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Title: Deletions in the repertoire of Pseudomonas syringae pv. tomato DC3000 type III secretion effector genes reveal functional overlap among effectors

Author
item KVITKO, BRIAN - CORNELL UNIV
item VELASQUEZ, ANDRE - CORNELL UNIV
item WEI, CHIA-FONG - CORNELL UNIV
item RUSSELL, ALISTAIR - CORNELL UNIV
item MARTIN, GREGORY - CORNELL UNIV & BTI
item Schneider, David
item COLLMER, ALAN - CORNELL UNIV

Submitted to: PLoS Pathogens
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 3/19/2009
Publication Date: 4/17/2009
Citation: Kvitko, B.H., Velasquez, A.C., Wei, C., Russell, A.B., Martin, G.B., Schneider, D.J., Collmer, A. 2009. Deletions in the repertoire of Pseudomonas syringae pv. tomato DC3000 type III secretion effector genes reveal functional overlap among effectors. PLoS Pathogens. 5(4):1-16.

Interpretive Summary: For many bacterial plant pathogens, the ability to secrete proteins directly into host cells is essential for full virulence. These proteins, referred to as effectors, are delivered by a specialized needle-like apparatus called the type III secretion system (T3SS). One such pathogen, Pseudomonas syringae pv. tomato DC3000 (DC3000), relies heavily on a T3SS system to cause disease in several hosts including tomato and Arabidopsis thaliana, but not Nicotiana benthamiana. The availability of a genomic sequence for DC3000 made it possible to determine the complete repertoire of effectors for this organism. A large fraction of these genes, 18 of 28, are clustered in regions that vary considerably between strains within this species. Systematic deletion of these regions yielded several novel findings. First, the deletion of one of these clustered effectors, hopQ1-1, extended the host range of DC3000 to include N. benthamiana. Second, systematic deletion of the regions containing clustered effectors produced a set of strains whose growth on N. benthamiana leaves was reduced to varying degrees. Further laboratory work on these strains detected a surprising functional redundancy among three effectors, AvrE, HopR1, and HopM1. Third, computational analysis of the protein sequences suggests that AvrE and HopR1 are members of a previously uncharacterized superfamily that has at least one representative in almost all bacterial plant pathogens exhibiting T3SS-dependent virulence. Finally, a model is proposed that connects this kind of functional redundancy among effectors to vulnerable steps in signaling and response pathways related to host defenses.

Technical Abstract: Many bacterial pathogens of plants and animals disarm and remodel host cells by injecting large repertoires of effectors via the type III secretion system (T3SS). The repertoires of individual strains appear to function as robust systems that can tolerate loss of individual effectors with little or no reduction in virulence. Pseudomonas syringae pv. tomato DC3000, the causative agent of bacterial speck of tomato, actively deploys 28 effectors. According to the current model for P. syringae-plant interactions, the primary function of the effectors is to suppress PAMP (pathogen-associated molecular pattern)-triggered immunity (PTI). A second layer of defense involves detection inside plant cells of injected effectors or their activity by resistance (R) proteins, which results in effector-triggered immunity (ETI). Pathogens may evade ETI by mutating the betraying effector gene or by deploying another effector that suppresses ETI. Here, we extend our analysis of DC3000 effector gene cluster polymutants by deleting to produce a strain lacking all 18 of the clustered effector genes. We explore the basis for the failure of the resulting mutant to grow well in N. benthamiana, and identify functional redundancy with the effector repertiore. This analysis leads to HopR1, a member of an effector superfamily that also contains the AvrE family. We then explore the effects of deleting the PAMP-encoding fliC gene on the growth of DC3000 effector polymutants. Our observations lead to the proposal that AvrE1/HopR1/HopM1 and AvrPto1/AvrPtoB form redundant-effector groups (REGs) that make major contributions to DC3000 growth in N. benthamiana by targeting different steps in PTI.