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Author: Monika Kałużna
Internal reviewer: Alice Boulanger
Expert reviewer: WANTED!

Class: XopD (Xanthomonas outer protein D)
Family: XopD
Prototype: XCV0437 (Xanthomonas euvesicatoria pv. euvesicatoria, ex Xanthomonas campestris pv. vesicatoria; strain 85-10)
GenBank ID: CAJ22068.1 (545 aa; original but wrong structural annotation)
GenBank ID: DAA34040.1 (760 aa; new structural annotation)
RefSeq ID: WP_228949438.1 (760 aa; new structural annotation)
3D structure: 2OIV, 2OIX (Chosed et al., 2007); 5JP1, 5JP3 ( Pruneda et al., 2016 )

Biological function

How discovered?

XopD was discovered in a cDNA-AFLP screen and reverse transcription-PCR analyses (Noël et al., 2002).

(Experimental) evidence for being a T3E

XopD is a desumoylating enzyme with strict specificity for its plant small ubiquitin-like modifier (SUMO) substrates (Chosed et al., 2007). C-terminus of XopD (amino acids 322–520) shares primary sequence similarity with the C48 family of cysteine peptidases (Rawlings et al., 2006). In the XopD polypeptide, amino acid positions 309–481 are most homologous to the C-terminal catalytic domain of the Ulp1 ubiquitin-like protease protein family, which is highly conserved (Li & Hochstrasser, 1999; Hotson et al., 2003). Unlike yeast Ulp1 which process a variety of SUMO substrates, XopD exhibits rigid SUMO substrate specificity, it will process only certain plant SUMOs, i.e. T-SUMO, AtSUMO-1, and AtSUMO-2 (Chosed et al., 2007). However, another study has shoxn that XopD shows a mixed activity, being a (tomato)-SUMO and Ubiquitin isopeptidase. The capacity to efficiently recognize both substrates suggest a large evolutionary pressure to become a multifunctionnal protease (Pruneda et al., 2016).

Besides C-terminal SUMO protease domain (Hotson et al., 2003; Chosed et al., 2007), XopD has a unique N-terminal region with a host range determining non-specific DNA-binding domain (DBD) (Kim et al., 2011) and a central domain with two internal ERF-associated amphiphilic repression (EAR) motifs (L/FDLNL/FXP) (Ohta et al., 2001), which were found in plant repressors that regulate stress induced transcription. XopD might repress host transcription during Xcv infection (Ohta et al., 2001; Kim et al., 2011).


The xopD gene expression is induced in a hrpG- and hrpX-dependent manner (Noël et al., 2002). It was described that, XopD promoter does not contain a PIP box, but a hrp box, which is found in all hrpL-dependent promoters in P.syringae and Erwinia spp. (GGAACTNA-N13-CGACNNA; consensus: GGAACcNa-N13/14-cCACNNA) (Noël et al., 2002; Innes et al., 1993). However, after carefully inspected the intergenic region of the Xanthomonas euvesicatoria pv. euvesicatoria 85-10 genome (Xcv 85-10) between the XCV0436 locus and the xopD locus for an alternative promoter and start site (Kim et al., 2011), identified a putative PIP box and ATG just downstream of the XCV0436 locus. Using ATG as the putative start codon, the respective xopD ORF predicts a protein with 760 aa with a longer N-terminal domain (Kim et al., 2011).


XopD is a unique virulence factor that promotes tolerance to Xcv 85-10 in infected host leaves and affects bacteria miltiplication (Kim et al., 2008). It was found that delays the onset leaf chlorosis and necrosis, two phenotypes associated with pathogen-triggered immunity (PTI) activation (Kim et al., 2008). Delaying in tissue damages and lower chlorophyll loss corelate with reduced host defense transcription and reduced salicylic acid (SA) levels-plant defense hormone that limits the spread of pathogens in infected host plant. Moreover, expression of XopD in planta is sufficient to repress not only SA- but also jasmonic acid–induced gene transcription (Hotson et al., 2003; Kim et al., 2008; Kim et al., 2011). It was also shown that XopD highly induces the tomato transcription factor, bHLH132 (Kim et al., 2019). This induction is dependant of XopD SUMO protease activity. This sutdy has shown that is involved in both plant development and plant defense regulation and that silencing bHLH132 mRNA expression results in stuned tomato with enhanced susceptibility to Xcv infection.

