Download Defence signalling pathways in cereals Pietro Piffanelli

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Defence signalling pathways in cereals
Pietro Piffanelli, Alessandra Devoto and Paul Schulze-Lefert*
The combination of mutational and molecular studies has shed
light on the role of reactive oxygen intermediates and
programmed cell death in cereal disease resistance
mechanisms. Rice Rac1 and barley Rar1 represent conserved
disease resistance signalling genes, which may have related
functions in animals. The analysis of non-pathogenic
Magnaporthe grisea mutants may provide novel tools to study
host defence pathways.
Addresses
The Sainsbury Laboratory, John Innes Centre, Colney Lane, Norwich
NR4 7UH, UK
*e-mail: [email protected]
Current Opinion in Plant Biology 1999, 2:295–300
http://biomednet.com/elecref/1369526600200295
© Elsevier Science Ltd ISSN 1369-5266
Abbreviations
7TM
seven transmembrane
CHORD cysteine- and histidine-rich domain
GPCR
G-protein-coupled receptor
HR
hypersensitive response
PCD
programmed cell death
R gene
resistance gene
REMI
restriction enzyme mediated integration
ROI
reactive oxygen intermediates
Introduction
Despite the flurry of molecularly isolated plant resistance
genes in dicot species [1–4], only fragmentary experimental
data are available on resistance signalling pathways and
even less is known about defence mechanisms. Little of the
information derived from dicot species has been used so far
to understand the molecular bases of attack and defence in
cereal plant–pathogen interactions. Instead, advances in
map-based cloning technologies [5–8] and transgene
expression in cereals, both transient and stable [9–11], have
made even complex monocot genomes amenable to molecular analysis. This has complemented the more traditional
tools of Mendelian genetics and mutational studies.
In this review we discuss some of the recent developments
aimed at the genetic and molecular dissection of both
pathogen and host signal transduction pathways in cereals.
They reflect the variety and complexity of attack and
defence strategies in monocot species and unveil novel
insights into the interplay of resistance and cell death control.
Attack, defence, and counter-defence: lessons
from fungal pathogenicity mutants
Unlike phytopathogenic bacteria, biotrophic and
hemibiotrophic fungal pathogens must pass through a
series of developmental transitions — including in many
cases differentiation of intricate infection structures such
as haustoria — before they can successfully colonise their
hosts. One would expect non-pathogenic strains either to
exhibit perturbations in these developmental programs or
to affect more specialised steps, for example those which
establish a communication with the host metabolism. In
the past three years, the use of insertional mutagenesis, in
particular restriction enzyme mediated integration
(REMI) mutagenesis, has successfully identified components controlling pathogenicity of the cereal pathogen
Magnaporthe grisea [12,13]. Perhaps unexpectedly, some of
these pathogenicity mutants have also shed light on host
defence mechanisms and signalling.
M. grisea is a hemibiotrophic filamentous ascomycete that
parasitises many grasses, including cereal crops such as
rice, wheat, barley, and millet [14,15]. Appressorium formation is a key step during pathogenesis not only for
Magnaporthe, but also for other ascomycete and basidiomycete plant pathogens. Appressoria are essential for
host cell wall penetration, as they prepare for the transition
from extracellular to invasive life style.
In the mps1 non-pathogenic mutant [16••], early development in rice leaves is indistinguishable from the wild-type
pathogenic strain, including appressorium formation.
However, the mps1 strain fails to penetrate epidermal cells.
Mps1 is highly sequence-related to Saccharomyces cerevisiae
and Schizosaccharomyces pombe mitogen-activated protein
kinases (Slt2 and Spm1, respectively) that play essential
roles in the maintenance of cell wall integrity. Because
Mps1 can rescue the yeast null mutant Slt2, the authors
speculated that the wild-type protein exerts an analogous
function in M. grisea by remodeling the appressorial wall to
facilitate formation of a penetration hypha. Surprisingly,
the mps1 mutation does not prevent infection of abraded
leaf surfaces, suggesting that Mps1 is not required for invasive growth. Whether this latter observation indicates the
existence of an Mps1-independent penetration mechanism, enabling invasive growth in the absence of an intact
epidermal leaf surface, remains to be clarified.
