Molecular Properties of the Xanthomonas AvrRxv Effector and Global Transcriptional Changes Determined by Its Expression in Resistant Tomato Plants

Abstract

The Xanthomonas campestris pv. vesicatoria avirulence gene AvrRxv specifies resistance on the tomato line Hawaii 7998 by interacting with three nondominant plant resistance genes. AvrRxv molecular properties that impinge on its avirulence activity were characterized and transcriptional changes caused by AvrRxv expression in resistant tomato plants were extensively examined. AvrRxv localized predominantly to the cytoplasm and possibly in association with plasma and nuclear membranes in both resistant and susceptible tomato plants. The AvrRxv cysteine protease catalytic core was found to be essential for host recognition, because introduction of mutations in this domain affected the ability of AvrRxv to elicit a hypersensitive response and the inhibition of bacterial growth in resistant plants. In addition, expression profiles were analyzed for approximately 8,600 tomato genes in resistant plants challenged with X. campestris pv. vesicatoria strains expressing wild-type AvrRxv or a catalytic core AvrRxv mutant. In all, 420 genes were identified as differentially modulated by the expression of a functional AvrRxv, including over 15 functional classes of proteins and a large number of transcription factors and signaling components. Findings of this study allow the development of new hypotheses about the molecular basis of recognition between AvrRxv and the corresponding resistance proteins, and set the stage for the dissection of signaling and cellular responses triggered in tomato plants by this avirulence factor.

Y4lO of Rhizobium sp. Strain NGR234 Is a Symbiotic Determinant Required for Symbiosome Differentiation

“…YopJ in mammalian host cells inhibits mitogen-activated protein (MAP) kinase and nuclear factor B (NF-B) signaling pathways (35) as well as the TLR3-mediated interferon response (48). In plant-pathogen interactions, resistance mechanisms (hypersensitive response) have been reported for certain nonhosts that seem to recognize a specific YopJ-like effector as avirulence protein (3,8,40,45,49,56,57). In Arabidopsis thaliana, ecotype Nd-1 plants carrying the RRS1-R resistance gene are able to recognize PopP2 (17), and the AvrBsT resistance of ecotype Pi-0 is caused by a mutation in a carboxylesterase, which is predicted to hydrolyze lysophospholipids and acylated proteins (15).…”

Identification of a host 14-3-3 protein that interacts with Xanthomonas effector AvrRxv

“…This suggests a strong conservation of function in the C-terminal domains of YopJ family members as was demonstrated by YopJ function in inhibition of yeast MAPK pathway [80,81]. The functional conservation of catalytic triad residues supports this as well (Table 3) [8,13,23]. We find this to be the case in our phylogenetic analyses of the family, where the C-termini containing the catalytic triad are significantly more conserved than the N-termini.…”

“…Furthermore, AvrRxv-like sequences are found in mammalian pathogens, including YopJ and YopP from Yersinia spp., AvrA from Salmonella, and VopP from Vibrio parahemeolyticus [7,[20][21][22]. Although there are nuclear localization signal sequences in many of these family members and PopP2 has been shown to localize to the nucleus, most AvrRxv family members, including AvrRxv, PopP1 and AvrXv4, apparently do not [6,13,17,23]. XopJ was shown to localize to the plasma membrane by virtue of a N-myristolylation motif, also essential for ability to induce HR on Nicotiana [24].…”

“…Apparently, the catalytic triad that is conserved in all members of the family, may have acetyltransferase rather than protease activity [25]. Mutation of any amino acid in the triad results in loss of function in YopJ, AvrBsT, AvrRxv and AvrXv4 [8,13,23]. It is not clear how to interpret analyses indicating that YopJ and AvrXv4 disrupt SUMO post-translation modifications in host cells [8,13], except possibly by affecting expression levels [25].…”

A Conserved Carboxylesterase Is a SUPPRESSOR OF AVRBST-ELICITED RESISTANCE inArabidopsis

“…Each protein contains the catalytic triad (His, Glu, and Cys) conserved in clan CE Cys proteases. In AvrBsT (Orth et al, 2000), AvrXv4 (Roden et al, 2004b), and AvrRxv (Bonshtien et al, 2005), these residues are required to induce the hypersensitive response (HR) inside resistant plant cells, suggesting that proteolysis or modification of host proteins is the initial signal that triggers immune responses. The host target(s) for these proteins is unknown, apart from AvrXv4, which displays weak small ubiquitin modifier isopeptidase activity in planta (Roden et al, 2004b).…”