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bacteria:t3e:xopah

The Type III Effector XopAH from //Xanthomonas//

Author: Steven J. Roberts, Anna Passelergue
Internal reviewer: Christian Vernière, Ralf Koebnik

Class: XopAH
Family: XopAH
Prototype: AvrXccC (Xanthomonas campestris pv. campestris; strain 8004), FZ025_RS19665 (Xanthomonas hyacinthi; strain CFBP 1156)
GenBank ID: ABQ10636.1 (440 aa),
RefSeq ID: WP_011037263.1 (331 aa, perhaps 109 aa too short since the 440-aa version would include a typical N-terminal palmitoylation signal, MGLC), WP_244292408.1 (356 aa)
Synonym: AvrXccC (Xanthomonas campestris pv. campestris), AvrXccFM (Xanthomonas campestris pv. campestris) (Castañeda et al., 2005)
3D structure: Unknown

Biological function

How discovered?

AvrXccC was described during a genome comparison analysis between Xanthomonas citri pv. citri and X. campestris pv. campestris Xcc strain ATCC 33913 = NCPPB 528 (Da Silva et al., 2002) and in a search of annotated genome (Castenada et al., 2005).

XopAH (FZ025_RS19665) was discovered as an ORF that is encoded downstream of a PIP box and a properly spaced ‐10 promoter motif (TTCGB‐N15 ‐TTCGB‐N30–32 ‐YANNNT) (Passelergue, 2025). Additional evidence came from the presence of conserved myristoylation and palmitoylation signals at the N terminus (Nimchuk et al., 2000; Thieme et al., 2007). The protein was also predicted as a type III effector by Effectidor II, a pan-genomic AI-based algorithm for the prediction of type III secretion system effectors (Wagner et al., 2025).

(Experimental) evidence for being a T3E

Secreted XopAH (AvrXccC) proteins were detected in culture fluid from Xcc 8004 and hrcV mutant complemented strains but not from the hrcV mutant (Wang et al., 2007). Insertion and deletion mutants affecting the locus (Xcc2109) in the type strain (Xcc 528) resulted in loss of virulence on the host Florida Broad Leaf Mustard (Castañeda et al., 2005).

XopAH (FZ025_RS19665) was shown to have a functional type III secretion signal using a reporter fusion with AvrBs1 (Zhao et al., 2013; Passelergue, 2025).

Regulation

Promoter activity assays showed that the expression of XopAH (avrXccC) is hrpG/hrpX-dependent (Wang et al., 2007).

The presence of a PIP box and a properly spaced ‐10 promoter motif (TTCGB‐N15 ‐TTCGB‐N30–32 ‐YANNNT) suggests that the xopAH gene (FZ025_RS19665) is under control of HrpG and HrpX (Wengelnik & Bonas, 1996; Wengelnik et al., 1996; Koebnik et al., 2006).

Phenotypes

AvrXccC is required for full virulence in the susceptible host cabbage (Brassica oleracea) (Wang et al., 2007) and results in avirulence in the resistant host mustard (Brassica napiformis) (Castaneda et al., 2005; He et al., 2007; Wang et al., 2007). The intact AvrB-AvrC domain of AvrXccC8004 is essential and sufficient to elicit defense responses in an Arabidopsis resistant ecotype (Col-0) (Ho et al., 2013).

In the interaction Arabidopsis / Xcc strain 8004, AvrXccC8004 not only presented its avirulence activity to trigger plant defense response but also possessed its virulence activity to manipulate the component involved in the ABA signalling pathway leading to an increase of ABA concentrations (Ho et al., 2013).

Localization

XopAH (AvrXccC) is anchored to the plant plasma membrane, and the N‐terminal myristoylation site (amino acids 2–7: GLcaSK) is essential for its localization (Wang et al., 2007).

The presence of conserved myristoylation and palmitoylation signals at the N terminus of XopAH (FZ025_RS19665) suggests again that the protein is localized to the plasma membrane in the plant host cell (Nimchuk et al., 2000; Thieme et al., 2007).

Enzymatic function

XopAH has a Fido/AvrB domain derived from the fic (cyclic adenosine monophosphate (cAMP)-induced filamentation and doc (death on curing) domains (Kinch et al., 2009). Structural comparisons resulted in the inclusion of similar segments of the T3 effector AvrB from Pseudomonas syringae species (Kinch et al., 2009; White et al., 2009). T3 effectors in the XopAH group could trans-AMPylate plant host proteins. AMPylation represents a posttranslational modification used to stably modify proteins with AMP (Kinch et al., 2009).

Interaction partners

Not known.

Conservation

In xanthomonads

In Xanthomonas campestris pv. campestris. XopAH is also present in X. arboricola pv. juglandis within strains causing Walnut Blight but is absent from the strains causing vertical oozing canker (Cesbron et al., 2015).

But also conserved in X. hydrangeae, X. axonopodis, X. hortorum, X. dyei.

