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

Author: [[https://www.researchgate.net/profile/Fernando_Tavares|Fernando Tavares]]\\
Reviewer: [[https://www.researchgate.net/profile/Amandine_Cunty|Amandine Cunty]]

Class: XopR\\
Family: XopR\\
Prototype: XOO4134 (//Xanthomonas oryzae// pv. //oryzae//; strain T7174R)\\
GenBank ID: [[https://www.ncbi.nlm.nih.gov/protein/BAE70889.1|BAE70889.1 ]] (437 aa)\\
RefSeq ID: XopR [[https://www.ncbi.nlm.nih.gov/protein/WP_011260681.1|WP_011260681.1]] (437 aa)\\
3D structure: Unknown

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

=== How discovered? ===

//xopR// was firstly identified as a putative T3E ORF (XOO4134) shown to be under regulation of HrpX preceded by both a PIP box and a -10 box-like motif (Furutani //et al.//, 2006). Later, translocation of XOO4134::Cya fusion proteins into plant cells were shown to occur via a T3SS (Furutani //et al.//, 2009; White //et al.//, 2009).
=== (Experimental) evidence for being a T3E ===

Evidence for T3SS-dependent secretion and translocation of XopR into plant cells was mainly based on calmodulin-dependent adenylate cyclase (Cya) reporter assays of fusion proteins (Furutani //et al.//, 2009). XopR<sub>//Xoo// </sub> was confirmed to have a functional type III secretion signal using a reporter fusion with AvrBs1 (Zhao //et al.//, 2013).
=== Regulation ===

Functional studies using //hrp//-inducing and non-//hrp//-inducing media and reverse-transcriptase PCR in wild type and //X. oryzae// pv. //oryzae// (//Xoo//) ∆//hrpX// mutants showed that the expression of //xopR// is //hrpX// dependent (Verma //et al.//, 2019). These results are indirectly supported by previous findings showing that //Xoo// mutants deficient for //xrvB//, a gene coding for a repressor of //hrp// gene expression, leads to an increase of XopR secretion into plant cells (Kametani-Ikawa //et al.//, 2011).

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//) were significantly reduced in the //Xoo// Δ//xrvC// mutant compared with those in the wild-type strain PXO99<sup>A</sup>  , but this did not apply to //xopR// (Liu //et al.//, 2016).
=== Phenotypes ===

In the last few years a comprehensive body of experimental evidence has been gathered supporting a multiple action of XopR in hampering host plant defenses, namely by fostering bacterial growth //in planta//, and suppressing pathogen-associated molecular patterns (PAMP) triggered host plant immunity (PTI) (Akimoto-Tomiyama //et al.//, 2012; Wang //et al.//, 2016; Medina //et al.//, 2018; Verma //et al.//, 2018; Verma //et al.//, 2019).

A //xopR// deletion mutant in the Chinese //Xoo// strain 13751 showed a significant reduction in virulence in hybrid rice cv. Teyou63 compared to the wild type (Zhao //et al.//, 2013). However, the growth of the mutant in host plant rice was not affected. These results indicated that //xopR// was required for full virulence of //Xoo// strain 13751 by inducing rice disease tolerance (Zhao //et al.//, 2013).

Later studies suggested that XopR suppress PAMP-triggered stomatal closure in transgenic //Arabidopsis// expressing XopR (Wang //et al.//, 2016). More recently, when compared with a //Xoo// wild type strain, //xopR// deficient mutants (//Xoo// ∆//xopR//) infiltrated in rice leaves led to an increase of callose deposits, and a significant higher production of reactive oxygen species (ROS), namely of hydrogen peroxide (H<sub>2</sub> O<sub>2</sub>) and superoxide anion (O<sub>2<sup>-</sup>  </sub>), known as the main components of the plant oxidative burst (Verma //et al.//, 2018). Furthermore, reverse transcriptase expression analyses of eight rice genes linked to plant disease resistance (//BRI1//, //GST1//, //PR2//, //PR5//, //RAC1//, //SERK1//, //WRKY29// and //WRKY71//) were shown to be up-regulated in rice leaves inoculated with //Xoo// ∆//xopR// (Verma //et al.//, 2018; Verma //et al.//, 2019). To further support these findings, complementation of //Xoo// ∆//xopR// with //xopR// was able to restore the disease phenotype of the wild type Xoo strain (Verma //et al.//, 2018; Verma //et al.//, 2019).
=== Localization ===

Confocal microscopy studies of XopR::EYFP (enhanced yellow fluorescent protein) fusion protein transiently expressed in //Nicotiana benthaminiana//, suggested that XopR is localized to the plasma membrane of plant epidermal cells (Akimoto-Tomiyama //et al.//, 2012; Verma //et al.//, 2019). These results are further corroborate by findings assigning XopR localization to the plasma membrane of rice protoplasts, contrary to other effectors analysed, namely XopL XopV, XopC, and XopW, which were localized to the cytoplasm (Wang //et al.//, 2016).
=== Enzymatic function ===

Unknown.

