Virulence systems of Pseudomonas syringae pv. tomato promote bacterial speck disease in tomato by targeting the jasmonate signaling pathway

Abstract

These authors contributed equally to this work. SummaryPseudomonas syringae pv. tomato strain DC3000 (Pst DC3000) causes bacterial speck disease on tomato. The pathogenicity of Pst DC3000 depends on both the type III secretion system that delivers virulence effector proteins into host cells and the phytotoxin coronatine (COR), which is thought to mimic the action of the plant hormone jasmonic acid (JA). We found that a JA-insensitive mutant (jai1) of tomato was unresponsive to COR and highly resistant to Pst DC3000, whereas host genotypes that are defective in JA biosynthesis were as susceptible to Pst DC3000 as wild-type (WT) plants. Treatment of WT plants with exogenous methyl-JA (MeJA) complemented the virulence defect of a bacterial mutant de®cient in COR production, but not a mutant defective in the type III secretion system. Analysis of host gene expression using cDNA microarrays revealed that COR works through Jai1 to induce the massive expression of JA and wound response genes that have been implicated in defense against herbivores. Concomitant with the induction of JA and wound response genes, the type III secretion system and COR repressed the expression of pathogenesis-related (PR) genes in Pst DC3000-infected WT plants. Resistance of jai1 plants to Pst DC3000 was correlated with a high level of PR gene expression and reduced expression of JA/wound response genes. These results indicate that COR promotes bacterial virulence by activating the host's JA signaling pathway, and further suggest that the type III secretion system might also modify host defense by targeting the JA signaling pathway in susceptible tomato plants.

Cross Talk in Defense Signaling

“…For instance, virulent P. syringae bacteria produce coronatine that functions as a potent mimic of JA-Ile (Nomura et al, 2005). It is assumed that coronatine triggers hypersensitive induction of JA-Ile responses, resulting in suppression of effectual SA-dependent defenses through pathway cross talk, as well as enhanced growth of the pathogen (Zhao et al, 2003;Brooks et al, 2005;Cui et Doares et al, 1995;Spoel et al, 2003). However, Doares et al (1995) provided evidence that exogenous application of SA to tomato (Solanum lycopersicum) plants strongly inhibited the JA-induced expression of genes encoding proteinase inhibitors I and II, suggesting that SA also targets the JA pathway downstream of JA biosynthesis.…”

Kinetics of Salicylate-Mediated Suppression of Jasmonate Signaling Reveal a Role for Redox Modulation

“…A wellstudied example is the suppression of SA-dependent host defenses by the jasmonate-mimicking virulence factor coronatine of the bacterial pathogen P. syringae (Zhao et al, 2003;Brooks et al, 2005;Cui et al, 2005;Laurie-Berry et al, 2006). Coronatine produced by P. syringae in a susceptible host actively inhibits the SA signaling pathway, thereby promoting susceptibility to this pathogen.…”

“…One of these virulence factors is the Pseudomonas syringae phytotoxin coronatine, which functions as a jasmonate analog. During the interaction with susceptible Arabidopsis plants, coronatine suppresses SA-dependent defenses, thereby promoting susceptibility to this pathogen (Zhao et al, 2003;Brooks et al, 2005;Cui et al, 2005;Laurie-Berry et al, 2006).…”

Transcriptional Profiling of Sorghum Induced by Methyl Jasmonate, Salicylic Acid, and Aminocyclopropane Carboxylic Acid Reveals Cooperative Regulation and Novel Gene Responses

“…Pathogens may also have evolved the ability to turn SA/JA antagonisms to their own advantage. P. syringae uses the JA mimic coronatine to induce the JA pathway, resulting in a reduced PR protein accumulation and increased pathogen susceptibility (Zhao et al, 2003).…”