For instance, XcvΔxopD mutants grow poorly in infected tomato leaves because defenses dependent from SA were not stifled (Kim et al., 2008). It is also known that XopDXcv85-10 directly interacts with tomato ethylene responsive transcription factor SlERF4. XopD desumoylates SlERF4 and suppress its activity in ethylene production, which is required for anti-Xcv ethylene stimulated immunity and symptom development (Kim et al., 2013). XopDXccB100 from the Xanthomonas campestris pv. campestris (Xcc) strain B100 specifically interacts with MYB30 to suppress its activity in activating plant defense responses required for anti-Xcc immunity (Canonne et al., 2011).

Comparative analysis of the XopD effector family in other phytopathogenic bacteria revealed that so called XopD-like proteins presents differences in sequence and length of their N-terminal domains. This suggests that the N-terminal domain of XopD and XopD-like effectors might impart substrate and/or host specificity.

Transgenic expression of XopDXcc8004 in Arabidopsis has shown an accumulation of host defense response in a SA-dependent way (Tan et al., 2015). Another study showed that psvA Xcc8004 and psvA XccATCC33913 (Castaneda et al., 2005) are not required for Xcc virulence in their host plants. Moreover, XopDXccB100, although having high sequence similarity with XopDXcv85–10 except for the KAE-rich domain localized in N-terminal region (Canonne et al., 2012), was not required for Xcc B100 virulence in Arabidopsis, N. benthamiana, and radish. These findings suggest that XopD-like effectors are not important for Xcc-plant interactions (Kim et al., 2011).


XopD localizes to subnuclear foci. The N terminus of XopD is required for targeting the effector to the plant nucleus; C-terminal domain encodes a Cys protease that cleaves SUMO-conjugated proteins (Hotson et al., 2003; Kim et al., 2008).

Enzymatic function

Peptidase, isopeptidase or desumoylating enzyme (Hotson et al., 2003).

Interaction partners



In xanthomonads

Yes (e.g. Xanthomonas campestris pv. vesicatoria, X. campestris pv. campestris (Kim et al., 2011).

In other plant pathogens/symbionts

Yes (Acidovorax and Pseudomonas spp., e.g., A. avenae subsp. citrulli, A. avenae subsp. avenae, P. savastanoi pv. savastanoi, P. syringae pv. eriobotryae, P. syringae pv. myricae, P. savastanoi pv. savastanoi, P. syringae pv. dendropanacis (Kim et al., 2011).


Canonne J, Marino D, Jauneau A, Pouzet C, Brière C, Roby D, Rivas S (2011). The Xanthomonas type III effector XopD targets the Arabidopsis transcription factor MYB30 to suppress plant defense. Plant Cell 23: 3498-3511. DOI: 10.1105/tpc.111.088815. Retraction in: Plant Cell (2018) 30: 253. DOI: 10.1105/tpc.17.00567

Canonne J, Pichereaux C, Mario D, Roby D, Rossignol M, Rivas S (2012). Identification of the protein sequence of the type III effector XopD from the B100 strain of Xanthomonas campestris pv. campestris. Plant Signal Behav. 7: 184-187. DOI: 10.4161/psb.18828.

