Author: Jaime Cubero
Internal reviewer: Eran Bosis
Expert reviewer: João C. Setubal

Class: XopE
Family: XopE3
Prototype: XAC3224 (Xanthomonas citri pv. citri)
RefSeq ID: WP_011052114.1 (356 aa)
Synonym: AvrXacE2 (Xanthomonas citri pv. citri)
3D structure: Contains a catalytic triad of cysteine, histidine and aspartic acid, and have been grouped with peptide N-glycanases (PNGases, members of the transglutaminase protein superfamily). XopE3 contains N-myristoylation motifs (Dunger et al., 2012).

The gene coding for XopE3 (avrXacE2) was first identified in the genome annotation of Xanthomonas citri subsp. citri A306 (da Silva et al., 2002).

There is no experimental evidence. It is inferred to be a T3E based on similarity to other XopE effectors.

avrXacE2 was shown to be regulated by HrpG regulon in X. citri (Guo et al., 2011). This effector does not contain PIP box-like sequences.

Lesions caused by mutants of X. citri on avrXacE2 show more extensive necrotic areas relative to those caused by wild-type bacteria in citrus leaves and grow slowly compared to wild type strain. This protein may function to attenuate cell death. No effect has been revealed on hypersensitive response (HR) on non-host plants (Dunger et al., 2012).

Confocal microscopy imaging of N. benthamiana cells expressing avrXacE2-GFP fusion shows a localization mainly in the plant cell membrane and in the nucleus (Dunger et al., 2012).

XopE3 belongs to the HopX effector family, which is part of the transglutaminase superfamily (Nimchuk et al., 2007).

In X. citri subsp. citri A306 the gene coding for XopE3 is in a region hypothesized to be a genomic island (Moreira et al., 2010). This region or parts of it are conserved in many Xanthomonas strains, as shown by a genomic neighborhood search in the Integrated Microbial Genomes platform. In particular, in this search gene XAC3225 is nearly always adjacent to XAC3224 (xopE3), suggesting that the protein coded by XAC3225 is an interaction partner of XopE3. Moreira et al. (2010) commented on this as follows: “Next to xopE3 (XAC3224) we find gene XAC3225, whose product is annotated as tranglycosylase mltB. This gene has strong similarity (e-value 10^-133 , 100% coverage) to hopAJ1 from P. syringae pv. tomato strain DC3000, where it is annotated as a T3SS helper protein. Although the hopAJ1 gene is not itself a T3SS substrate, it contributes to effector translocation (Oh et al., 2007). A mutant with a deletion of XAC3225 has reduced ability to cause canker (mutant phenotypes include a reduction in water soaking, hyperplasia, and necrosis compared to wild type) (Laia et al., 2009)”.

Yes (e.g., X. citri, X. arboricola, X. axonopodis).

Yes (Ralstonia, Pseudomonas, Acidovorax).

da Silva AC, Ferro JA, Reinach FC, Farah CS, Furlan LR, Quaggio RB, Monteiro-Vitorello CB, Van Sluys MA, Almeida NF, Alves LM, do Amaral AM, Bertolini MC, Camargo LE, Camarotte G, Cannavan F, Cardozo J, Chambergo F, Ciapina LP, Cicarelli RM, Coutinho LL, Cursino-Santos JR, El Dorry H, Faria JB, Ferreira AJ, Ferreira RC, Ferro MI, Formighieri EF, Franco MC, Greggio CC, Gruber A, Katsuyama AM, Kishi LT, Leite RP, Lemos EG, Lemos MV, Locali EC, Machado MA, Madeira AM, Martinez-Rossi NM, Martins EC, Meidanis J, Menck CF, Miyaki CY, Moon DH, Moreira LM, Novo MT, Okura VK, Oliveira, MC, Oliveira VR, Pereira HA, Rossi A, Sena JA, Silva C, de Souza RF, Spinola LA,Takita MA, Tamura RE, Teixeira EC, Tezza RI, Trindade dos SM, Truffi D, Tsai, SM, White FF, Setubal JC, Kitajima JP (2002). Comparison of the genomes of two Xanthomonas pathogens with differing host specificities. Nature 417: 459-463. DOI: 10.1038/417459a

Dunger G, Garofalo CG, Gottig N, Garavaglia BS, Rosa MC, Farah CS, Orellano EG, Ottado J (2012). Analysis of three Xanthomonas axonopodis pv. citri effector proteins in pathogenicity and their interactions with host plant proteins. Mol. Plant Pathol. 13: 865-876. DOI: 10.1111/j.1364-3703.2012.00797.x

Guo Y, Figueiredo F, Jones J, Wang N (2011). HrpG and HrpX play global roles in coordinating different virulence traits of Xanthomonas axonopodis pv. citri. Mol Plant Microbe Interact. 24: 649-661. DOI: 10.1094/MPMI-09-10-0209

Laia ML, Moreira LM, Dezajacomo J, Brigati JB, Ferreira CB, Ferro MI, Silva AC, Ferro JA, Oliveira JC (2009). New genes of Xanthomonas citri subsp. citri involved in pathogenesis and adaptation revealed by a transposon-based mutant library. BMC Microbiol. 2009, 9: 12. DOI: 10.1186/1471-2180-9-12

Moreira LM, Almeida NF, Potnis N, Digiampietri LA, Adi SS, Bortolossi JC, da Silva AC, da Silva AM, de Moraes FE, de Oliveira JC, de Souza RF (2010). Novel insights into the genomic basis of citrus canker based on the genome sequences of two strains of Xanthomonas fuscans subsp. aurantifolii. BMC Genomics 11: 238. DOI: 10.1186/1471-2164-11-238

Nimchuk ZL, Fisher EJ, Desvaux D, Chang JH, Dangl JL (2007). The HopX (AvrPphE) family of Pseudomonas syringae type III effectors require a catalytic triad and a novel N-terminal domain forfunction. Mol. Plant Microbe Interact. 20: 346-357. DOI: 10.1094/MPMI-20-4-0346

Oh HS, Kvitko BH, Morello JE, Collmer A (2007). Pseudomonas syringae lytic transglycosylases coregulated with the type III secretion system contribute to the translocation of effector proteins into plant cells. J. Bacteriol. 189: 8277-8289. DOI: 10.1128/JB.00998-07