Despite aborted penetration attempts, the mps1 strain still
retains its ability to induce actin re-assembly in attacked
epidermal cells, an early and common host cell response to
attempted fungal attack. There is direct experimental evidence that actin disassembly and re-assembly is a critical
component of non-host resistance in barley, since cytochalasins, actin polymerisation inhibitors, enable a number of
non-barley pathogens to penetrate cell walls and to establish either infection hyphae or haustoria [17,18]. Localized
autofluorescence in the plant cells, directly subtending
appressoria, is also induced by both wild-type and mutant
mps1 strains. This cell-wall associated autofluorescence in
the host cells is considered an early plant defence response
[19]. It is a widespread phenomenon in interactions with
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Biotic interactions
phytopathogenic fungi and is likely to be the result of
oxidative cross-linking of phenolics to the plant cell wall.
Taken together, these observations demonstrate that at
least a subset of early plant defence responses is triggered
prior to host cell wall penetration.
The M. grisea abc1 mutant, contrary to mps1, affects intracellular growth within epidermal cells, that is to say
intracellular hyphae formation ceases shortly after successful penetration [20•]. The ABC1 protein belongs to the
family of ABC carriers and shows highest sequence-relatedness to multi-drug resistance efflux pump transporters
in yeast (PDR5 and CDR1). Strikingly, Abc1 transcription
is strongly upregulated upon contact with the host epidermal cell. One interpretation is that ABC1 represents a
counter-defence component against rice defence mechanisms by exporting anti-microbial compounds at early
stages of pathogenesis. Contrary to yeast PDR5 and CDR1
mutants, however, the abc1 mutant does not exhibit
altered sensitivity to a series of tested antifungal drugs
including the rice phytoalexin sakuranetin. If ABC1 is
indeed an efflux pump of host defence compounds, these
must be widespread among cereals as the abc1 mutant
exhibits arrested intracellular growth in both rice and barley. Alternatively, ABC1 is not part of a counter-defence
mechanism, but may be involved in exporting small fungal
molecules that could either act as toxins or function in
reprogramming the host metabolism to the advantage of
the fungus.
In sum, the abc1 and mps1 mutants provide the first examples that fungal pathogenicity mutants can also be valuable
tools to investigate host defence mechanisms. For example, they may be used in future experiments to dissect the
temporal and spatial succession and the interplay between
broad-spectrum defence mechanisms and race-specific
resistance responses (see below).
Recognition inside and outside the host cell
Race-specific resistance is, as in dicots, a widespread phenomenon in cereal–pathogen interactions. In each case,
cognate gene pairs in host (R genes) and pathogen (Avr
genes) are essential components to trigger a resistance
response. R gene products in monocots and dicots share
the same structural features [21]. The major class contains
an amino-terminal nucleotide binding site (NBS) and carboxy-terminal leucine-rich repeats (LRR) of various
lengths. A second class comprises genes containing a
kinase and/or a LRR domain [22]. Experimental and indirect evidence suggest that the highly variable LRRs in
both classes of R genes have a major role in recognition of
pathogen determinants encoded by Avr genes [23,24]. The
molecular isolation of Xa1 and Xa21 in rice [25,26], each
conferring Avr-dependent resistance to the bacterial leaf
pathogen Xanthomonas oryzae pv. oryzae, provides the first
example that a host plant can recognise determinants from
the same pathogen via NBS–LRR and LRR–kinase type
genes. Xa1, a member of the NBS–LRR class, is predicted
to reside within the cytoplasm, whereas Xa21, a member of
the LRR-kinase class, is likely to be a transmembrane protein with the LRRs exposed extracellularly. This suggests
that recognition events of X. oryzae determinants can occur
both extra- and intracellularly. As Avr genes are likely to
function primarily as pathogenicity factors [27], this may
suggest that X. oryzae can target both extra- and intracellular host factors to induce favourable growth conditions.
It is an intriguing question whether the different
sequence-deduced subcellular locations of Xa21 and Xa1
proteins result in different R gene triggered signalling
pathways. A mutational approach has been initiated to
identify genes required for Xa21 function (PC Ronald
et al., personal communication). Nine fully susceptible
and 15 partially susceptible lines of rice were recovered
from 4,500 M2 families, following radiation and chemical
mutagenesis of a rice genotype containing Xa21. All nine
fully susceptible mutants contained deletions in the Xa21
gene. In contrast, none of the 15 partially susceptible lines
showed detectable rearrangements in the R gene. It will
be interesting to find out whether susceptibility in the latter class of mutants is caused by weakly defective alleles
of Xa21, or is the result of mutations in other genes
required for Xa21 function. As all candidate suppressor
mutants of Xa21 exhibit only partial susceptibility, this
may indicate that the resistance reaction branches rapidly
downstream of Xa21, or that the downstream components
are partially redundant. Alternatively, null alleles of the
suppressors may be lethal.
