leaf. C, Cytologically-recognizable events (except for proteinase
activity, identified by inhibitor studies) seen in a resistant cultivar ‘ Dixie Cream ’ that exhibits a hypersensitive response. Current evidence suggests
that the listed events occur sequentially, proceeding clockwise from the increase in cytosolic calcium levels, although the relative timing of the
initiation of protease activity and microtubule disappearance is not certain. Protoplast consistency refers to changes to and from a gel-like state.
eliciting molecules or activities. Nevertheless, in contrast to
the high frequency with which non-specific elicitors (i.e.
active in a variety of host or non-host plants) of plant
defences have been isolated from non-biotrophic fungi,
relatively few have been extracted from rust fungi. Fungal
wall components, expecially chitin, commonly act as nonspecific elicitors (e.g. Bohland et al., 1997), yet exudates and
wall fragments of chitin-containing infection hyphae of the
cowpea rust fungus, Uromyces Šignae, were found not to
mimic the fungus in its ability to trigger silica deposition in
non-host bean leaves (Ryerson and Heath, 1992). However,
wall components of germ tubes of the wheat stem rust
fungus, Puccinia graminis f.sp. tritici, and apoplastic fluids
from rust-infected, susceptible, wheat leaves will trigger
lignification in wheat genotypes with chromosome 5A
(irrespective of their susceptibility to the fungus) (Sutherland
et al. 1989 ; Beissmann et al., 1992). This Puccinia elicitor
also stimulates lipoxygenase activity in wheat, apparently
by a different signalling pathway than chitin oligosaccharides (Bohland et al., 1997).
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Heath—Plant-fungal Signalling in Rust Infections
If infection hyphae of rust fungi produce non-specific
elicitors of plant defences, then each rust fungus must
suppress such responses in its host species. Suggested
candidates for these ‘ suppressors ’ have been surface
carbohydrates (Mendgen et al., 1988) or suppressor-active
substances found in intercellular washing fluids (IWFs)
from rust-infected plants (Li and Heath, 1990 ; Beissmann
and Kogel, 1992). However, the biological significance of
these latter suppressors is uncertain as they many not show
the same plant species specificity as the fungus (Li and
Heath, 1990 ; Fernandez and Heath, 1991).
In the dikaryotic parasitic stage, the fungus forms an
intercellular mycelium from which intracellular haustoria
are formed (Fig. 1). These haustoria are generally considered
to be feeding structures and they develop from haustorial
mother cells (HMCs) that adhere to the plant cell surface.
For some rust fungal species, an unknown signal on this
surface may be necessary for HMC induction (Mendgen,
1982 ; Read et al., 1992). Studies with the cowpea rust
fungus, Uromyces Šignae, suggest that the first-formed
HMC is programmed to die unless a ‘ survival signal ’ is
received from the plant at the time the HMC produces a
penetration peg (Heath and Perumalla, 1988). The ability of
sugar mixtures to prevent HMC senescence and allow
haustorium formation in Šitro, if applied during penetration
peg development (Heath, 1990), implies that the survival
signal may be released as the penetration peg digests its way
through the plant cell wall ; however, the exact in planta
signal has yet to be identified.
In summary, the data show that for the dikaryotic,
parasitic phase of a typical rust fungus, a successive sequence
of plant signals are required to control fungal development
from the time the urediospore germinates on the leaf surface
to when the fungus penetrates its first plant cell within the
leaf (Heath, 1995). These early stages of intercellular growth
are associated with fungal activities or products that trigger
defence responses in surrounding cells of non-host plant
species. However, these defences seem to be prevented in
host species by mechanisms that have yet to be elucidated.