In other plant pathogens/symbionts

Yes (AvrB Pseudomonas savastanoi, Pseudomonas syringae) (Lee et al., 2004; Desveaux et al., 2007)

But also conserved in Pseudomonas spp., Xylophilus ampelinus and Exilibacterium sp.,

References

Castañeda A, Reddy JD, El-Yacoubi B, Gabriel DW (2005). Mutagenesis of all eight avr genes in Xanthomonas campestris pv. campestris had no detected effect on pathogenicity, but one avr gene affected race specificity. Mol. Plant Microbe Interact. 18: 1306-1317. DOI: 10.1094/MPMI-18-1306

Cesbron S, Briand M, Essakhi S, Gironde S, Boureau T, Manceau C, Fischer-Le Saux M, Jacques MA (2015). Comparative genomics of pathogenic and nonpathogenic strains of Xanthomonas arboricola unveil molecular and evolutionary events linked to pathoadaptation. Front. Plant Sci. 6: 1126. DOI: 10.3389/fpls.2015.01126

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 Santos M, 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

Desveaux D, Singer AU, Wu AJ, McNulty BC, Musselwhite L, Nimchuk Z, Sondek J, Dangl JL (2007). Type III effector activation via nucleotide binding, phosphorylation, and host target interaction. PLoS Pathog. 3: e48. DOI: 10.1371/journal.ppat.0030048. Erratum in: PLoS Pathog. (2007) 3: e90.

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

Ho YP, Tan CM, Li MY, Lin H, Deng WL, Yang JY (2013). The AvrB_AvrC Domain of AvrXccC of Xanthomonas campestris pv. campestris is required to elicit plant defense responses and manipulate ABA homeostasis. Mol. Plant Microbe Interact. 26: 419-430. DOI: 10.1094/mpmi-06-12-0164-r

Kinch LN, Yarbrough ML, Orth K, Grishin NV (2009). Fido, a novel AMPylation domain common to Fic, Doc, and AvrB. PLoS One 4: e5818. DOI: 10.1371/journal.pone.0005818

Koebnik R, Krüger A, Thieme F, Urban A, Bonas U (2006). Specific binding of the Xanthomonas campestris pv. vesicatoria AraC-type transcriptional activator HrpX to plant-inducible promoter boxes. J. Bacteriol. 188: 7652-7660. DOI: 10.1128/JB.00795-06

Lee CC, Wood MD, Ng K, Andersen CB, Liu Y, Luginbühl P, Spraggon G, Katagiri F (2004). Crystal structure of the type III effector AvrB from Pseudomonas syringae. Structure 12: 487-494. DOI: 10.1016/j.str.2004.02.013

Nimchuk Z, Marois E, Kjemtrup S, Leister RT, Katagiri F, Dangl JL (2000). Eukaryotic fatty acylation drives plasma membrane targeting and enhances function of several type III effector proteins from Pseudomonas syringae. Cell 101: 353-363. DOI: 10.1016/s0092-8674(00)80846-6

Passelergue A (2025). Discovery of eight type III effector genes harboring the PIP box in clade-I xanthomonads. Master's thesis, Université de Montpellier, France.

Qian W, Jia Y, Ren SX, He Y Q, Feng JX, Lu LF, Sun Q, Ying G, Tang DJ, Tang H, Wu W, Hao P, Wang L, Jiang BL, Zeng S, Gu WY, Lu G, Rong L, Tian Y, Yao Z, Fu G, Chen B, Fang R, Qiang B, Chen Z, Zhao GP, Tang JL, He C (2005). Comparative and functional genomic analyses of the pathogenicity of phytopathogen Xanthomonas campestris pv. campestris. Genome Res. 15: 757-767. DOI: 10.1101/gr.3378705

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

Wagner N, Baumer E, Lyubman I, Shimony Y, Bracha N, Martins L, Potnis N, Chang JH, Teper D, Koebnik R, Pupko T (2025). Effectidor II: a pan-genomic AI-based algorithm for the prediction of type III secretion system effectors. Bioinformatics 41: btaf272. DOI: 10.1093/bioinformatics/btaf272

Wang L, Tang X, He C (2007). The bifunctional effector AvrXccC of Xanthomonas campestris pv. campestris requires plasma membrane-anchoring for host recognition. Mol. Plant Pathol. 8: 491-501. DOI: 10.1111/j.1364-3703.2007.00409.x

Wengelnik K, Bonas U (1996). HrpXv, an AraC-type regulator, activates expression of five of the six loci in the hrp cluster of Xanthomonas campestris pv. vesicatoria. J. Bacteriol. 178: 3462-3469. DOI: 10.1128/jb.178.12.3462-3469.1996

Wengelnik K, Van den Ackerveken G, Bonas U (1996). HrpG, a key hrp regulatory protein of Xanthomonas campestris pv. vesicatoria is homologous to two-component response regulators. Mol. Plant Microbe Interact. 9: 704-712. DOI: 10.1094/mpmi-9-0704

White FF, Potnis N, Jones JB, Koebnik R (2009). The type III effectors of Xanthomonas. Mol. Plant Pathol. 10: 749-766. DOI: 10.1111/j.1364-3703.2009.00590.x

Zhao S, Mo WL, Wu F, Tang W, Tang JL, Szurek B, Verdier V, Koebnik R, Feng JX (2013). Identification of non-TAL effectors in Xanthomonas oryzae pv. oryzae Chinese strain 13751 and analysis of their role in the bacterial virulence. World J. Microbiol. Biotechnol. 29: 733-744. DOI: 10.1007/s11274-012-1229-5

Acknowledgements

This fact sheet is based upon work from COST Action CA16107 EuroXanth, supported by COST (European Cooperation in Science and Technology).

bacteria/t3e/xopah.txt · Last modified: 2025/07/31 14:23 by apasselergue