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====== The Type III Effector XopAP from //Xanthomonas// ======

Author: [[https://www.researchgate.net/profile/Saul_Burdman|Saul Burdman]]\\
Internal reviewer: [[https://www.researchgate.net/profile/Joel_Pothier2|Joël F. Pothier]]\\
Expert reviewer: [[https://www.researchgate.net/profile/Doron_Teper|Doron Teper]]

Class: XopAP\\
Family: XopAP\\
Prototype: XPE_1567 (//Xanthomonas euvesicatoria// pv. //perforans//; strain 91- 118) and XCV3138 (//Xanthomonas euvesicatoria// pv. //euvesicatoria//, ex //Xanthomonas campestris// pv. //vesicatoria//; strain 85-10)\\
GenBank ID (XPE_1567): [[https://www.ncbi.nlm.nih.gov/protein/AQS78154.1|AQS78154.1]] (358 aa)\\
GenBank ID (XCV3138): [[https://www.ncbi.nlm.nih.gov/protein/CAJ24869.1|CAJ24869.1]] (464 aa)\\
RefSeq ID: [[https://www.ncbi.nlm.nih.gov/protein/WP_236504155.1|WP_236504155.1]] (426 aa)\\
3D structure: Unknown

===== Biological function =====

=== How discovered? ===

XopAO was predicted to be a type 3 effector based on homology to Rip38, a predicted type 3 effector from //Ralstonia solanacearum// (Potnis //et al.//, 2011). XopAP ([[http://www.ncbi.nlm.nih.gov/protein/CAJ24869.1|XCV3138]] in //X. euvesicatoria// strain 85-10; GenBank [[https://www.ncbi.nlm.nih.gov/nuccore/AM039952.1|AM039952.1]]) was re-discovered using a machine-learning approach (Teper //et al//., 2016).
=== (Experimental) evidence for being a T3E ===

XopAP fused to the AvrBs2 reporter was shown to translocate into plant cells in an //hrpF//-dependent manner (Teper //et al//., 2016).

=== Regulation ===

The //xopAP// gene was shown to be induced in //X. citri// subsp. //citri// strain 306 in nutrient broth (Jalan //et al//., 2013). In //X. euvesicatoria// strain 85-10, the //xopAP// gene does not contain a PIP-box motif in its promoter region (Teper //et al//., 2016). //xopAP// in //X. citri// pv. //citri// is positively regulated by the stringent response regulators RelA and SpoT (Zhang et al. 2019).

=== Phenotypes ===

A //Xanthomonas euvesicatoria// strain 85-10 mutant defective in //xopAP// was compromised in induction of disease symptoms in leaves of susceptible pepper plants, relative to wild-type 85-10. This phenotype was associated with reduced ion leakage and higher chlorophyll content as compared with leaves inoculated with wild-type 85-10. No differences were observed between the //xopAP// mutant and wild-type 85-10 in their ability to colonize the leaves of susceptible pepper plants (Teper //et al//., 2016). //Agrobacterium//-mediated expression of XopAP in //Nicotiana benthamiana// caused a bleaching phenotype that was detected three days after agroinfiltration, and was reflected by reduced chlorophyll content. However, in these experiments, XopAP did not induce significant increase in ion leakage in the inoculated area (Teper //et al//., 2016). Results from this study indicate that XopAP acts as a virulence determinant in //X. euvesicatoria//, and contributes to the development of disease symptoms. A further study by Popov and colleagues (2018) revealed that XopAP was among the //X. euvesicatoria// 85-10 effectors that inhibited PAMP-triggered immunity, as assessed by inhibition of activation of a flg22-inducible reporter gene in //Arabidopsis// protoplasts (Popov //et al//., 2018). Expression of XopAP in an attenuated mutant of //Pseudomonas syringae// pv. //tomato// (DC3000 ΔCEL) increased its virulence on tomato. Also, the DC3000 ΔCEL strain carrying //xopAP// induced decreased callose deposition in //Arabidopsis// cell walls than the DC3000 ΔCEL strain (Popov //et al//., 2018). XopAP shares similarity with the //Ralstonia solanacearum// type III effector RipAL and both effectors possess a putative lipase domain (Peeters //et al//., 2013; Teper //et al//., 2016). //R. solanacearum// RipAL was shown to suppress salicylic acid-mediated defense responses and induce jasmonic acid production in //N. benthamiana// (Nakano & Mukaihara, 2018). Mutations in the putative catalytic residues within the lipase-like domain of RipAL abolished these activities (Nakano & Mukaihara, 2018).

Virulence and infection of //X. oryzae// pv. //oryzicola// (//Xoc//) increased in transgenic rice (//Oryza sativa// L.) plants overexpressing //xopAP//. XopAP inhibited the acidification of vacuoles by competing with vacuolar H<sup>+</sup>-pyrophosphatase (V-PPase) for binding to PtdIns(3,5)P<sub>2</sub> , leading to stomatal opening. Transgenic rice overexpressing XopAP also showed inhibition of stomatal closure when challenged by //Xoc// infection and treatment with the PAMP flg22. Moreover, XopAP suppressed flg22-induced gene expression, reactive oxygen species burst and callose deposition in host plants, demonstrating that XopAP subverts PAMP-triggered immunity during //Xoc// infection. Taken together, these findings demonstrated that XopAP overcomes stomatal immunity in plants by binding to lipids (Liu //et al.//, 2022).
=== Localization ===