Castaneda 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

Chosed R, Tomchick DR, Brautigam CA, Mukherjee S, Negi VS, Machius M, Orth K (2007). Structural analysis of Xanthomonas XopD provides insights into substrate specificity of ubiquitin-like protein proteases. J. Biol. Chem. 282: 6773-6782. DOI: 10.1074/jbc.M608730200

Hotson A, Chosed R, Shu H, Orth K, Mudgett MB (2003). Xanthomonas type III effector XopD targets SUMO-conjugated proteins in planta. Mol. Microbiol. 50: 377-389. DOI: 10.1046/j.1365-2958.2003.03730.x

Innes RW, Bent AF, Kunkel BN, Bisgrove SR, Staskawicz BJ (1993). Molecular analysis of avirulence gene avrRpt2 and identification of a putative regulatory sequence common to all known Pseudomonas syringae avirulence genes. J. Bacteriol. 175: 4859-4869. DOI: 10.1128/jb.175.15.4859-4869.1993

Kim JG, Taylor KW, Hotson A, Keegan M, Schmelz EA, Mudgett MB (2008). XopD SUMO protease affects host transcription, promotes pathogen growth, and delays symptom development in Xanthomonas-infected tomato leaves. Plant Cell 20: 1915-1929. DOI: 10.1105/tpc.108.058529

Kim JG, Stork W, Mudgett MB (2013). Xanthomonas type III effector XopD desumoylates tomato transcriptionfactor SlERF4 to suppress ethylene responses and promote pathogen. Cell Host Microbe 13: 143-154. DOI: 10.1016/j.chom.2013.01.006

Kim JG, Taylor KW, Mudgett MB (2011). Comparative analysis of the XopD type III secretion (T3S) effector family in plant pathogenic bacteria. Mol. Plant Pathol. 12: 715-730. DOI: 10.1111/j.1364-3703.2011.00706.x

Li SJ, Hochstrasser M (1999). A new protease required for cell-cycle progression in yeast. Nature 398: 246-251. DOI: 10.1038/18457

Noël L, Thieme F, Nennstiel D, Bonas U (2002). Two novel type III-secreted proteins of Xanthomonas campestris pv. vesicatoria are encoded within the hrp pathogenicity island. J. Bacteriol. 184: 1340-1348. DOI: 10.1128/jb.184.5.1340-1348.2002

Ohta M, Matsui K, Hiratsu K, Shinshi H, Ohme-Takagi M (2001). Repression domains of class II ERF transcriptional repressors share an essential motif for active repression. Plant Cell 13: 1959-1968. DOI: 10.1105/tpc.010127

Pruneda JN, Durkin CH, Geurink PP, Ovaa H, Santhanam B, Holden DW, Komander D (2016). The molecular basis for ubiquitin and ubiquitin-like specificities in bacterial effector proteases. Mol. Cell 63: 261-276. DOI: 10.1016/j.molcel.2016.06.015

Rawlings ND, Morton FR, Barrett AJ (2006). MEROPS: the peptidase database. Nucl. Acids Res. 34: D270-D272. DOI: 10.1093/nar/gkj089

Tan CM, Li MY, Yang PY, Chang SH, Ho YP, Lin H, Deng WL, Yang JY (2015). Arabidopsis HFR1 is a potential nuclear substrate regulated by the Xanthomonas type III effector XopDXcc8004. PLoS One 10: e0117067. DOI: 10.1371/journal.pone.0117067

Further reading

Canonne J, Marino D, Noël LD, Arechaga I, Pichereaux C, Rossignol M, Roby D, Rivas S (2010). Detection and functional characterization of a 215 amino acid N-terminal extension in the Xanthomonas type III effector XopD. PLoS One 5: e15773. DOI: 10.1371/journal.pone.0015773. Retraction in: PLoS One (2018) 13: e0190773. DOI: 10.1371/journal.pone.0190773

Raffaele S, Rivas S (2013). Regulate and be regulated: integration of defense and other signals by the AtMYB30 transcription factor. Front. Plant Sci. 4: 98. DOI: 10.3389/fpls.2013.00098

Tan L, Rong W, Luo H, Chen Y, He C (2014). The Xanthomonas campestris effector protein XopDXcc8004 triggers plant disease tolerance by targeting DELLA proteins. New Phytol. 204: 595-608. DOI: 10.1111/nph.12918

bacteria/t3e/xopd.txt · Last modified: 2023/10/02 21:22 by rkoebnik