Defence Signalling Pathways in Cereals Pietro Piffanelli, Alessandra Devoto and Paul Schulze-Lefert*
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295 Defence signalling pathways in cereals Pietro Piffanelli, Alessandra Devoto and Paul Schulze-Lefert* The combination of mutational and molecular studies has shed hosts. One would expect non-pathogenic strains either to light on the role of reactive oxygen intermediates and exhibit perturbations in these developmental programs or programmed cell death in cereal disease resistance to affect more specialised steps, for example those which mechanisms. Rice Rac1 and barley Rar1 represent conserved establish a communication with the host metabolism. In disease resistance signalling genes, which may have related the past three years, the use of insertional mutagenesis, in functions in animals. The analysis of non-pathogenic particular restriction enzyme mediated integration Magnaporthe grisea mutants may provide novel tools to study (REMI) mutagenesis, has successfully identified compo- host defence pathways. nents controlling pathogenicity of the cereal pathogen Magnaporthe grisea [12,13]. Perhaps unexpectedly, some of Addresses these pathogenicity mutants have also shed light on host The Sainsbury Laboratory, John Innes Centre, Colney Lane, Norwich defence mechanisms and signalling. NR4 7UH, UK *e-mail: [email protected] M. grisea is a hemibiotrophic filamentous ascomycete that Current Opinion in Plant Biology 1999, 2:295–300 parasitises many grasses, including cereal crops such as rice, wheat, barley, and millet [14,15]. Appressorium for- http://biomednet.com/elecref/1369526600200295 mation is a key step during pathogenesis not only for © Elsevier Science Ltd ISSN 1369-5266 Magnaporthe, but also for other ascomycete and basid- Abbreviations iomycete plant pathogens. Appressoria are essential for 7TM seven transmembrane host cell wall penetration, as they prepare for the transition CHORD cysteine- and histidine-rich domain from extracellular to invasive life style. GPCR G-protein-coupled receptor HR hypersensitive response In the mps1 non-pathogenic mutant [16••], early develop- PCD programmed cell death R gene resistance gene ment in rice leaves is indistinguishable from the wild-type REMI restriction enzyme mediated integration pathogenic strain, including appressorium formation. ROI reactive oxygen intermediates However, the mps1 strain fails to penetrate epidermal cells. Mps1 is highly sequence-related to Saccharomyces cerevisiae Introduction and Schizosaccharomyces pombe mitogen-activated protein Despite the flurry of molecularly isolated plant resistance kinases (Slt2 and Spm1, respectively) that play essential genes in dicot species [1–4], only fragmentary experimental roles in the maintenance of cell wall integrity. Because data are available on resistance signalling pathways and Mps1 can rescue the yeast null mutant Slt2, the authors even less is known about defence mechanisms. Little of the speculated that the wild-type protein exerts an analogous information derived from dicot species has been used so far function in M. grisea by remodeling the appressorial wall to to understand the molecular bases of attack and defence in facilitate formation of a penetration hypha. Surprisingly, cereal plant–pathogen interactions. Instead, advances in the mps1 mutation does not prevent infection of abraded map-based cloning technologies [5–8] and transgene leaf surfaces, suggesting that Mps1 is not required for inva- expression in cereals, both transient and stable [9–11], have sive growth. Whether this latter observation indicates the made even complex monocot genomes amenable to mole- existence of an Mps1-independent penetration mecha- cular analysis. This has complemented the more traditional nism, enabling invasive growth in the absence of an intact tools of Mendelian genetics and mutational studies. epidermal leaf surface, remains to be clarified. In this review we discuss some of the recent developments Despite aborted penetration attempts, the mps1 strain still aimed at the genetic and molecular dissection of both retains its ability to induce actin re-assembly in attacked pathogen and host signal transduction pathways in cereals. epidermal cells, an early and common host cell response to They reflect the variety and complexity of attack and attempted fungal attack. There is direct experimental evi- defence strategies in monocot species and unveil novel dence that actin disassembly and re-assembly is a critical insights into the interplay of resistance and cell death control. component of non-host resistance in barley, since cytocha- lasins, actin polymerisation inhibitors, enable a number of Attack, defence, and counter-defence: lessons non-barley pathogens to penetrate cell walls and to estab- from fungal pathogenicity mutants lish