Identification of Pseudomonas syringae pv. tomato genes induced during infection of Arabidopsis thaliana

Boch, Jens; Joardar, Vinita; Gao, Lisa; Robertson, Tara L.; Lim, Melisa; Kunkel, Barbara N.

doi:10.1046/j.1365-2958.2002.02877.x

Cited by 180 publications

(168 citation statements)

References 73 publications

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“…4b and 1b). hrpL encodes a sigma factor that regulates both TTSS and coronatine biosynthetic genes through the hrp box (29). These results demonstrate that TTSS is essential for DC3000 to suppress the NHO1 expression.…”

Section: Flagellin Is Required For Nho1 Induction and Resistance In Nmentioning

confidence: 74%

Flagellin induces innate immunity in nonhost interactions that is suppressed by Pseudomonas syringae effectors

Lin

Zhang

et al. 2005

Proc. Natl. Acad. Sci. U.S.A.

258

248

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Arabidopsis NONHOST1 (NHO1) is required for limiting the in planta growth of nonhost Pseudomonas bacteria but completely ineffective against the virulent bacterium Pseudomonas syringae pv. tomato DC3000. However, the molecular basis underlying this observation remains unknown. Here we show that NHO1 is transcriptionally activated by flagellin. The nonhost bacterium P. syringae pv. tabaci lacking flagellin is unable to induce NHO1, multiplies much better than does the wild-type bacterium, and causes disease symptoms on Arabidopsis. DC3000 also possesses flagellin that is potent in NHO1 induction, but this induction is rapidly suppressed by DC3000 in a type III secretion systemdependent manner. Direct expression of DC3000 effectors in protoplasts indicated that at least nine effectors, HopS1, HopAI1, HopAF1, HopT1-1, HopT1-2, HopAA1-1, HopF2, HopC1, and AvrPto, are capable of suppressing the flagellin-induced NHO1 expression. One of the effectors, HopAI1, is conserved in both animal and plant bacteria. When expressed in transgenic Arabidopsis plants, HopAI1 promotes growth of the nonpathogenic hrpL ؊ mutant bacteria. In addition, the purified phytotoxin coronatine, a known virulence factor of P. syringae, suppresses the flagellin-induced NHO1 transcription. These results demonstrate that flagellin-induced defenses play an important role in nonhost resistance. A remarkable number of DC3000 virulence factors act in the plant cell by suppressing the species level defenses, and that contributes to the specialization of DC3000 on Arabidopsis.type III secretion system ͉ virulence ͉ pathogen-associated molecular patterns ͉ basal defense ͉ coronatine N onhost resistance refers to resistance shown by an entire plant species to a specific parasite (1). This resistance is expressed by every plant toward the majority of potential phytopathogens and differs from the cultivar-level resistance conditioned by gene-forgene interactions (2, 3). Plant defenses can be induced by ''general elicitors'' of pathogen or plant origin, including oligosaccharides, lipids, polypeptides, and glycoproteins (4). However, a role of these elicitors in plant disease resistance in a natural setting is often difficult to establish, because plants' responses to elicitors do not differentiate resistant and susceptible plants. Many of the elicitors are now known as pathogen-associated molecular patterns (PAMPs). The best-characterized PAMP known to activate innate immunity in plants is flagellin from Pseudomonas bacteria (5). A conserved N-terminal peptide of flagellin, flg22, is a potent elicitor of defense responses in tomato and Arabidopsis (5, 6). In Arabidopsis, flg22 is perceived by FLS2, a receptor-like kinase that activates downstream events through a MAP kinase cascade (7,8). Pretreatment of Arabidopsis with flg22 peptide not only globally induces defense gene expression, but also protects plants from subsequent infection of the virulent DC3000 (9). Arabidopsis plants lacking FLS2 exhibit enhanced disease susceptibility to DC3000 under certain ...

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Section: Flagellin Is Required For Nho1 Induction and Resistance In Nmentioning

confidence: 74%

Flagellin induces innate immunity in nonhost interactions that is suppressed by Pseudomonas syringae effectors

Lin

Zhang

et al. 2005

Proc. Natl. Acad. Sci. U.S.A.