SIGNALLING DURING INTRACELLULAR
GROWTH IN SUSCEPTIBLE PLANTS
Strictly speaking, intracellular structures produced by
biotrophic fungi are not completely intracellular as they are
always surrounded by a continuation of the plant plasma
membrane. Inexplicably, the haustoria produced by the two
parasitic stages of rust fungi are radically different, even for
autoecious rust fungi that produce the two stages in the
same plant species (Littlefield and Heath, 1979 ; Heath and
Skalamera, 1997). M-haustoria produced by the monokaryotic stage seem to be barely modified hyphae ; in contrast,
not only are D-haustoria formed from HMCs that show
complex, unique, cellular development (Heath and Heath,
1975 ; Harder and Chong, 1991), but the tubular neck has a
different wall composition to the larger, terminal, body
(Harder and Chong, 1991). D-haustoria show specific gene
expression (Hahn and Mendgen, 1997) and around the Dhaustorial neck is an iron- and phosphorus-rich neckband
which bridges the fungal and plant plasma membranes and
forms a seal to apoplastic flow of solutes along the junction
between the two organisms (Heath, 1976 ; Heath and Allen,
1985 ; Harder and Chong, 1991). Functionally, the neckband
is analogous to the Casparian strip in plant roots and the
tight junction in multicellular animals, but it is unique
because of the inter-organismal co-operation that must be
required for its formation. Whether the haustorium requires
any plant signals during its development is unknown, but
the fact that haustoria formed in Šitro do not mature
(Heath, 1989) suggests that such signals might exist.
Because the formation of the monokaryotic stage of a rust
fungus often involves direct penetration into an epidermal
cell (prior to forming a haustorium-bearing intercellular
mycelium), rust fungi can form three types of intracellular
structures during their life cycle : the invasion hypha
[consisting of a spherical intraepidermal vesicle from which
the primary hyphae grow (Fig. 2)] and the M- and Dhaustoria. For all three, plant plasma membrane is
synthesized to accommodate the growing fungus, probably
as an inadvertent response to the pressure exerted by the
fungus, although a fungal signal could conceivably be
involved. Cytochemical staining suggests that the extrahaustorial membrane around both M- and D- haustoria is
differentiated from the rest of the plant plasma membrane
and often lacks ATPase activity (Heath and Skalamera,
1997) ; the membrane around the invasion hypha has not
been investigated. For D-haustoria, this lack of ATPase
activity could be related to the apparent lack of large
protein complexes in the extrahaustorial membrane as
revealed by electron microscopy after freeze-fracture (Littlefield and Bracker, 1972). Interestingly, the pattern of callose
deposition after the fungus senesces or is killed indicates
that this membrane also lacks callose synthase activity,
whereas the plant membrane surrounding M-haustoria and
invasion hyphae does not (Stark-Urnau and Mendgen,
1995 ; Skalamera, Jibodh and Heath, 1997). These observations are consistent with either the plant membrane
surrounding different intracellular fungal structures having
different origins, or the neckband around the D-haustorium
preventing the diffusion of integral membrane proteins into
the extrahaustorial membrane from other regions of the
plant plasma membrane. In either case, it seems that
different intracellular structures of the same rust fungus
have different effects on the plant in terms of the properties
of the plant plasma membrane that surrounds them.
Not only is the plant plasma membrane affected in rustinvaded cells, but so too are other cellular components.
Nitroblue tetrazolium staining has shown that there is a
transient increase in electron-generating activity within
plant mitochondria nearest to the fungus when cells are
entered by invasion hyphae, M-haustoria, or D-haustoria of
U. Šignae (Heath, unpubl. res.), possibly related to the
transient increase in glutamate dehydrogenase activity
reported for flax cotyledons infected with Melampsora lini
(Sadler and Shaw, 1979). Electron microscopy has revealed
rearrangements of the plant’s cellular components, the most
ubiquitous of which are the accumulation of endoplasmic
reticulum adjacent to the fungus (Heath and Skalamera,
1997), often in a fungus-specific manner (Harder and
Chong, 1991). Another universal response is the association
Heath—Plant-fungal Signalling in Rust Infections
of the plant nucleus with the fungus once the latter is well
established within the plant cell (Heath and Skalamera,
1997). For cowpea epidermal cells containing invasion
hyphae of U. Šignae, this latter association and early fungal
growth are not accompanied by gross rearrangements of the
cytoskeleton other than a disappearance of cortical microtubules around the penetration site (Skalamera and Heath,
unpubl. res.), and are unaffected by inhibitors of transcription or translation (Heath, Nimchuk and Xu, 1997).
