Pseudomonas syringae manipulates systemic plant defenses against pathogens and herbivores

Abstract

Many pathogens are virulent because they specifically interfere with host defense responses and therefore can proliferate. Here, we report that virulent strains of the bacterial phytopathogen Pseudomonas syringae induce systemic susceptibility to secondary P. syringae infection in the host plant Arabidopsis thaliana. This systemic induced susceptibility (SIS) is in direct contrast to the well studied avirulence͞R gene-dependent resistance response known as the hypersensitive response that elicits systemic acquired resistance. We show that P. syringae-elicited SIS is caused by the production of coronatine (COR), a pathogen-derived functional and structural mimic of the phytohormone jasmonic acid (JA). These data suggest that SIS may be a consequence of the previously described mutually antagonistic interaction between the salicylic acid and JA signaling pathways. Virulent P. syringae also has the potential to induce net systemic susceptibility to herbivory by an insect (Trichoplusia ni, cabbage looper), but this susceptibility is not caused by COR. Rather, consistent with its role as a JA mimic, COR induces systemic resistance to T. ni. These data highlight the complexity of defense signaling interactions among plants, pathogens, and herbivores. (1), selection often favors the evolution of inducible rather than constitutive resistance (2). Plant defenses effective against one enemy may or may not confer resistance to other enemies (3). Moreover, some pathways involved in defense appear to have negative regulatory effects on pathways involved in resistance to other enemies (4, 5). Dissecting the mechanics of defense signaling ''cross-talk'' and its implications for calibrating phenotypic responses therefore is critical for understanding the ecology and evolution of plant resistance.Plant microbial pathogens are referred to as virulent if they cause disease symptoms in susceptible hosts and avirulent if they elicit a strong defense response that blocks pathogenesis (6). One mechanism by which pathogens, such as the Gram-negative bacterium Pseudomonas syringae, activate an immune response is through the translocation of effector proteins (virulence factors) directly into host cells via a type III secretion system (6). Detection of type III effectors by resistance proteins encoded by R genes activates a signaling cascade leading to rapid, localized programmed cell death known as the hypersensitive response (HR), which is correlated with the restriction of pathogen growth at the infection site (6). In turn, the HR leads to a systemic response mediated by salicylic acid (SA) called systemic acquired resistance (SAR), in which noninfected leaves become resistant to a wide range of bacterial and fungal pathogens whose growth is limited by SA-dependent responses. Genes encoding type III effectors that are recognized through host R genes in an avirulent interaction are termed avirulence genes (avr) because of the phenotype they confer. Virulent pathogens, in contrast, cause disease either because they do not produce type ...

Methyl Salicylate Production and Jasmonate Signaling Are Not Essential for Systemic Acquired Resistance inArabidopsis

“…Our presented results rule out a decisive role of the JA pathway during SAR because systemic resistance in the JA biosynthesis mutants dde2 and opr3, as well as in the downstream signaling mutants coi1, jar1, and jin1, is significantly enhanced in response to a local Psm inoculation ( Figure 8B). A SAR-positive phenotype for coi1 mutants has also been reported by Cui et al (2005). The correlation between SAR, JA petiole exudation, and systemic JA elevation reported by Truman et al (2007) is questionable because it was not tested in this study whether the high inoculum (OD 0.2) used for analytical JA determinations indeed induces a SAR response.…”

“…In addition, we have never detected increased levels of JA or OPDA in distant tissue under these conditions (Mishina et al, 2008). Taken together, data from our and other laboratories (Cui et al, 2005;Chaturvedi et al, 2008) argue against a significant function of the JA pathway during SAR establishment and long-distance signaling. Moreover, the wild-type-like SAR-inducing capacity of Pst cor 2 mutants reveals that bacterial production of the JA-Ile-mimicking phytotoxin coronatine does not affect the SAR process, neither positively nor negatively ( Figure 9B).…”

Abscisic Acid-Induced Resistance against the Brown Spot Pathogen Cochliobolus miyabeanus in Rice Involves MAP Kinase-Mediated Repression of Ethylene Signaling

“…For instance, some P. syringae pathovars have shown an ability to synthesize ET both in vitro and in planta from Met through the 2-keto-4-methylthiobutyric acid pathway (Weingart et al, 2001). This ability, together with the production of the JA mimic coronatine and auxins by the same microorganisms, is assumed to contribute to hormonal saturation and consequent circumvention of effectual defenses (Cui et al, 2005;Sreedharan et al, 2006). More recently, Ralstonia solanacearum has been seen to produce ET by means of the HrpG regulon (Valls et al, 2006).…”

Arabidopsis PECTIN METHYLESTERASEs Contribute to Immunity against Pseudomonas syringae

“…As expected, DDE2 was not required for induction by Pma ES4326, because this strain produces the JA-Ile mimic, coronatine (Cui et al, 2005;Katsir et al, 2008). We studied diagnostic mutants to distinguish the roles of two branches of JA signaling.…”