Author: Jaime Cubero
Internal reviewer: Eran Bosis
Expert reviewer:

Class: XopE
Family: XopE2
Prototype: XCV2280 (Xanthomonas euvesicatoria pv. euvesicatoria, ex Xanthomonas campestris pv. vesicatoria; strain 85-10)
RefSeq ID: WP_011347479.1 (358 aa)
Synonym: AvrXacE3 (Xanthomonas citri pv. citri); AvrXccE1 (Xanthomonas campestris pv. campestris)
3D structure: Myristoylation motif at the extreme N terminus (Thieme et al., 2007).

XopE2 was first identified by sequence homology searches (da Silva et al., 2002 (XACb0011); Thieme et al. 2005; Thieme et al., 2007).

XopE2 fused to the AvrBs3 reporter was shown to translocate into plant cells in an hrpF-dependent manner (Thieme et al., 2007).

XopE2 from X. euvesicatoria was found to be regulated by HrpG and HrpX, its promoter contains a PIP BOX and it is coregulated with the T3 secretion machinery (Thieme et al., 2007).

• XopE2 shows an avirulence activity in Solanum pseudocapsicum (Thieme et al., 2007).
• Agrobacterium mediated transient expression of XopE2 shows avirulence activity in the ornamental plant S. pseudocapsicum (Lin et al., 2011).
• XopE2 proteins were shown to be capable of suppressing the hypersensitive response (HR) of Nicotiana spp. induced by HopPsyA of P. syringae pv. syringae 61 and the reaction occurs within the plant cells after their delivery by TTSS (Lin et al., 2011).
• XopE2 inhibits growth of yeast cells in the presence of sodium chloride and caffeine (Salomon et al., 2011).
• Expression of XopE2 in yeast affects the yeast cell wall and the endoplasmic reticulum stress response (Bosis et al., 2011).
• XopE2 appears to promote wall-bound invertase activity in pepprt leaves (Sonnewald et al., 2011).
• XopE2 mutants grow to equivalent titers as wild type X. euvesicatoria in tomato leaves indicating that is not required for bacterial multiplication in planta. XopE2 together with XopE1 and XopO may function redundantly to inhibit X. euvesicatoria induced chlorosis in tomato leaves (Dubrow et al., 2018).
• XopE2 inhibits the activation of a PTI-inducible promoter by the bacterial peptide elf18 in Arabidopsis protoplasts and by flg22 in tomato protoplasts. This effector inhibits flg22-induced callose deposition in planta and enhanced disease symptoms caused by attenuated Pseudomonas syringae bacteria (Popov et al., 2016).

XopE2 fused to GFP in a binary vector under control of the Cauliflower mosaic virus 35S promoter expressed in Nicotiana benthamiana leaves, using Agrobacterium-mediated gene transfer, allowed to localize XopE2::GFP confined to the periphery of the cells and not detectable in the nucleus or in the cytoplasm. Localization of the XopE2::GFP to the plasma membrane of N. benthamiana mesophyll cells could be confirmed by immunocytochemistry (Thieme et al., 2007).

XopE2 belongs to the HopX effector family, which are part of the transglutaminase superfamily (Nimchuk et al., 2007).

XopE2 was found to physically interact with tomato 14-3-3 (TFT) proteins. XopE2 is phosphorylated at multiple residues in planta for maximal binding to TFT10 (Dubrow et al., 2018).

In xanthomonads

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

Yes (Pseudomonas, Ralstonia).

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

Bosis E, Salomon D, Sessa G (2011). A simple yeast-based strategy to identify host cellular processes targeted by bacterial effector proteins. PLoS One 6: e27698. DOI: 10.1371/journal.pone.0027698

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

Lin RH, Peng CW, Lin YC, Peng HL, Huang HC (2011). The XopE2 effector protein of Xanthomonas campestris pv. vesicatoria is involved in virulence and in the suppression of the hypersensitive response. Bot. Stud. 52: 55-72. Link

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

Popov G, Fraiture M, Brunner F, Sessa G (2016). Multiple Xanthomonas euvesicatoria type III effectors inhibit flg22-triggered immunity. Mol. Plant Microbe Interact. 29: 651-660. DOI: 10.1094/MPMI-07-16-0137-R

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

Sonnewald S, Priller JP, Schuster J, Glickmann E, Hajirezaei MR, Siebig S, Mudgett MB, Sonnewald U (2012). Regulation of cell wall-bound invertase in pepper leaves by Xanthomonas campestris pv. vesicatoria type three effectors. PLoS One 7: e51763. DOI: 10.1371/journal.pone.0051763

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

He YQ, Zhang L, Jiang BL, Zhang ZC, Xu RQ, Tang DJ, Qin J, Jiang W, Zhang X, Liao J, Cao JR, Zhang SS, Wei ML, Liang XX, Lu GT, Feng JX, Chen B, Cheng J, Tang JL (2007). Comparative and functional genomics reveals genetic diversity and determinants of host specificity among reference strains and a large collection of Chinese isolates of the phytopathogen Xanthomonas campestris pv. campestris. Genome Biol. 8: R218. DOI: 10.1186/gb-2007-8-10-r218