This last observation raises the question of the functional
significance of the nucleus-fungal association (Heath and
Skalamera, 1997). Contrast-enhanced video microscopy of
early stages of infection by basidiosporelings into living cells
has revealed that the plant nucleus first migrates to the
fungus as the fungal penetration peg grows through the
epidermal cell wall. This migration is apparently triggered
by plant wall components released by enzyme digestion and
is calcium- and protein kinase-dependent (Heath et al.,
1997), as are biochemical defences triggered in other systems
by cell wall degradation products (Ebel and Cosio, 1994). If
the nucleus remains at the penetration site during the entry
of the fungus into the cell lumen, fungal growth ceases
following the encasement of the penetration peg in callose (a
glucan containing β-1,3-linkages). Callose deposition commonly requires calcium influx into the cell (Kauss, Waldmann and Quader, 1990) and is a normal plant response to
physical and chemical perturbations (Russo and Bushnell,
1989). Therefore, it seems likely that both nuclear migration
and callose deposition are part of a non-specific response of
the plant cell to localized wall damage, perhaps involving
the same signal transduction pathway. Nevertheless, in
most epidermal cells in both resistant and susceptible
cowpea cultivars, a callose papilla, or any other sign of a
defensive cellular response, is not seen during the first few
hours of fungal growth within the cell. Instead, the plant
nucleus leaves the penetration site at the time that the fungal
penetration peg touches the plant plasma membrane and
does not return until the fungus ceases its originally spherical
growth and establishes a hyphal tip. Observations of fixed
tissue suggest that this sequence of events also occurs during
formation of M- and D-haustoria in mesophyll cells (Heath
et al., 1997).
The inference from these, and a variety of other
observations is that, like intercellular infection hyphae,
intracellular invasion hyphae and M- or D- haustoria of
rust fungi can interfere with the plant defences that might be
expected to be triggered by fungal penetration (Heath and
Skalamera, 1997). As discussed later, one of these defences
may be cell death, which would be particularly detrimental
to a biotrophic pathogen. Significantly, the lack of callose
deposition in association with the nucleus moving away
from the penetration site in cowpea epidermal cells suggests
that, rather than directly inhibiting these plant defences, the
penetrating fungus interferes with the signalling system that
would normally trigger them. A precedent for such a
phenomenon is set by the non-biotroph, Mycosphaerella
pinodes, which apparently suppresses defence responses in
its host plant, pea, by secreting glycopeptides that inhibit
ATPase activity and a polyphosphoinositol-dependent
signal cascade (Shiraishi et al., 1994).
717
Once the fungus has prevented defence responses associated with the penetration process and is inside the cell, it
is possible that it avoids further ‘ irritation ’ of its host by
lacking activities or features that might otherwise trigger a
plant reaction. This might explain, for example, why walls
of young D-haustoria lack chitin (Harder and Chong,
1991), which is a potent defence elicitor in some plants.
However, walls of M-haustoria contain chitin (Harder and
Chong, 1991), so if the avoidance hypothesis has any
validity, this chitin must be masked by other wall components.
In summary, intracellular invasion hyphae and haustoria
of rust fungi have profound effects on the cellular structure
and activity of invaded plant cells. Some of these effects are
specific for a particular type of intracellular structure but
many are not. Presumably, some of them relate to the
acquisition of nutrients from the plant cell (Spencer-Phillips
and Gay, 1981), but others must be involved in preventing
the defence responses that the physical and chemical
activities of the fungus ought to elicit. The fungal molecules
or features that control these effects are totally unknown.
