The YopJ superfamily in plant-associated bacteria

Abstract

Bacterial pathogens employ the type III secretion system to secrete and translocate effector proteins into their hosts. The primary function of these effector proteins is believed to be the suppression of host defence responses or innate immunity. However, some effector proteins may be recognized by the host and consequently trigger a targeted immune response. The YopJ/HopZ/AvrRxv family of bacterial effector proteins is a widely distributed and evolutionarily diverse family, found in both animal and plant pathogens, as well as plant symbionts. How can an effector family effectively promote the virulence of pathogens on hosts from two separate kingdoms? Our understanding of the evolutionary relationships among the YopJ superfamily members provides an excellent opportunity to address this question and to investigate the functions and virulence strategies of a diverse type III effector family in animal and plant hosts. In this work, we briefly review the literature on YopJ, the archetypal member from Yersinia pestis, and discuss members of the superfamily in species of Pseudomonas, Xanthomonas, Ralstonia and Rhizobium. We review the molecular and cellular functions, if known, of the YopJ homologues in plants, and highlight the diversity of responses in different plant species, with a particular focus on the Pseudomonas syringae HopZ family. The YopJ superfamily provides an excellent foundation for the study of effector diversification in the context of wide-ranging, co-evolutionary interactions.

Figure 1

Phylogenetic relationships of the YopJ superfamily of type III secreted effector (T3SE) proteins. Neighbour‐joining tree of YopJ family of T3SE proteins. Bootstrap support is indicated above each node, with only values above 60% being shown. Accession numbers for each protein are presented in parentheses following the protein name and species. Modified from Ma et al. (2006). The scale bar indicates the evolutionary distances computed using the JTT substitution matrix (in numbers of amino acid substitutions per site).

Figure 2

Functional diversification of the YopJ superfamily of type III secreted effector (T3SE) proteins. The HopZ family of Pseudomonas syringae T3SE proteins demonstrates the remarkable functional diversification of the YopJ superfamily in plants. In Arabidopsis thaliana ecotype Col‐0, HopZ1a and HopZ1b are recognized by two independent resistance (R) proteins resulting in a hypersensitive response (HR) (Lewis et al., 2010). Both recognition events require an intact myristoylation sequence and catalytic cysteine for recognition, indicating that it is likely that the enzymatic activity of these effectors on membrane‐bound host targets is recognized by their corresponding R proteins (Lewis et al., 2008). HopZ2 promotes the growth of P. syringae in Arabidopsis. This activity requires an intact myristoylation sequence and catalytic cysteine, indicating that HopZ2 targets a membrane‐associated protein(s) to promote P. syringae virulence (Lewis et al., 2008). HopZ3 also promotes the growth of P. syringae, but does not possess a myristoylation sequence, suggesting that its targets are soluble proteins (Vinatzer et al., 2006). In soybean, HopZ1a induces an HR in cultivars OAC Bayfield and Williams 82, which requires an intact myristoylation sequence and catalytic cysteine (Zhou et al., 2009). HopZ2 and HopZ3 also trigger an HR in soybean cultivars OAC Bayfield and Williams 82 (not shown; R. L. Morgan and W. Ma, unpublished data). HopZ1b can promote the growth of P. syringae in soybean cultivar OAC Bayfield, and it has recently been demonstrated that this virulence activity partially requires the 2‐hydroxyisoflavanone dehydratase (GmHID1), which interacts directly with HopZ1b (Zhou et al., 2011). Although all members of the HopZ family possess the catalytic triad present in the archetypical member YopJ, their biochemical function on host targets remains to be demonstrated. YopJ can acetylate and inactivate eukaryotic mitogen‐activated protein kinase kinases (MAPKKs), thereby suppressing host immune responses (Mittal et al., 2006; Mukherjee et al., 2006; Mukherjee and Orth, 2008). Ac, acetyl group.