Three unique mutants of <i>Arabidopsis</i> identify <i>eds</i> loci required for limiting growth of a biotrophic fungal pathogen

Dewdney, Julia; Reuber, T. Lynne; Wildermuth, Mary C.; Devoto, Alessandra; Cui, Jianping; Stutius, Lisa M.; Drummond, Emma P.; Ausubel, Frederick M.

doi:10.1046/j.1365-313x.2000.00870.x

Cited by 227 publications

(207 citation statements)

References 83 publications

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“…If surveillance of cell wall integrity is conserved in plants, one would expect that biotrophic fungi will have evolved means to manipulate components of cell wall integrity in order to suppress SA-dependent resistance. Consistent with this, inefficient SA-dependent resistance (often designated 'basal defence') limits the extent of powdery mildew growth in compatible interactions [16][17][18]. Further evidence of a connection between cell wall structure and stress signalling comes from the finding that a mutation in Arabidopsis CONSTITUTIVE EXPRES-SION OF VSP1 (CEV1), which encodes the cellulose synthase isoform CesA3, or treatment with inhibitors of cellulose biosynthesis leads to enhanced production of jasmonate and ethylene, to constitutive expression of jasmonate/ethylene stress-response genes, and to enhanced resistance to a broad range of pathogens [19 ,20].…”

Section: Introductionmentioning

confidence: 80%

Knocking on the heaven’s wall: pathogenesis of and resistance to biotrophic fungi at the cell wall

Schulze‐Lefert

2004

Current Opinion in Plant Biology

124

101

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New findings challenge the traditional view of the plant cell wall as passive structural barrier to invasion by fungal microorganisms. A surveillance system for cell wall integrity appears to sense perturbation of the cell wall structure upon fungal attack and is interconnected with known plant defence signalling pathways. Biotrophic fungi might manipulate this surveillance system for the establishment of biotrophy. The attempts of fungi to invade also induce a sub-cellular polarisation in attacked cells, which activates an ancient vesicle-associated resistance response that possibly enables the focal transport of regulatory cargo and the secretion of toxic cargo. The underlying resistance machinery might have been subverted by biotrophic fungi for pathogenesis. IntroductionPenetration through the plant cell wall represents an Achilles heel in the pathogenesis of most biotrophic fungi and marks a lifestyle transition from extra-cellular to invasive growth. Modification of the plant cell wall was recognised for the first time as potential resistance mechanism almost 80 years ago following work in which 78 plant species and varieties were challenged with Alternaria spp. and other leaf-spotting fungi [1]. The termination of fungal pathogenesis at the cell wall was commonly associated with wall 'thickenings' and the formation of local additions or 'callosities' in the paramural space (i.e. the space between the cell wall and the plasma membrane). Formation of these cell wall appositions (CWAs) or papillae is usually accompanied by a co-localised accumulation of phenolics and reactive oxygen species [2][3][4][5][6]. The complex process of sub-cellular cell wall remodelling is tightly linked to the rapid disassembly and subsequent focal reassembly of the plant cytoskeleton at fungal entry sites, which is indicative of a pathogen-triggered cell polarisation [6][7][8][9]. There has been a long-standing controversy, however, over whether CWAs function in disease resistance or facilitate the entry of fungal pathogens into host cells by providing a structural collar for the intruder. New molecular genetic data from Arabidopsis and barley have indeed revealed that molecular processes at and in CWAs have Janus-faced functions, that is, functions for fungal pathogenesis and in resistance responses. Focal vesicle transport and vesicle fusion events that are dependent on SNAP (soluble N-ethylmaleimide-sensitive-factor-association protein) receptor (SNARE) proteins at the plasma membrane emerge as potential common underlying mechanisms that might be interconnected with a poorly understood cell wall integrity surveillance system. In this review, I discuss the seemingly paradoxical functions of these processes in establishing the biotrophic lifestyle and in disease resistance at the cell periphery.Linking cell wall structure to biotic stress signalling Callose, a (1!3)-b-D-glucan, has long been known to be synthesised and deposited rapidly at CWAs upon microbial attack. This polymer was thought to contribute to a physical barrie...

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Section: Introductionmentioning

confidence: 80%

Knocking on the heaven’s wall: pathogenesis of and resistance to biotrophic fungi at the cell wall

Schulze‐Lefert

2004

Current Opinion in Plant Biology

124

101

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“…While some genes can be activated by either exogenous SA or exogenous JA (Schenk et al, 2000), other responses activated by SAdependent signaling are inhibited by JA-dependent signaling, and vice versa. Support for the latter idea includes observations that several Arabidopsis mutants with defects in SA-dependent signaling show enhanced inducible expression of PDF1.2: NahG and npr1 plants express PDF1.2 at higher levels than wild-type plants after treatment with rose bengal or infection by Alternaria brassicicola (Clarke et al, 1998;Penninckx et al, 1996); pad4 and eds4 plants (eds4 plants have reduced SA levels after infection) display enhanced PDF1.2 expression in response to treatment with rose bengal or JA (Gupta et al, 2000); sid2 plants fail to accumulate SA and display enhanced PDF1.2 expression in response to Erisyphe orontii infection (Dewdney et al, 2000); JA treatment inhibits SA-dependent cell death in response to ozone exposure (Rao et al, 2000); and, conversely, constitutive expression of PDF1.2 in cpr6 plants is inhibited by treatment with INA, an inducer of SAdependent signaling (Clarke et al, 1998).…”

