ABSTRACTDuring bacterial wilt of tomato, the plant pathogen Ralstonia solanacearum upregulates expression ofpopS, which encodes a type III-secreted effector in the AvrE family. PopS is a core effector present in all sequenced strains in theR. solanacearumspecies complex. The phylogeny ofpopSmirrors that of the species complex as a whole, suggesting that this is an ancient, vertically inherited effector needed for association with plants. ApopSmutant ofR. solanacearumUW551 had reduced virulence on agriculturally importantSolanumspp., including potato and tomato plants. However, thepopSmutant had wild-type virulence on a weed host,Solanum dulcamara, suggesting that some species can avoid the effects of PopS. ThepopSmutant was also significantly delayed in colonization of tomato stems compared to the wild type. Some AvrE-type effectors from gammaproteobacteria suppress salicylic acid (SA)-mediated plant defenses, suggesting that PopS, a betaproteobacterial ortholog, has a similar function. Indeed, thepopSmutant induced significantly higher expression of tomato SA-triggered pathogenesis-related (PR) genes than the wild type. Further, pretreatment of roots with SA exacerbated thepopSmutant virulence defect. Finally, thepopSmutant had no colonization defect on SA-deficient NahG transgenic tomato plants. Together, these results indicate that this conserved effector suppresses SA-mediated defenses in tomato roots and stems, which areR. solanacearum’s natural infection sites. Interestingly, PopS did not trigger necrosis when heterologously expressed inNicotianaleaf tissue, unlike the AvrE homolog DspEPccfrom the necrotrophPectobacterium carotovorumsubsp.carotovorum. This is consistent with the differing pathogenesis modes of necrosis-causing gammaproteobacteria and biotrophicR. solanacearum.IMPORTANCEThe type III-secreted AvrE effector family is widely distributed in high-impact plant-pathogenic bacteria and is known to suppress plant defenses for virulence. We characterized the biology of PopS, the only AvrE homolog made by the bacterial wilt pathogenRalstonia solanacearum. To our knowledge, this is the first study ofR. solanacearumeffector function in roots and stems, the natural infection sites of this pathogen. Unlike the functionally redundantR. solanacearumeffectors studied to date, PopS is required for full virulence and wild-type colonization of two natural crop hosts.R. solanacearumis a biotrophic pathogen that causes a nonnecrotic wilt. Consistent with this, PopS suppressed plant defenses but did not elicit cell death, unlike AvrE homologs from necrosis-causing plant pathogens. We propose that AvrE family effectors have functionally diverged to adapt to the necrotic or nonnecrotic lifestyle of their respective pathogens.