Pto- and Prf-Mediated Recognition of AvrPto and AvrPtoB Restricts the Ability of Diverse Pseudomonas syringae Pathovars to Infect Tomato

Abstract

The molecular basis underlying the ability of pathogens to infect certain plant species and not others is largely unknown. Pseudomonas syringae is a useful model species for investigating this phenomenon because it comprises more than 50 pathovars which have narrow host range specificities. Tomato (Solanum lycopersicum) is a host for P. syringae pv. tomato, the causative agent of bacterial speck disease, but is considered a nonhost for other P. syringae pathovars. Host resistance in tomato to bacterial speck disease is conferred by the Pto protein kinase which acts in concert with the Prf nucleotide-binding lucine-rich repeat protein to recognize P. syringae pv. tomato strains expressing the type III effectors AvrPto or AvrPtoB (HopAB2). The Pto and Prf genes were isolated from the wild tomato species S. pimpinellifolium and functional alleles of both of these genes now are known to exist in many species of tomato and in other Solanaceous species. Here, we extend earlier reports that avrPto and avrPtoB genes are widely distributed among pathovars of P. syringae which are considered nonhost pathogens of tomato. This observation prompted us to examine the possibility that recognition of these type III effectors by Pto or Prf might contribute to the inability of many P. syringae pathovars to infect tomato species. We show that 10 strains from presumed nonhost P. syringae pathovars are able to grow and cause pathovar-unique disease symptoms in tomato leaves lacking Pto or Prf, although they did not reach the population levels or cause symptoms as severe as a control P. syringae pv. tomato strain. Seven of these strains were found to express avrPto or avrPtoB. The AvrPto- and AvrPtoB-expressing strains elicited disease resistance on tomato leaves expressing Pto and Prf. Thus, a gene-for-gene recognition event may contribute to host range restriction of many P. syringae pathovars on tomato species. Furthermore, we conclude that the diverse disease symptoms caused by different Pseudomonas pathogens on their normal plant hosts are due largely to the array of virulence factors expressed by each pathovar and not to specific molecular or morphological attributes of the plant host.

The HopZ Family ofPseudomonas syringaeType III Effectors Require Myristoylation for Virulence and Avirulence Functions inArabidopsis thaliana

“…Several groups have studied HopAB homologues to determine their virulence and avirulence functions in tomato (33,34), soybean (26), snap bean (27), and Arabidopsis (22); however, this extended family has not been studied from an evolutionary perspective, which limits our understanding of the selective pressures giving rise to this diversity. Since the evolutionary context of the HopZ family is well understood, the HopZ type III effectors provide a unique opportunity to assess the evolutionary pressures driving virulence and avirulence and how these forces drive the underlying molecular and cellular mechanisms of pathogenhost interactions.…”

“…Recent genome-wide screens have identified hundreds of type III effector proteins in P. syringae pathovars that can be subdivided into approximately 50 families (35). Although individual effectors have been studied to determine their virulence and/or avirulence functions, detailed analyses of evolutionarily diverse effector families for a specific host are limited (27,33,34,57).The YopJ/HopZ family is a common and widely distributed class of effector proteins, and members of this family are found in both animal-and plant-pathogenic bacteria. Originally characterized as a cysteine protease (49), the Yersinia pestis YopJ protein was recently shown to possess acetyltransferase activity (43,45).…”

“…Recent genome-wide screens have identified hundreds of type III effector proteins in P. syringae pathovars that can be subdivided into approximately 50 families (35). Although individual effectors have been studied to determine their virulence and/or avirulence functions, detailed analyses of evolutionarily diverse effector families for a specific host are limited (27,33,34,57).…”

Crystal Structure of the Complex between Pseudomonas Effector AvrPtoB and the Tomato Pto Kinase Reveals Both a Shared and a Unique Interface Compared with AvrPto-Pto

“…The resulting constructs were confirmed by sequencing, transformed into DC3000DavrPtoDavrPtoB by electroporation, and analyzed for protein secretion as described previously . Protein gel blotting was performed using a rat anti-HA antibody (2000-fold dilution; Roche Applied Science) or anti-AvrPtoB rabbit antibody (Lin and Martin, 2007). Detection of proteins was performed using horseradish peroxidase-conjugated secondary antibodies (antirat and anti-rabbit) and the ECL plus detection system (AmershamPharmacia).…”

Lifestyles of the Effector Rich: Genome-Enabled Characterization of Bacterial Plant Pathogens

“…for their different plant species. The latter specificity is generally stable in the field despite the observation that loss of just one or two effectors can expand host range to new plant species (Castaneda et al, 2005;Lin and Martin, 2007;Wei et al, 2007;. It is possible that multiple adaptations involving PAMP perception, nutrition, and antimicrobial factors underlie host and tissue specificity.…”