SIGNALLING DURING INTRACELLULAR
GROWTH IN RESISTANT HOST PLANTS
The most common response of resistant plants to cellular
invasion by biotrophic or non-biotrophic fungal pathogens
is rapid cell death. In resistant cultivars of a host plant, this
‘ hypersensitive response ’ (HR) may be conditioned by
parasite-specific resistance genes but it also occurs following
penetration of cells of non-host species in which such genes
may be absent (Heath, 1996). The HR is an effective defence
mechanism against biotrophs and non-biotrophs alike
because of the accompanying upregulation of a multitude of
‘ defence ’ genes that produce a highly antimicrobial
environment in and around the dead cell (Goodman and
Novacky, 1994 ; Levine et al., 1994). The ubiquity of this
response suggests that it may be a form of programmed cell
death (pcd) (Heath and Skalamera, 1997), and in host
resistance to U. Šignae, it is accompanied by the cleavage of
plant DNA into internucleosomal fragments (Ryerson and
Heath, 1996), a hallmark of a form of pcd in animals known
as apoptosis (Earnshaw, 1995). The rapidly increasing
number of reports of such fragmentation during developmentally-regulated cell death in plants (e.g. Orzaez and
Granell, 1997) raises the possibility that the HR is
mechanistically related to other forms of plant pcd.
However, the unique antimicrobial features of the HR
suggest that it may represent a special type of pcd evolved
specifically as a defence against microbial attack (Ryerson
and Heath, 1996).
If the HR is a form of pcd rather than the direct effect of
a fungal toxin, then the fact that biotrophs can trigger this
response upon invasion of non-host cells (e.g. Heath, 1984 ;
Meyer and Heath, 1988) indicates that biotrophs do not
lack HR-inducing features. The HR, therefore, has to be
one of the most important plant defences for a biotrophic
rust fungus to negate in its host species. Rust fungi may
possibly resemble animal viruses which produce gene
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Heath—Plant-fungal Signalling in Rust Infections
products that specifically prevent pcd during pathogenesis
(Hale et al., 1996). If this is the case, then the HR seen in
resistant cultivars of host species must result either from the
failure of this HR-prevention process, or by the specific
elicitation of the HR by an additional fungal signal.
The HR induced in non-host or host plants by non-rust
fungi has been suggested to be triggered by an oxidative
burst that releases active oxygen species (AOS) as a
consequence of recognition by the plant of a fungal elicitor
(Levine et al., 1994). In the case of host plant resistance to
biotrophic fungal pathogens, which generally exhibit ‘ genefor-gene ’ relationships, elicitors would be expected to be the
direct or indirect products of fungal avirulence genes that
interact with the products of ‘ matching ’ resistance genes in
the plant. In cultured tomato cells, the peptide avirulence
gene product from the intercellular, non-rust biotroph,
Cladosporium fulŠum, causes an oxidative burst associated
with G-protein-mediated increases in the activities of plasma
membrane ATPase, calcium channels and NADPH oxidase
(Ti, Higgins and Blumwald, 1997). However, although
scavengers of AOS can prevent the cell browning and
autofluorescence associated with the HR in rust-infected
cowpea epidermal cells (Chen and Heath, 1994), these and
other scavengers do not prevent the plant cells from dying
and there are no cytologically detectable signs of an oxidative
burst (Heath, unpubl. res.). These data are consistent with
the conclusion, discussed earlier, that the rust fungus ‘ turns
off ’ adverse responses, including the HR, that are elicited
non-specifically by fungal activities during the penetration
of both resistant and susceptible host cells. They also
suggest avirulence gene products of rust fungi might be
expected to subsequently elicit the HR by a different
mechanism to those of C. fulŠum. Small peptides that elicit
cell death only in rust-resistant cowpea cultivars have been
found in exudates of basidiospore germlings of U. Šignae
after they have formed an appressorium, and can be isolated
from IWFs from susceptible cowpea plants infected with the
monokaryotic stage of the fungus (D’Silva and Heath,
1997). However, they are not found in IWFs from leaves
containing the dikaryotic stage of the fungus, suggesting
that they may be restricted to the D-haustorium at this stage
and are prevented from reaching the apoplast by the
haustorial neckband (Chen and Heath, 1992).