either infection hyphae or haustoria [17,18]. Localized Unlike phytopathogenic bacteria, biotrophic and autofluorescence in the plant cells, directly subtending hemibiotrophic fungal pathogens must pass through a appressoria, is also induced by both wild-type and mutant series of developmental transitions — including in many mps1 strains. This cell-wall associated autofluorescence in cases differentiation of intricate infection structures such the host cells is considered an early plant defence response as haustoria — before they can successfully colonise their [19]. It is a widespread phenomenon in interactions with 296 Biotic interactions phytopathogenic fungi and is likely to be the result of to reside within the cytoplasm, whereas Xa21, a member of oxidative cross-linking of phenolics to the plant cell wall. the LRR-kinase class, is likely to be a transmembrane pro- Taken together, these observations demonstrate that at tein with the LRRs exposed extracellularly. This suggests least a subset of early plant defence responses is triggered that recognition events of X. oryzae determinants can occur prior to host cell wall penetration. both extra- and intracellularly. As Avr genes are likely to function primarily as pathogenicity factors [27], this may The M. grisea abc1 mutant, contrary to mps1, affects intra- suggest that X. oryzae can target both extra- and intracellu- cellular growth within epidermal cells, that is to say lar host factors to induce favourable growth conditions. intracellular hyphae formation ceases shortly after success- ful penetration [20•]. The ABC1 protein belongs to the It is an intriguing question whether the different family of ABC carriers and shows highest sequence-relat- sequence-deduced subcellular locations of Xa21 and Xa1 edness to multi-drug resistance efflux pump transporters proteins result in different R gene triggered signalling in yeast (PDR5 and CDR1). Strikingly, Abc1 transcription pathways. A mutational approach has been initiated to is strongly upregulated upon contact with the host epider- identify genes required for Xa21 function (PC Ronald mal cell. One interpretation is that ABC1 represents a et al., personal communication). Nine fully susceptible counter-defence component against rice defence mecha- and 15 partially susceptible lines of rice were recovered nisms by exporting anti-microbial compounds at early from 4,500 M2 families, following radiation and chemical stages of pathogenesis. Contrary to yeast PDR5 and CDR1 mutagenesis of a rice genotype containing Xa21. All nine mutants, however, the abc1 mutant does not exhibit fully susceptible mutants contained deletions in the Xa21 altered sensitivity to a series of tested antifungal drugs gene. In contrast, none of the 15 partially susceptible lines including the rice phytoalexin sakuranetin. If ABC1 is showed detectable rearrangements in the R gene. It will indeed an efflux pump of host defence compounds, these be interesting to find out whether susceptibility in the lat- must be widespread among cereals as the abc1 mutant ter class of mutants is caused by weakly defective alleles exhibits arrested intracellular growth in both rice and bar- of Xa21, or is the result of mutations in other genes ley. Alternatively, ABC1 is not part of a counter-defence required for Xa21 function. As all candidate suppressor mechanism, but may be involved in exporting small fungal mutants of Xa21 exhibit only partial susceptibility, this molecules that could either act as toxins or function in may indicate that the resistance reaction branches rapidly reprogramming the host metabolism to the advantage of downstream of Xa21, or that the downstream components the fungus. are partially redundant. Alternatively, null alleles of the suppressors may be lethal. In sum, the abc1 and mps1 mutants provide the first exam- ples that fungal pathogenicity mutants can also be valuable Transducing death signals tools to investigate host defence mechanisms. For exam- Localised and rapid cell death at attempted infection sites ple, they may be used in future experiments to dissect the is probably one of the most common host responses to temporal and spatial succession and the interplay between pathogens in R gene-triggered resistance of higher plants. broad-spectrum defence mechanisms and race-specific This hypersensitive reaction (HR) is believed to confine resistance responses (see below). pathogen growth. Biochemically, the HR involves the co- ordinate activation of a complex series of events of which Recognition inside and outside the host cell the generation of reactive oxygen intermediates (ROI) is Race-specific resistance is, as in dicots, a widespread phe- one of the earliest to detect. Collectively, ROI include – nomenon in cereal–pathogen interactions. In each case, H2O2, O2• and OH•, of which only H2O2 is relatively