Transducing death signals
Localised and rapid cell death at attempted infection sites
is probably one of the most common host responses to
pathogens in R gene-triggered resistance of higher plants.
This hypersensitive reaction (HR) is believed to confine
pathogen growth. Biochemically, the HR involves the coordinate activation of a complex series of events of which
the generation of reactive oxygen intermediates (ROI) is
one of the earliest to detect. Collectively, ROI include
H2O2, O2•– and OH•, of which only H2O2 is relatively stable in solution. ROI are believed to drive downstream
responses, including oxidative cross-linking of cell walls,
accumulation of phenolics and phytoalexins, induction of a
whole range of pathogenesis-related (PR) proteins, and the
activation of proteases and protease inhibitors [28]. The
end of this ‘biochemical inferno’ is the death of one or a
cluster of host cells at the infection site. We are only now
beginning to find answers to key questions: is host cell
death the cause of or a consequence of R gene-triggered
resistance? What are the regulatory components linking R
gene-mediated pathogen recognition to the plethora of
downstream responses? One focus of research has been to
find out whether the HR is a form of programmed cell
death (PCD). If this is the case, then, the first question
becomes obsolete because resistance would have to be
envisaged as an integral part of a genetic program destined
to terminate in host cell death.
Defence signalling pathways in cereals Piffanelli, Devoto and Schulze-Lefert
One of the best characterized cereal systems used to study
the genetic and molecular relationship between cell death
and resistance is represented by the interaction between
the obligate biotrophic fungus Erysiphe graminis f. sp. hordei
and its natural host, barley. Obligate biotrophs may actively seek to suppress host cell death, as their life-cycle
depends entirely upon host living tissues [29]. At least two
genetically separable pathways control resistance to this
pathogen [30] in barley leaves. The first is an R gene-triggered pathway which can be activated by different
resistance alleles encoded at the Mla locus and by other
unlinked powdery mildew R gene loci [31]. Each of these
R genes requires at least two additional genes, Rar1 and
Rar2, to execute the resistance response [32]. The second
resistance pathway also requires at least three gene functions: Mlo, Ror1, and Ror2. Unlike the first, in which
race-specific resistance is triggered by dominant R genes,
this second pathway is mediated by recessive mlo alleles,
each conferring broad-spectrum resistance to all tested
powdery mildew isolates [33].
A conserved cell death component in plants
and animals?
Rar1 was recently isolated using a map-based cloning
approach ([7], T Lahaye et al., unpublished data). The
deduced sequence of the 25.5 kDa RAR1 protein uncovered a novel 60 amino acid domain, designated CHORD
(cysteine- and histidine-rich domain). CHORD is arrayed
in a tandem repeat in RAR1 and maybe involved in metal
ion co-ordination. Surprisingly, CHORD-containing proteins are not only conserved in all tested higher plant
species, but also in protozoa and metazoa, including
Drosophila melanogaster, the nematode Caenorhabditis elegans, and Homo sapiens. To test the function of the
CHORD-containing protein in the nematode C. elegans,
the corresponding single-copy gene, chp, was silenced by
RNA interference (RNAi). Silencing of chp revealed semisterility, embryo lethality and gonad hyperplasia. The
latter phenotype is reminiscent of ced-3 and ced-4 cell death
execution mutants [34]. PCD in the germline and soma of
C. elegans is known to depend upon the same execution
machinery (ced-3, ced-4, and ced-9), but to be controlled by
distinct sets of regulatory genes. This suggests an essential
function for chp in the nematode. Whether the gonad
hyperplasia phenotype in the silenced chp nematodes also
indicates an involvement of the gene in the control of
germline PCD remains to be tested.
The significance of Rar1 is based on its requirement for
the function of multiple R genes, indicating a convergence
point in race-specific resistance. Interestingly, susceptible
rar1 mutants compromise an R gene-triggered host cell
death response including the attacked epidermal and subtending mesophyll cells. Moreover, Rar1-dependent and R
gene-specified resistance coincides with a biphasic H2O2
accumulation of which only the second wave is compromised in susceptible rar1 mutant plants. Thus, Rar1
appears to function downstream of R gene-mediated
297
pathogen recognition, but upstream of the second wave of
H2O2 accumulation.
