Molecular Evolution of Pseudomonas syringae Type III Secreted Effector Proteins.

Marcus M Dillon,Darrell Desveaux,Renan N.D Almeida,Alexandre Martel,David S Guttman,Bevan S Weir,Bradley Laflamme

doi:10.3389/fpls.2019.00418

Marcus M Dillon, Darrell Desveaux + Show 5 more

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https://doi.org/10.3389/fpls.2019.00418

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Abstract

Diverse Gram-negative pathogens like Pseudomonas syringae employ type III secreted effector (T3SE) proteins as primary virulence factors that combat host immunity and promote disease. T3SEs can also be recognized by plant hosts and activate an effector triggered immune (ETI) response that shifts the interaction back toward plant immunity. Consequently, T3SEs are pivotal in determining the virulence potential of individual P. syringae strains, and ultimately help to restrict P. syringae pathogens to a subset of potential hosts that are unable to recognize their repertoires of T3SEs. While a number of effector families are known to be present in the P. syringae species complex, one of the most persistent challenges has been documenting the complex variation in T3SE contents across a diverse collection of strains. Using the entire pan-genome of 494 P. syringae strains isolated from more than 100 hosts, we conducted a global analysis of all known and putative T3SEs. We identified a total of 14,613 putative T3SEs, 4,636 of which were unique at the amino acid level, and show that T3SE repertoires of different P. syringae strains vary dramatically, even among strains isolated from the same hosts. We also find substantial diversification within many T3SE families, and in many cases find strong signatures of positive selection. Furthermore, we identify multiple gene gain and loss events for several families, demonstrating an important role of horizontal gene transfer (HGT) in the evolution of P. syringae T3SEs. These analyses provide insight into the evolutionary history of P. syringae T3SEs as they co-evolve with the host immune system, and dramatically expand the database of P. syringae T3SEs alleles.

Highlights

Over the past three decades, type III secreted effectors (T3SEs) have been recognized as primary mediators of many host–microbe interactions (Michiels and Cornelis, 1991; Salmond and Reeves, 1993; Hueck, 1998; Coburn et al, 2007; Deng et al, 2017; Hu et al, 2017; Rapisarda and Fronzes, 2018). These proteins are translocated directly from the pathogen cell into the host cytoplasm by the type III secretion system (T3SS), where they perform a variety of functions that generally promote virulence and suppress host immunity (Coburn et al, 2007; Zhou and Chai, 2008; Cunnac et al, 2009; Oh et al, 2010; Buttner, 2016; Khan et al, 2018)
We identified a total of 14,613 T3SEs from 494 P. syringae whole-genomes that include strains from 11 of the 13 P. syringae species complex phylogroups
We validated our approach and assessed whether the reliance on protein queries (e.g., BLASTP) substantially increased the likelihood of missing T3SEs without predicted protein sequences due to the lack of a properly called coding sequence. To do this we examined whether we recovered all T3SEs from the well characterized repertoires of P. syringae strains PtoDC3000, PsyB728a, Pph1448a, and PtoT1 (Cunnac et al, 2009; Xin et al, 2018)

Summary

Introduction

Over the past three decades, type III secreted effectors (T3SEs) have been recognized as primary mediators of many host–microbe interactions (Michiels and Cornelis, 1991; Salmond and Reeves, 1993; Hueck, 1998; Coburn et al, 2007; Deng et al, 2017; Hu et al, 2017; Rapisarda and Fronzes, 2018) These proteins are translocated directly from the pathogen cell into the host cytoplasm by the type III secretion system (T3SS), where they perform a variety of functions that generally promote virulence and suppress host immunity (Coburn et al, 2007; Zhou and Chai, 2008; Cunnac et al, 2009; Oh et al, 2010; Buttner, 2016; Khan et al, 2018). This expanding collection of strains and the increased availability of comparative genomics data presents unique opportunities for obtaining insight into the determinants of host specificity in P. syringae (Baltrus et al, 2011, 2012; O’Brien et al, 2011, 2012; Dillon et al, 2019)

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