Unknown. Subcellular localization analyses of the //R. solanacearum// homolog, RipAL, suggested that RipAL localizes to chloroplasts and targets chloroplast lipids in plant cells (Nakano & Mukaihara, 2018).
=== Enzymatic function ===

Unknown. XopAP contains a putative lipase domain (lipase class 3 family domain; conserved protein domain family [[https://www.ncbi.nlm.nih.gov/Structure/cdd/cddsrv.cgi?uid=PLN03037|PLN03037]]) in amino acid positions 236-322 (Teper //et al//., 2016).
=== Interaction partners ===

XopAP was found to bind to phosphatidylinositol 3,5-bisphosphate (PtdIns(3,5)P<sub>2</sub> ), a membrane phospholipid that functions in pH control in lysosomes, membrane dynamics, and protein trafficking (Liu //et al.//, 2022).
===== Conservation =====

=== In xanthomonads ===

Yes (//e.g.,// //X. campestris//, X//. axonopodis//, //X. perforans//, X//. citri, X. alfalfae//, //X. prunicola//, //X. phaseoli//, //X. hortorum//, //X. arboricola//, //X. translucens//, //X. oryzae//, //X. hyacinthi, X. transluscens//) (e.g Potnis //et al//., 2011; Jalan et al., 2013; Peng //et al//., 2016; Constantin //et al//., 2017).
=== In other plant pathogens/symbionts ===

Yes (//Ralstonia solanacearum,// plant-pathogenic //Acidovorax// species, //Brenneria rubrifaciens//, //Robbsia andropogonis//).
===== References =====

Constantin EC, Haegeman A, Van Vaerenbergh J, Baeyen S, Van Malderghem C, Maes M, Cottyn B (2017). Pathogenicity and virulence gene content of //Xanthomonas// strains infecting Araceae, formerly known as //Xanthomonas axonopodis// pv. //dieffenbachiae//. Plant Pathol. 66: 1539-1554. DOI: [[https://doi.org/10.1111/ppa.12694|10.1111/ppa.12694]]

Jalan N, Kumar D, Andrade MO, Yu F, Jones JB, Graham JH, White FF, Setubal JC, Wang N (2013). Comparative genomic and transcriptome analyses of pathotypes of //Xanthomonas citri// subsp. //citri// provide insights into mechanisms of bacterial virulence and host range. BMC Genomics 14: 551. DOI: [[https://doi.org/10.1186/1471-2164-14-551|10.1186/1471-2164-14-551]]

Liu L, Li Y, Xu Z, Chen H, Zhang J, Manion B, Liu F, Zou L, Fu ZQ, Chen G (2022). The //Xanthomonas// type III effector XopAP prevents stomatal closure by interfering with vacuolar acidification. J. Integr. Plant Biol. 64: 1994-2008. DOI: [[https://doi.org/10.1111/jipb.13344|10.1111/jipb.13344]]

Nakano M, Mukaihara T (2018). //Ralstonia solanacearum// type III effector RipAL targets chloroplasts and induces jasmonic acid production to suppress salicylic acid-mediated responses in plants. Plant Cell Physiol. 59: 2576-2589. DOI: [[https://doi.org/10.1093/pcp/pcy177|10.1093/pcp/pcy177]]

Peeters N, Carrere S, Anisimova M, Plener L, Cazale AC, Genin S (2013). Repertoire, unified nomenclature and evolution of the type III effector gene set in the //Ralstonia solanacearum// species complex. BMC Genomics 14: 859. DOI: [[https://doi.org/10.1186/1471-2164-14-859|10.1186/1471-2164-14-859]]

Peng, Z., Hu, Y., Xie, J., Potnis N, Akhunova A, Jones J, Liu Z, White FJ, Liu S (2016). Long read and single molecule DNA sequencing simplifies genome assembly and TAL effector gene analysis of //Xanthomonas translucens//. BMC Genomics 17: 21. DOI: [[https://doi.org/10.1186/s12864-015-2348-9|10.1186/s12864-015-2348-9]]

Popov G, Fraiture M, Brunner F, Sessa G (2018). Multiple //Xanthomonas euvesicatoria// type III effectors inhibit flg22-triggered immunity. Mol. Plant Microbe Interact. 29: 651-660. DOI: [[https://doi.org/10.1094/MPMI-07-16-0137-R|10.1094/MPMI-07-16-0137-R]]

Potnis N, Krasileva K, Chow V, Almeida NF, Patil PB, Ryan RP, Sharlach M, Behlau F, Dow JM, Momol M, White FF, Preston JF, Vinatzer BA, Koebnik R, Setubal JC, Norman DJ, Staskawicz BJ, Jones JB (2011). Comparative genomics reveals diversity among xanthomonads infecting tomato and pepper. BMC Genomics 12: 146. DOI: [[https://doi.org/10.1186/1471-2164-12-146|10.1186/1471-2164-12-146]]

Teper D, Burstein D, Salomon D, Gershovitz M, Pupko T, Sessa G (2016). Identification of novel //Xanthomonas euvesicatoria// type III effector proteins by a machine-learning approach. Mol. Plant Pathol. 17: 398-411. DOI: [[https://doi.org/10.1111/mpp.12288|10.1111/mpp.12288]]

Zhang Y, Teper D, Xu J, Wang N (2019). Stringent response regulators (p)ppGpp and DksA positively regulate virulence and host adaptation of //Xanthomonas citri//. Mol. Plant Pathol. 20:1550-1565. DOI: [[https://bsppjournals.onlinelibrary.wiley.com/doi/full/10.1111/mpp.12865|10.1111/mpp.12865. ]]

===== Acknowledgements =====

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