Author: Lucas Morinière
Internal reviewer: Coline Sciallano
Expert reviewer:

Class: XopX
Family: XopX
Prototype: XopX (Xanthomonas euvesicatoria pv. euvesicatoria, ex Xanthomonas campestris pv. vesicatoria; strain 85-10)
RefSeq ID: WP_011346212.1 (699 aa)
3D structure: Unknown

XopX was discovered through the screening of a genomic cosmid library of X. euvesicatoria strain GM98-38 conjugated in X. campestris pv. campestris followed by inoculation in tobacco plants (Nicotiana benthamiana) (Metz et al., 2005).

Translational fusions of XopX with the calmodulin-dependent adenylate cyclase domain of Bordetella pertussis (Cya) were exchanged by simple homologous recombination into the genomic copy of xopX of X. euvesicatoria strains 85* (constitutive hrp expression mutant), 85* ΔhrcV (T3SS-defective mutant) and wild-type GM98-38. All Cya fusion strains except 85* ΔhrcV still induced cell death response activity in N. benthamiana. Moreover, leaf extracts of N. benthamiana inoculated with these fusion strains were assayed for cAMP, and only strains with a functional T3SS showed an increase in cAMP levels due to translocation of the Cya reporter protein into the plant (Metz et al., 2005).

qRT-PCR revealed that transcript levels of 15 out of 18 tested non-TAL effector genes (as well as the regulatory genes hrpG and hrpX), including xopX, were significantly reduced in the Xanthomonas oryzae pv. oryzae ΔxrvC mutant compared with those in the wild-type strain PXO99^A (Liu et al., 2016).

• XopX was demonstrated to be cytotoxic when expressed in yeast, suggesting it may target a conserved eukaryotic cell process required for cell viability (Salomon et al., 2011).
• During infection of rice (Oryzae sativa) with X. oryzae pv. oryzae, XopX was shown to be an inhibitor of rice innate immune response, as it suppresses LipA-induced callose deposition (Sinha et al., 2013).
• XopX is required for the development of X. euvesicatoria-induced symptoms in the bacterial spot disease of tomato (Solanum lycopersicum) and pepper (Capsicum annuum). Indeed, it promotes ethylene production, and therefore chlorosis and plant cell death during infection by X. euvesicatoria of susceptible tomato and in transient expression assays in tobacco. Interestingly, it also suppresses flagellin-induced production of reactive oxygen species (ROS) while promoting the accumulation of pattern-triggered immunity (PTI) gene transcripts (Stork et al., 2015). Eventually, the complex behavior of XopX in planta, which combines activation and suppression of immunity-related plant responses at the same time, allows to classify this effector with the T3Es that activates the plant ‘default to death and defense’ response (Lindeberg et al., 2012; Stork et al., 2015).
• When transiently expressed in N. benthamina by Agrobacterium tumefaciens–mediated expression system, XopX from X. oryzae pv. oryzicola cause the nonhost HR at approximatey 2 days (Li et al., 2015).
• A ∆xopK mutant strain of Xanthomonas phaseoli pv. manihotis (aka Xanthomonas axonopodis pv. manihotis) showed reduced growth in planta and delayed spread through the vasculature system of cassava (Mutka et al., 2016).
• Agrobacterium-mediated transient expression of both XopQ and XopX in rice cells resulted in induction of rice immune responses. These immune responses were not observed when either protein was individually expressed in rice cells. XopQ-XopX induced rice immune responses were not observed with a XopX mutant that is defective in 14-3-3 binding (Deb et al., 2020).
• A screen for Xanthomonas effectors which can suppress XopQ-XopX induced rice immune responses, led to the identification of five effectors, namely XopU, XopV, XopP, XopG and AvrBs2, that could individually suppress these immune responses. These results suggest a complex interplay of Xanthomonas T3SS effectors in suppression of both pathogen-triggered immunity and effector-triggered immunity to promote virulence on rice (Deb et al., 2020).

Unknown.

Unknown.

It has been suggested that XopX-triggering of plant cell death response was dependent of another cofactor delivered by the T3SS, yet still unknown (Metz et al., 2005).

