Modular Study of the Type III Effector Repertoire in Pseudomonas syringae pv. tomato DC3000 Reveals a Matrix of Effector Interplay in Pathogenesis

Hai-Lei Wei,Wei Zhang,Alan Collmer

doi:10.1016/j.celrep.2018.04.037

Hai-Lei Wei, Wei Zhang + Show 1 more

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https://doi.org/10.1016/j.celrep.2018.04.037

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Journal: Cell Reports	Publication Date: May 1, 2018
Citations: 83	License type: cc-by

Affiliation: Cornell University, Plant (United States)

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The bacterial pathogen Pseudomonas syringae pv. tomato DC3000 suppresses the two-tiered innate immune system of Nicotiana benthamiana and other plants by injecting a complex repertoire of type III secretion effector (T3E) proteins. Effectorless polymutant DC3000D36E was used with a modularized system for native delivery of the 29 DC3000 T3Es singly and in pairs. Assays of the performance of this T3E library in N.benthamiana leaves revealed a matrix of T3E interplay, with six T3Es eliciting death and eight others variously suppressing the death activity of the six. The T3E library was also interrogated for effects on DC3000D36E elicitation of a reactive oxygen species burst, for growth in planta, and for T3Es that reversed these effects. Pseudomonas fluorescens and Agrobacterium tumefaciens heterologous delivery systems yielded notably different sets of death-T3Es. The DC3000D36E T3E library system highlights the importance of 13 T3Es and their interplay in interactions with N.benthamiana.

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A common strategy of microbial pathogens of plants and animals is to inject large repertoires of effector proteins that subvert host immunity
Studies with DC3000 suggest that the repertoire contains at least two redundant effector groups (REGs) with complementary functions: HopM1 and AvrE1 redundantly promote the apoplastic water soaking that favors bacterial growth, whereas AvrPto and AvrPtoB redundantly suppress the pattern-triggered immunity (PTI) that is elicited by flagellin perception at the plant cell surface via the pattern recognition receptor FLS2 (Boller and Felix, 2009; Kvitko et al, 2009; Martin, 2012; Xin et al, 2016)
To facilitate study of T3E functions in a native system, we have developed a library of DC3000 T3E genes for modularized deployment in DC3000D36E, singly or in pairs, and we used the library with N. benthamiana to comprehensively identify T3Es that elicit or suppress effector-triggered immunity (ETI)-associated death, increase or reduce bacterial populations in planta, and suppress a flagellin-dependent reactive oxygen species (ROS) response to bacteria or reverse that suppression

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Introduction

A common strategy of microbial pathogens of plants and animals is to inject large repertoires of effector proteins that subvert host immunity. Tomato (Pst) DC3000 uses the type III secretion system (T3SS) to inject 29 type III effectors (T3Es), and it has become a model for exploring the functional structure of effector repertoires and concomitantly probing the structure of the plant immune system (Lindeberg et al, 2012; Xin and He, 2013). Pst DC3000 is experimentally attractive because it can be pathogenic on three model plants: Arabidopsis thaliana, tomato, and Nicotiana benthamiana; many of its effectors have been extensively studied, and the complete repertoire has been genetically disassembled and partially reassembled (Bu€ttner, 2016; Cunnac et al, 2011; Wei and Collmer, 2017; Xin and He, 2013). A minimal level of virulence in N. benthamiana or Arabidopsis can be achieved with single representatives of each of the two REGs or with plant mutants that reproduce the actions of the two REGs on host targets (Chakravarthy et al, 2018; Xin et al, 2016)

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