Section: Discussionmentioning

confidence: 99%

“…Perturbations in SA-dependent signaling have been reported to affect jasmonic acid (JA)-dependent signaling, including the expression of PDF1.2 (Clarke et al, 1998;Dewdney et al, 2000;Gupta et al, 2000;Penninckx et al, 1996;Penninckx et al, 1998;Rao et al, 2000). We found enormous genotype-speci®c variation in PDF1.2 mRNA levels ( Figure 6c).…”

Section: Analysis Of Defense Gene Expression In Double Mutantsmentioning

confidence: 99%

Constitutive salicylic acid‐dependent signaling in cpr1 and cpr6 mutants requires PAD4

Jirage¹,

Zhou²,

Cooper³

et al. 2001

The Plant Journal

126

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SummarySalicylic acid (SA)-dependent signaling controls activation of a set of plant defense mechanisms that are important for resistance to a variety of microbial pathogens. Many Arabidopsis mutants that display altered SA-dependent signaling have been isolated. We used double mutant analysis to determine the relative positions of the pad4, cpr1, cpr5, cpr6, dnd1 and dnd2 mutations in the signal transduction network leading to SA-dependent activation of defense gene expression and disease resistance. The pad4 mutation causes failure of SA accumulation in response to infection by certain pathogens, while the other mutations cause constitutively high levels of SA, defense gene expression and resistance. The cpr1 pad4, cpr5 pad4, cpr6 pad4, dnd1 pad4 and dnd2 pad4 double mutants were constructed and assayed for stature, presence of spontaneous lesions, resistance to Pseudomonas syringae and Peronospora parasitica, SA levels, expression of PAD4, PR-1 and PDF1.2, and accumulation of camalexin. We found that the effects of the cpr1 and cpr6 mutations on SA-dependent gene expression are completely dependent on PAD4 function. In contrast, SA accumulation in the lesion-mimic mutant cpr5 is partially PAD4-independent, while in dnd1 and dnd2 mutants it is completely PAD4-independent. A model describing a possible arrangement of activities in the signal transduction network is presented.

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“…Another member of Group 4, the gene encoding ICS1, has been extensively characterized in the context of pathogenesis (Dewdney et al, 2000;Wildermuth et al, 2001). We here found that basal ICS1 expression is completely abolished upon infection.…”

Section: Changes Independent From Npr1 and Jar1mentioning

confidence: 99%

“…Plants with mutations in the SA or JA signaling pathways (e.g. pad4, eds5, eds14, eds15, sid2, npr1-3, NahG, and coi-1) are hypersusceptible to G. cichoracearum and its closest relative Golovinomyces orontii (formerly Erysiphe orontii; Reuber et al, 1998;Dewdney et al, 2000;Ellis et al, 2002aEllis et al, , 2002b. In addition, plant mutants with constitutive or inducible activation of the SA-(pmr4, edr1) or JA/ET-(wrky70, cev-1) dependent defenses are resistant to G. cichoracearum (Frye and Innes, 1998;Ellis and Turner, 2001;Nishimura et al, 2003;Li et al, 2006).…”

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confidence: 99%

Genome-Wide Expression Profiling Arabidopsis at the Stage ofGolovinomyces cichoracearumHaustorium Formation

et al. 2008

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(T.S., K.D.)Compatibility between plants and obligate biotrophic fungi requires fungal mechanisms for efficiently obtaining nutrients and counteracting plant defenses under conditions that are expected to induce changes in the host transcriptome. A key step in the proliferation of biotrophic fungi is haustorium differentiation. Here we analyzed global gene expression patterns in Arabidopsis thaliana leaves during the formation of haustoria by Golovinomyces cichoracearum. At this time, the endogenous levels of salicylic acid (SA) and jasmonic acid (JA) were found to be enhanced. The responses of wild-type, npr1-1, and jar1-1 plants were used to categorize the sensitivity of gene expression changes to NPR1 and JAR1, which are components of the SA and JA signaling pathways, respectively. We found that the infection process was the major source of variation, with 70 genes identified as having similarly altered expression patterns regardless of plant genotype. In addition, principal component analysis (PCA) identified genes responding both to infection and to lack of functional JAR1 (17 genes) or NPR1 (18 genes), indicating that the JA and SA signaling pathways function as secondary sources of variation. Participation of these genes in the SA or JA pathways had not been described previously. We found that some of these genes may be sensitive to the balance between the SA and JA pathways, representing novel markers for the elucidation of cross-talk points between these signaling cascades. Conserved putative regulatory motifs were found in the promoter regions of each subset of genes. Collectively, our results indicate that gene expression changes in response to infection by obligate biotrophic fungi may support fungal nutrition by promoting alterations in host metabolism. In addition, these studies provide novel markers for the characterization of defense pathways and susceptibility features under this infection condition.

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Three unique mutants of Arabidopsis identify eds loci required for limiting growth of a biotrophic fungal pathogen

Cited by 227 publications

References 83 publications

Knocking on the heaven’s wall: pathogenesis of and resistance to biotrophic fungi at the cell wall

Knocking on the heaven’s wall: pathogenesis of and resistance to biotrophic fungi at the cell wall

Constitutive salicylic acid‐dependent signaling in cpr1 and cpr6 mutants requires PAD4

Genome-Wide Expression Profiling Arabidopsis at the Stage ofGolovinomyces cichoracearumHaustorium Formation

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