None of the Rar1-dependent R genes have been isolated
from barley. However, the above-mentioned structural similarities between R genes in monocot and dicot species
makes it likely that these will have a similar structure to the
intracellular NBS–LRR or the extracellular LRR classes.
To date, only two other genes representing convergence
points in race-specific resistance to pathogens have been
characterised at the molecular level. Both are from the dicot
Arabidopsis: NDR1 [35] encodes a small and possibly membrane-anchored protein with unknown function, and EDS1
[36] is predicted to be an intracellular protein containing
three sequence motifs characteristic of lipases. RAR1,
NDR1, and EDS1 differ from each other in that the
Arabidopsis proteins are plant-specific, whereas homologues
of barley Rar1 exist in all eukaryotic species examined so
far, except yeast. If the gonad hyperplasia phenotype,
induced by silencing of the Rar1 homologue chp in C. elegans is indeed a consequence of a deregulated germline
PCD, then CHORD proteins may share cell death control
functions in plants and animals. Alternatively, the
sequence-conserved Rar1 homologues control distinct cellular functions in plants and animals.
Similar to human macrophages or neutrophils, ROI are
believed to function in plant defence by either directly
killing the pathogen, or indirectly by triggering a cell death
program [37]. Homologues of gp91phox, a component of
the H2O2-generating complex in mammalian neutrophils,
were recently identified in both monocot and dicot plants
[38–40]. Support for a functional role of this H2O2-generating complex in pathogen defence derives from the
expression of constitutively active and dominant-negative
forms of the small GTP-binding protein OsRac1
(K Shimamoto et al., personal communication), a rice
homologue of the human Rac. The human RAC protein is
one out of three cytosolic factors which, together with two
membrane-bound proteins — P22phox and the above
mentioned GP91phox, define the neutrophil multicomplex enzyme NADPH oxidase [41]. Rice contains three
sequence-related genes of human Rac, designated OsRac1
to OsRac3, each revealing about 60% amino acid sequence
identity to the human counterpart (K Shimamoto, personal communication). Recombinant OsRAC1 was shown to
have both GTP-binding and GTPase activities.
Transgenic expression of a constitutively active form of
OsRAC1 led to the formation of discrete spontaneous leaf
necrosis in young and adult plants. Transgenic expression
of a dominant-negative form of OsRAC1 significantly compromised R-gene triggered resistance upon challenge with
an avirulent M. grisea isolate, though not completely.
Because the constitutively active form of OsRAC1 was also
shown to mediate a constitutive and DPI (diphenyleniodonium)-sensitive H2O2 accumulation in suspension
cultures derived from transformed rice calli, the authors
conclude that the OsRAC1 variant acts specifically through
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Biotic interactions
an altered activity of the NADPH-dependent oxidase
complex. Together with the compromised second wave of
H2O2 accumulation in partially susceptible barley rar1
mutants, the experimental data suggest that in R gene-triggered pathogen resistance at least some of the H2O2
accumulation is catalyzed by a cereal NADPH-dependent
oxidase complex.
A plant-specific death pathway intertwined
with pathogen resistance
Molecular and genetic analysis of the mutation-induced
and broad-spectrum mlo-mediated resistance to the powdery mildew fungus in barley underlines the intimate link
between pathogen defence mechanisms and cell death
control in plants. Wild-type Mlo encodes the prototype of a
novel class of plant-specific integral membrane proteins
[5]. Molecular analysis of susceptible Mlo and a number of
resistant mlo genotypes confirmed that resistance is caused
by a lack of the wild-type gene. We have recently shown
that MLO resides in the plasma membrane of leaf cells
and it is membrane-anchored via seven transmembrane
helices so that the amino-terminus is located extracellularly and the carboxy-terminal tail intracellularly. The
wild-type protein functions in a cell-autonomous fashion
as, in mlo genotypes, transient expression of Mlo in single
epidermal leaf cells is sufficient to confer susceptibility to
the fungus Erysiphe graminis f. sp hordei [10]. Following a
genome-wide search for Mlo sequence-related genes in
Arabidopsis thaliana, we estimate the presence of approximately 35 Mlo family members, each sharing common
gene structure and predicted protein topology. This
genome-wide analysis in Arabidopsis also suggests that Mlorelated genes represent the only abundant gene family
encoding 7TM proteins in higher plants. The genetic
diversification of Mlo family members within a single
species, their topology and subcellular localization are reminiscent of the most abundant class of 7TM receptors in C.