XopX interacts with two of the eight rice 14-3-3 proteins. Mutants of XopX that are defective in 14-3-3 binding are also defective in suppression of immune responses, suggesting that interaction with 14-3-3 proteins is required for suppression of host innate immunity (Deb et al., 2020).

Yeast two-hybrid, bimolecular fluorescence complementation (BiFC) and co-IP assays indicated that XopQ and XopX interact with each other (Deb et al., 2020).

Yes, xopX homologs can be found in almost every sequenced Xanthomonas spp. strain, except X. albilineans and X. sacchari, making it an ancient Xanthomonas core T3E (Stork et al., 2015).

Related proteins (query cover > 80% and percent identity > 50 %) can be detected in several unclassified Burkholderiales (Xylophilus ampelinus, Rivibacter sp., Rhizobacter sp., Mitsuaria sp.) and in the Comamonadaceae (Hydrogenophaga taeniospiralis).

Deb S, Ghosh P, Patel HK, Sonti RV (2020). Interaction of the Xanthomonas effectors XopQ and XopX results in induction of rice immune responses. Plant J., in press. DOI: 10.1111/tpj.14924

Jiang BL, He YQ, Cen WJ, Wei HY, Jiang GF, Jiang W, Hang XH, Feng JX, Lu GT, Tang DJ, Tang JL (2008). The type III secretion effector XopXccN of Xanthomonas campestris pv. campestris is required for full virulence. Res. Microbiol. 159: 216-220. DOI: 10.1016/j.resmic.2007.12.004 Information needs to be added to the profile.

Li S, Wang Y, Wang S, Fang A, Wang J, Liu L, Zhang K, Mao Y, Sun W (2015). The type III effector AvrBs2 in Xanthomonas oryzae pv. oryzicola suppresses rice immunity and promotes disease development. Mol. Plant Microbe Interact. 28: 869-880. DOI: 10.1094/MPMI-10-14-0314-R Information needs to be added to the profile.

Lindeberg M, Cunnac S, Collmer A (2012). Pseudomonas syringae type III effector repertoires: last words in endless arguments. Trends Microbiol. 20: 199-208. DOI: 10.1016/j.tim.2012.01.003

Liu Y, Long J, Shen D, Song C (2016). Xanthomonas oryzae pv. oryzae requires H-NS-family protein XrvC to regulate virulence during rice infection. FEMS Microbiol. Lett. 363: fnw067. DOI: 10.1093/femsle/fnw067

Medina CA, Reyes PA, Trujillo CA, Gonzalez JL, Bejarano DA, Montenegro NA, Jacobs JM, Joe A, Restrepo S, Alfano JR, Bernal A (2018). The role of type III effectors from Xanthomonas axonopodis pv. manihotis in virulence and suppression of plant immunity. Mol. Plant Pathol. 19: 593-606. DOI: 10.1111/mpp.12545 Information needs to be added to the profile.

Metz M, Dahlbeck D, Morales CQ, Sady BA, Clark ET, Staskawicz BJ (2005). The conserved Xanthomonas campestris pv. vesicatoria effector protein XopX is a virulence factor and suppresses host defense in Nicotiana benthamiana: XopX effector protein suppresses plant host defense. Plant J. 41: 801-814. DOI: 10.1111/j.1365-313X.2005.02338.x

Mutka AM, Fentress SJ, Sher JW, Berry JC, Pretz C, Nusinow DA, Bart R (2016). Quantitative, image-based phenotyping methods provide insight into spatial and temporal dimensions of plant disease. Plant Physiol. 172: 650-660. DOI: 10.1104/pp.16.00984

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: 10.1094/MPMI-09-10-0196

Sinha D, Gupta MK, Patel HK, Ranjan A, Sonti RV (2013). Cell wall degrading enzyme induced rice innate immune responses are suppressed by the type 3 secretion system effectors XopN, XopQ, XopX and XopZ of Xanthomonas oryzae pv. oryzae. PLoS One 8: e75867. DOI: 10.1371/journal.pone.0075867

Stork W, Kim JG, Mudgett MB (2015). Functional analysis of plant defense suppression and activation by the Xanthomonas core type III effector XopX. Mol. Plant. Microbe Interact. 28: 180-194. DOI: 10.1094/MPMI-09-14-0263-R