Author: Jaime Cubero
Internal reviewer: Ralf Koebnik
Expert reviewer:

Class: XopE
Family: XopE1
Prototype: XCV0294 (Xanthomonas euvesicatoria pv. euvesicatoria, ex Xanthomonas campestris pv. vesicatoria; strain 85-10)
RefSeq ID: CAJ21925.1 (400 aa)
Synonym: AvrXacE1 (Xanthomonas citri pv. citri)
3D structure: Myristoylation motif at the extreme N terminus (Thieme et al., 2007).

XopE1 was first identified by sequence homology searches (da Silva et al., 2002; Thieme et al., 2005).

XopE1 fused to the AvrBs3 reporter was shown to be secreted into culture supernatants in a hrcV-dependent manner (Thieme et al., 2007). The same fusion constract was translocated into plant cells in a hrcV- and hrpF-dependent manner (Thieme et al., 2007).

Using RT-PCR analyses, XopE1 from X. euvesicatoria was found to be upregulated by HrpG and HrpX (Thieme et al., 2007). The promoter of xopE1_XCV85-10 contains a PIP BOX (Thieme et al., 2007).

Transcriptome analysis (RNA-seq) and qRT-PCR revealed that avrXacE1 (xopE1) gene expression is downregulated in a X. citri pv. citri ΔphoP mutant, indicating that PhoP is a positive regulator of xopE1 expression (Wei et al., 2019).

Agrobacterium-mediated expression of XopE1 triggers a fast cell-death reaction in non host Nicotiana plants revealing that XopE1 is recognized by Nicotiana. Its membrane localization delays the detection by the plant surveillance system and contributes to inactivate plant immune responses (Thieme et al., 2007). XopE1 was associated to different grades of cytotoxicity and intermediate growth inhibition on yeast and caused phenotypes ranging from chlorosis to cell death when transiently expressed via Agrobacterium in either host or non-host plants (Salomon et al., 2011; Adlung et al., 2016). XopE1 mutants grew to equivalent titers as wild-type X. euvesicatoria in tomato leaves indicating that is not required for bacterial multiplication in planta. However, XopE1 was found to be required to suppress chlorosis and tissue collapse at very late stages of Xanthomonas infection. XopE1 together with XopE2 and XopO may function redundantly to inhibit X. euvesicatoria-induced chlorosis in tomato leaves (Dubrow et al., 2018).

XopE1 fused to GFP reporter in a binary vector under control of the Cauliflower mosaic virus 35S promoter and transiently expressed in Nicotiana benthamiana leaves, using Agrobacterium-mediated gene transfer, allowed to observe XopE1::GFP to be confined to the periphery of the cells and being not detectable in the nucleus or in the cytoplasm.

XopE1 belongs to the HopX effector family, members of which belong to the transglutaminase superfamily (Nimchuk et al., 2007).

XopE1 was found to physically interact with tomato 14-3-3s (TFT) (Dubrow et al., 2018). In addition, XopE1 was predicted to interact with VirK, which is secreted by the T2SS and for which a possible role in the modulation of plant immune response during the infection process was suggested (Assis et al., 2017).

Yes (e.g., X. alfalfa, X. citri, X. euvesicatoria, X. phaseoli).

Yes (Acidovorax spp., Pseudomonas spp., Ralstonia solanacearum; more distant homologs in rhizobia).

Adlung N, Prochaska H, Thieme S, Banik A, Blüher D, John P, Nagel O, Schulze S, Gantner J, Delker C, Stuttmann J, Bonas U (2016). Non-host resistance induced by the Xanthomonas effector XopQ is widespread within the genus Nicotiana and functionally depends on EDS1. Front. Plant Sci. 7: 1796. DOI: 10.3389/fpls.2016.01796

Assis RAB, Polloni LC, Patané JSL, Thakur S, Felestrino ÉB, Diaz-Caballero J, Digiampietri LA, Goulart LR, Almeida NF, Nascimento R, Dandekar AM, Zaini PA, Setubal JC, Guttman DS, Moreira LM (2017). Identification and analysis of seven effector protein families with different adaptive and evolutionary histories in plant-associated members of the Xanthomonadaceae. Sci. Rep. 7:16133. DOI: 10.1038/s41598-017-16325-1

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

Dubrow Z, Sunitha S, Kim JG, Aakre CD, Girija AM, Sobol G, Teper D, Chen YC, Ozbaki-Yagan N, Vance H, Sessa G, Mudgett MB (2018). Tomato 14-3-3 proteins are required for Xv3 disease resistance and interact with a subset of Xanthomonas euvesicatoria effectors. Mol. Plant Microbe Interact. 31: 1301-1311. DOI: 10.1094/MPMI-02-18-0048-R

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

Salomon D, Dar D, Sreeramulu S, Sessa G (2011). Expression of Xanthomonas campestris pv. vesicatoria type III effectors in yeast affects cell growth and viability. Mol Plant Microbe Interact. 24: 305-314. DOI: 0.1094/MPMI-09-10-0196

Thieme F, Koebnik R, Bekel T, Berger C, Boch J, Büttner D, Caldana C, Gaigalat L, Goesmann A, Kay S, Kirchner O, Lanz C, Linke B, McHardy AC, Meyer F, Mittenhuber G, Nies DH, Niesbach-Klösgen U, Patschkowski T, Rückert C, Rupp O, Schneiker S, Schuster SC, Vorhölter F, Weber E, Pühler A, Bonas U, Bartels D, Kaiser O (2005). Insights into genome plasticity and pathogenicity of the plant pathogenic bacterium Xanthomonas campestris pv. vesicatoria revealed by the complete genome sequence. J. Bacteriol. 187: 7254-7266. DOI: 10.1128/JB.187.21.7254-7266.2005

Thieme F, Szczesny R, Urban A, Kirchner O, Hause G, Bonas U (2007). New type III effectors from Xanthomonas campestris pv. vesicatoria trigger plant reactions dependent on a conserved N-myristoylation motif. Mol. Plant Microbe Interact. 20: 1250-1261. DOI: 10.1094/MPMI-20-10-1250

Wei C, Ding T, Chang C, Yu C, Li X, Liu Q (2019). Global regulator PhoP is necessary for motility, biofilm formation, exoenzyme production and virulence of Xanthomonas citri subsp. citri on citrus plants. Genes 10: 340. DOI: 10.3390/genes10050340