The recent cloning of rust-resistance genes in flax
(Anderson et al., 1997) and, possibly, wheat (Feuillet,
Schachermayr and Keller, 1997) will hopefully lead to
elucidation of how rust fungal elicitors trigger the HR.
These rust-resistance genes share common features with
plant resistance genes against other types of pathogens and
seem to code for components of signal transduction
pathways (Lamb, 1996). Assuming that the signal transduction pathway leading to the HR in different systems shares
some common features, it is possible that different fungal
elicitors interact with the pathway at different points.
The cellular changes that accompany the HR triggered by
rust fungi have been most comprehensively studied in
epidermal cells of resistant cowpea cultivar, Dixie Cream,
responding to invasion hyphae of U. Šignae. As illustrated
in Fig. 2 C, among the earliest signs of the HR are a rise in
cytoplasmic calcium levels (Xu and Heath, unpubl. res.), a
change in appearance of the plant nucleus (preceding DNA
cleavage) (Heath et al., 1997), the cessation of cytoplasmic
streaming (Heath et al., 1997), and the disappearance of
microtubules (Skalamera and Heath, unpubl. res.). The loss
of microtubules has also been seen in resistant mesophyll
cells containing D-haustoria of the flax rust fungus
(Kobayashi, Kobayashi and Hardham, 1994). In cowpea,
the HR also can be delayed by protease inhibitors (Heath,
unpubl. res.), suggesting that as in animal apoptosis (Hale et
al., 1996) and other forms of plant pcd (Beers and Freeman,
1997), protease activity plays a role in the execution phase
of cell death. However, how this series of events are set in
motion by the fungal elicitor, and which play primary roles,
are unknown.
The absence of a HR in some rust-resistant host plants
raises the question of whether the HR is only one of several
consequences of the interactions between avirulence and
resistance gene products. For example, in a predominantly
non-HR resistant cowpea cultivar, the plant plasma membrane around D-haustoria of U. Šignae appears abnormal
(Heath and Heath, 1971) and all intracellular fungal
structures are rapidly encased in callose (Heath and Heath,
1971 ; Skalamera and Heath 1996 ; Skalamera et al., 1997).
Unexpectedly, this callose deposition is prevented by antimicrofilament agents and protein glycosylation inhibitors
that have no effect on the deposition of wound-induced
callose, or on the rare example of fungal-penetrationinduced callose in susceptible plants (Skalamera and Heath,
1996 ; Skalamera et al., 1997). One interpretation of these
data is that protein glycosylation and the actin cytoskeleton
are involved in the recognition and}or transduction of the
fungal elicitor that triggers resistance in this cowpea cultivar.
However, although the HR in other rust-resistant cultivars
is delayed by antimicrofilament agents, protein glycosylation
inhibitors do not inhibit this response in these cultivars, or
in the callose-forming cultivar on the rare occasion that a
HR occurs. These observations raise the interesting questions of whether the HR and callose formation in the latter
cultivar are triggered independently, and how both are
controlled by the single resistance gene present in this
cultivar (Heath, 1994).
CONCLUSIONS
Although the exact nature of the interactions are generally
unknown, it is obvious that the interactions between rust
fungi and their host plants are enormously sophisticated
and complex. The signals involved in these interactions have
been best recognized for the dikaryotic, parasitic phase of
these fungi (Fig. 1) although few have been completely
characterized. For the monokaryotic, parasitic phase,
information is still primarily descriptive (Fig. 2), but this
phase holds the promise of being more amenable to future
study because of the undifferentiated nature of the fungal
thallus (implying that signals and activities may not be
restricted to specific fungal structures such as haustoria),
and because invasion hyphae may be studied directly in
living epidermal cells. To date, most studies have centred on
disease resistance. However, given that defence responses,
Heath—Plant-fungal Signalling in Rust Infections
and in particular the hypersensitive response, may be the
‘ default state ’ of plant cells to fungal invasion, the unique
and more interesting plant-rust fungi interactions may be
those that keep the invaded cell alive and condition
susceptibility ; of these interactions we are almost completely
ignorant.
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