elegans and H. sapiens, the G-protein-coupled receptors
(GPCRs) [42]. These receptors relay extracellular signals
through ligand binding into amplified intracellular
responses via activation of the α subunit of heterotrimeric
G proteins [43,44]. Mlo family members do not share significant sequence similarities with GPCRs, but this does
not preclude MLO being a GPCR, as mammalian GPCR
subfamilies often exhibit negligible amino acid sequence
relatedness with each other [45]. Determining whether
MLO functions like a GPCR or through a novel mechanism remains one of the future challenges.
An apparent pleiotropic effect in mlo plants — the developmentally-controlled leaf necrosis even under axenic
conditions [46] — suggests a possible link between cell
death control and pathogen resistance. Resistance mediated by mlo is dependent upon at least two additional genes,
Ror1 and Ror2, as double mutants mlo ror1 and mlo ror2 are
susceptible to powdery mildew attack [33]. Similarly, developmentally-controlled lesion formation in mlo genotypes is
dependent on Ror1 and Ror2 as both double mutant geno-
types show a reduced number of spontaneous leaf lesions.
Thus, the same three genes that control broad-spectrum
resistance to the fungus also control spontaneous leaf cell
death [30]. Therefore, we re-examined previous observations that leaf epidermal cells resist fungal attack in mlo
plants without an accompanying host cell death. Host cells
retain viability even 30 hours after microscopically
detectable arrest of fungal germlings within the host cell
wall. Thereafter, however, clusters of mesophyll cells, subtending attacked epidermal cells, undergo a cell death
response. This pathogen-triggered cell death in mlo genotypes is also dependent on Ror1 and Ror2 since it is
compromised in both mlo ror1 and mlo ror2 double mutants
(J Orme, personal communication). This suggests that signals emanate from the attacked but non-penetrated
epidermal host cell into subtending mesophyll tissue, leading in the latter to the execution of a cell death program.
Thus, although the mesophyll cell death can be spatially
and temporally separated from the mlo-mediated resistance
reaction, both responses are clearly genetically intertwined.
This may suggest that Mlo has a primary function in the
negative control of leaf cell death which converges, via Ror1
and Ror2, in a pathogen defence pathway.
Conclusions
Pathogen defence and pathogenicity mechanisms can
define opposite sides of the same coin. This is reflected by
a unique collection of non-pathogenic M. grisea mutants
whose analysis is uncovering both general host defence
responses and pathogen counter defence mechanisms.
Disease resistance components Rar1 and OsRac1 provide
the first molecular insights into the signalling of R-genetriggered resistance in cereals. Both proteins are conserved
between plants and animals. However, more experimental
evidence is needed to critically examine a possible functional overlap of the plant genes and their animal
counterparts. Currently, data identify ROI as critical signalling molecules and PCD as the underlying theme in R
gene-mediated resistance responses to biotrophic and
hemibiotrophic cereal fungi. The interconnection between
pathogen resistance and cell death is also underlined by
the genetic and molecular dissection of broad-spectrum
mlo-controlled resistance. In contrast to Rar1 and OsRac1,
Mlo homologues are only found in plants, indicating the
existence of another, possibly plant-specific, PCD control
mechanism. Future comparative functional analysis of Mlo,
Rar1 and OsRac1 homologues should reveal if wiring diagrams in pathogen resistance and cell death control are
conserved between monocots and dicots.
Acknowledgements
The authors are grateful to K Shimamoto, PC Ronald, T Lahaye, K Shirasu
and J Orme who made available unpublished information to assist the
preparation of this review. Many thanks to all members of the P ShulzeLefert lab for helpful discussions and suggestions, and to R Innes for critical
reading of the review. Research work in P Shulze-Lefert’s lab is supported
by grants from the European Union (TMR program — Biotechnology), the
Gatsby Foundation and from the Biotechnology and Biological Sciences
Research Council.
Defence signalling pathways in cereals Piffanelli, Devoto and Schulze-Lefert
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