258

248

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“…Bacterial Avr proteins are translocated into the host cells through a type III protein secretion system (Galan and Collmer, 1999) which, in the case of Pseudomonas syringae DC3000, is thought to deliver more than 30 effector proteins (Boch et al, 2002;Collmer et al, 2002;Fouts et al, 2002;Guttman et al, 2002;Petnicki-Ocwieja et al, 2002;Zwiesler-Vollick et al, 2002). AvrRPM1 and AvrRpt2 from P. syringae provide examples of such type III effector proteins that are recognized by the products of the RPM1 and RPS2 resistance genes, respectively (Dangl et al, 1992;Innes et al, 1993).…”

mentioning

confidence: 99%

The Transcriptional Innate Immune Response to flg22. Interplay and Overlap with Avr Gene-Dependent Defense Responses and Bacterial Pathogenesis

et al. 2004

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Animals and plants carry recognition systems to sense bacterial flagellin. Flagellin perception in Arabidopsis involves FLS2, a Leu-rich-repeat receptor kinase. We surveyed the early transcriptional response of Arabidopsis cell cultures and seedlings within 60 min of treatment with flg22, a peptide corresponding to the most conserved domain of flagellin. Using Affymetrix microarrays, approximately 3.0% of 8,200 genes displayed transcript level changes in flg22 elicited suspension cultures and seedlings. FLARE (Flagellin Rapidly Elicited) genes mostly encode signaling components, such as transcription factors, protein kinases/phosphatases, and proteins that regulate protein turnover. Approximately 80% of flg22-induced genes were also upregulated in Arabidopsis seedlings treated with cycloheximide. This suggests that many FLARE genes are negatively regulated by rapidly turned-over repressor proteins. Twenty-one tobacco Avr9/Cf-9 rapidly elicited (ACRE) cDNA full-length sequences were used to search for their Arabidopsis orthologs (AtACRE). We identified either single or multiple putative orthologs for 17 ACRE genes. For 13 of these ACRE genes, at least one Arabidopsis ortholog was induced in flg22-elicited Arabidopsis suspension cells and seedlings. This result revealed a substantial overlap between the Arabidopsis flg22 response and the tobacco Avr9 race-specific defense response. We also compared FLARE gene sets and genes induced in basal or gene-for-gene interactions upon different Pseudomonas syringae treatments, and infer that Pseudomonas syringae pv tomato represses the flagellin-initiated defense response.

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“…One powerful strategy for targeting gene expression in the natural context is through promoter trap analysis [i.e., in vivo expression technology (IVET)] (6). Variants of this approach have been successfully applied to identify genes induced during phyllosphere colonization of bacterial pathogens (7)(8)(9). However, by definition, the IVET strategy can only give an incomplete picture of the physiology of bacteria.…”

mentioning

confidence: 99%

A proteomic study of Methylobacterium extorquens reveals a response regulator essential for epiphytic growth

Gourion

Rossignol

Vorholt

2006

Proc. Natl. Acad. Sci. U.S.A.

151

129

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Aerial plant surfaces are colonized by diverse bacteria such as the ubiquitous Methylobacterium spp. The specific physiological traits as well as the underlying regulatory mechanisms for bacterial plant colonization are largely unknown. The purpose of this study was to identify proteins produced specifically in the phyllosphere by comparing the proteome of Methylobacterium extorquens colonizing the leaves either with that of bacteria colonizing the roots or with that of bacteria growing on synthetic medium. We identified 45 proteins that were more abundant in M. extorquens present on plant surfaces as compared with bacteria growing on synthetic medium, including 9 proteins that were more abundant on leaves compared with roots. Among the proteins induced during epiphytic growth, we found enzymes involved in methanol utilization, prominent stress proteins, and proteins of unknown function. In addition, we detected a previously undescribed type of two-domain response regulator, named PhyR, that consists of an N-terminal sigma factor (RpoE)-like domain and a C-terminal receiver domain and is predicted to be present in essentially all Alphaproteobacteria. The importance of PhyR was demonstrated through phenotypic tests of a deletion mutant strain shown to be deficient in plant colonization. Among PhyR-regulated gene products, we found a number of general stress proteins and, in particular, proteins known to be involved in the oxidative stress response such as KatE, SodA, AhpC, Ohr, Trx, and Dps. The PhyRregulated gene products partially overlap with the bacterial in planta-induced proteome, suggesting that PhyR is a key regulator for adaptation to epiphytic life of M. extorquens.fitness ͉ sigma factor ͉ stress ͉ two-component system

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Identification of Pseudomonas syringae pv. tomato genes induced during infection of Arabidopsis thaliana

Cited by 180 publications

References 73 publications

Flagellin induces innate immunity in nonhost interactions that is suppressed by Pseudomonas syringae effectors

Flagellin induces innate immunity in nonhost interactions that is suppressed by Pseudomonas syringae effectors

The Transcriptional Innate Immune Response to flg22. Interplay and Overlap with Avr Gene-Dependent Defense Responses and Bacterial Pathogenesis

A proteomic study of Methylobacterium extorquens reveals a response regulator essential for epiphytic growth

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