=== Interaction partners ===

Co-immunoprecipitation assays indicate that XopR associates with various receptor-like cytoplasmic kinases (RLCKs), including BIK1 known to be involved in pathogen-associated molecular patterns (PAMP) to triggered stomatal closure (Wang //et al.//, 2016). //In vitro// kinase assays indicate that XopR is phosphorylated by BIK1 likely affecting BIK1 targets, and possibly impairing PAMP-triggered stomatal immunity (Wang //et al.//, 2016).
===== Conservation =====

=== In xanthomonads ===

Yes (e.g. //X. arboricola, X. axonopodis//, //X. campestris//, //X. citri//, //X. gardneri//, //X. oryzae//, //X. phaseoli//, //X. populi//, //X. vasicola//, //X. bromi//, //X. cucurbitae// inferred from a BlastP search for a query coverage higher than 90% and a percent identity over 35%).
=== In other plant pathogens/symbionts ===

Unknown.

===== References =====

Akimoto-Tomiyama C, Furutani A, Tsuge S, Washington EJ, Nishizawa Y, Minami E, Ochiai H (2012). XopR, a type III effector secreted by //Xanthomonas oryzae// pv. //oryzae//, suppresses microbe-associated molecular pattern-triggered immunity in //Arabidopsis thaliana//. Mol. Plant Microbe Interact. 25: 505-514. DOI: [[https://doi.org/10.1094/mpmi-06-11-0167|10.1094/mpmi-06-11-0167]]

Furutani A, Nakayama T, Ochiai H, Kaku H, Kubo Y, Tsuge S (2006). Identification of novel HrpXo regulons preceded by two //cis//-acting elements, a plant-inducible promoter box and a −10 box-like sequence, from the genome database of //Xanthomonas oryzae// pv. //oryzae//. FEMS Microbiol. Lett. 259: 133-141. DOI: [[https://doi.org/10.1111/j.1574-6968.2006.00265.x|10.1111/j.1574-6968.2006.00265.x]]

Furutani A, Takaoka M, Sanada H, Noguchi Y, Oku T, Tsuno K, Ochiai H, Tsuge S (2009). Identification of novel type III secretion effectors in //Xanthomonas oryzae// pv. //oryzae//. Mol. Plant Microbe Interact. 22: 96-106. DOI: [[https://doi.org/10.1094/mpmi-22-1-0096|10.1094/mpmi-22-1-0096]]

Kametani-Ikawa Y, Tsuge S, Furutani A, Ochiai H (2011). An H-NS-like protein involved in the negative regulation of //hrp// genes in //Xanthomonas oryzae// pv. //oryzae//. FEMS Microbiol. Lett. 319: 58-64. DOI: [[https://doi.org/10.1111/j.1574-6968.2011.02266.x|10.1111/j.1574-6968.2011.02266.x]]

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: [[https://doi.org/10.1093/femsle/fnw067|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: [[https://doi.org/10.1111/mpp.12545|10.1111/mpp.12545]]

Verma G, Sharma M, Mondal KK (2018). XopR TTSS-effector regulates //in planta// growth, virulence of Indian strain of //Xanthomonas oryzae// pv. //oryzae// via suppressing reactive oxygen species production and cell wall-associated rice immune responses during blight induction. Funct. Plant Biol. 45: 561-574. DOI: [[https://doi.org/10.1071/FP17147|10.1071/FP17147]]

Verma G, Mondal KK, Kulshreshtha A, Sharma M (2019). XopR T3SS-effector of //Xanthomonas oryzae// pv. //oryzae// suppresses cell death-mediated plant defense response during bacterial blight development in rice. 3 Biotech. 9: 272. DOI: [[https://doi.org/10.1007/s13205-019-1802-9|10.1007/s13205-019-1802-9]]

Wang S, Sun J, Fan F, Tan Z, Zou Y, Lu D (2016). A //Xanthomonas oryzae// pv. //oryzae// effector, XopR, associates with receptor-like cytoplasmic kinases and suppresses PAMP-triggered stomatal closure. Sci. China Life Sci. 59: 897-905. DOI: [[https://doi.org/10.1007/s11427-016-5106-6|10.1007/s11427-016-5106-6]]

White FF, Potnis N, Jones JB, Koebnik R (2009). The type III effectors of //Xanthomonas//. Mol. Plant Pathol. 10: 749-766. DOI: [[https://doi.org/10.1111/j.1364-3703.2009.00590.x|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: [[https://doi.org/10.1007/s11274-012-1229-5|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).
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