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 ...

SummaryTo identify components of the defense response that limit growth of a biotrophic fungal pathogen, we isolated Arabidopsis mutants with enhanced disease susceptibility to Erysiphe orontii. Our initial characterization focused on three mutants, eds14, eds15, and eds16. None of these is considerably more susceptible to a virulent strain of the bacterial pathogen Pseudomonas syringae pv. maculicola (Psm). All three mutants develop a hypersensitive response when in®ltrated with Psm expressing the avirulence gene avrRpt2, which activates resistance via the LZ-NBS/LRR resistance protein encoded by RPS2. The growth of Psm(avrRpt2), while somewhat greater in the mutants than in the wild type, is less than growth of the isogenic virulent strain. These results indicate that resistance mediated via LZ-NBS/LRR R genes is functional. Analysis of the growth of avirulent Peronospora parasitica strains showed that the resistance pathway utilized by TIR-NBS/LRR R genes is also operative in all three mutants. Surprisingly, only eds14 and eds16 were more susceptible to Erysiphe cichoracearum. Analysis of the expression pro®les of PR-1, BGL2, PR-5 and PDF1.2 in eds14, eds15, and eds16 revealed differences from the wild type for all the lines. In contrast, these mutants were not signi®cantly different from wild type in the deposition of callose at sites of E. orontii penetration. All three mutants have reduced levels of salicylic acid after infection. eds16 was mapped to the lower arm of chromosome I and found by complementation tests to be allelic to the salicylic acid-de®cient mutant sid2.

Plants have evolved different but interconnected strategies to defend themselves against herbivorous insects and microbial pathogens. We used an Arabidopsis/Pseudomonas syringae pathosystem to investigate the impact of pathogen-induced defense responses on cabbage looper (Trichoplusia ni) larval feeding. Arabidopsis mutants [npr1, pad4, eds5, and sid2(eds16)] or transgenic plants (nahG) that are more susceptible to microbial pathogens and are compromised in salicylic acid (SA)-dependent defense responses exhibited reduced levels of feeding by T. ni compared with wild-type plants. Consistent with these results, Arabidopsis mutants that are more resistant to microbial pathogens and have elevated levels of SA (cpr1 and cpr6) exhibited enhanced levels of T. ni feeding. These experiments suggested an inverse relationship between an active SA defense pathway and insect feeding. In contrast to these results, there was increased resistance to T. ni in wild-type Arabidopsis ecotype Columbia plants that were infected with P. syringae pv. maculicola strain ES4326 (Psm ES4326) expressing the avirulence genes avrRpt2 or avrB, which elicit a hypersensitive response, high levels of SA accumulation, and systemic acquired resistance to bacterial infection. Similar results were obtained with other ecotypes, including Landsberg erecta, Cape Verdi Islands, and Shakdara. When infected with Psm ES4326(avrRpt2) or Psm ES4326(avrB), nahG transgenic and npr1 mutant plants (which are more susceptible to virulent and avirulent P. syringae strains) failed to show the increased insect resistance exhibited by wild-type plants. It was surprising that wild-type plants, as well as nahG and npr1 plants, infected with Psm ES4326 not expressing avrRpt2 or avrB, which elicits disease, became more susceptible to T. ni. Our results suggest two potentially novel systemic signaling pathways: a systemic response elicited by HR that leads to enhanced T. ni resistance and overrides the SA-mediated increase in T. ni susceptibility, and a SA-independent systemic response induced by virulent pathogens that leads to enhanced susceptibility to T. ni.Plants are frequently subjected to simultaneous insect herbivory and pathogen infection. They respond to these two different types of attackers with the induction of distinctive and overlapping subsets of secondary compounds or other defense responses involving antimicrobial or insecticidal activity. Although each type of interaction has been separately studied, the host response to the combined attack by insects and pathogens has received much less attention despite the abundance of reports indicating that pathogens and insects affect each other's performance on the host (Maleck and Dietrich, 1999;Paul et al., 2000). This study describes a model to study the three-way interactions between plants, insect herbivores, and microbial pathogens.Plants respond to insect herbivory with a complicated arsenal of defensive responses, including the synthesis of insecticidal secondary metabolites, antifeeding proteins, and/o...