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--- bacteria:t3e:xopc [2020/07/03 16:41] – rkoebnik
+++ bacteria:t3e:xopc [2025/02/12 23:50] (current) – jfpothier
@@ Line 1: / Line 1: @@
-====== XopC ======
+====== The Type III Effector XopC from //Xanthomonas// ======
 Author: [[https://www.researchgate.net/profile/Alice_Castaing|Alice Boulanger]]\\
-Internal reviewer: [[https://www.researchgate.net/profile/Ralf_Koebnik|Ralf Koebnik]]\\
+Internal reviewer: [[https://www.researchgate.net/profile/Ralf_Koebnik|Ralf Koebnik]]
-Expert reviewer: FIXME
 Class: XopC\\
-Family: XopC\\
+Families: XopC1 and XopC2\\
-Prototype: XopC (XCV2435) [//Xanthomonas euvesicatoria// pv. //euvesicatoria// aka //Xanthomonas campestris// pv. //vescicatoria//; strain 85-10 (//Xcv//)]\\
+Prototype (XopC1): XCV2435 (//Xanthomonas euvesicatoria// pv. //euvesicatoria//, ex //Xanthomonas campestris// pv. //vesicatoria//; strain 85-10)\\
-RefSeq ID: [[https://www.ncbi.nlm.nih.gov/protein/CAJ24112.1|CAJ24112.1]] (834 aa)\\
+GenBank ID (XopC1): [[https://www.ncbi.nlm.nih.gov/protein/CAJ24112.1|CAJ24112.1]] (834 aa)\\
-D structure: Unknown
+Prototype (XopC2): XOC_1264 (//Xanthomonas oryzae// pv. //oryzicola//; strain BLS256)\\
+GenBank ID (XopC2): [[https://www.ncbi.nlm.nih.gov/protein/AEQ95452.1|AEQ95452.1]] (549 aa - likely too short)\\
+GenBank ID (XopC2; strain GX01): [[https://www.ncbi.nlm.nih.gov/protein/QEO98660.1|QEO98660.1]] (596 aa)\\
+RefSeq ID (XopC1): [[https://www.ncbi.nlm.nih.gov/protein/WP_011347616.1|WP_011347616.1]] (834 aa)\\
+RefSeq ID (XopC2): [[https://www.ncbi.nlm.nih.gov/protein/WP_041183113.1|WP_041183113.1]] (412 aa - likely too short)\\
+D structure: Unknown. XopC2 from //Xanthomonas axonopodis// pv. //punicae// is predicted to be a 661 amino-acids protein with 5 alpha helices and 17 beta strands. It has 21 protein binding and one helical transmembrane region of 18 amino acids (Mondal et al., 2020).
 ===== Biological function =====
@@ Line 15: / Line 19: @@
 === How discovered? ===
-XopC was discovered in //Xcv// in a cDNA-AFLP screen (Noël //et al//., 2001). XopC was also identified in a genetic screen, using a Tn//5//-based transposon construct harboring the coding sequence for the HR-inducing domain of AvrBs2, but devoid of the effectors' T3SS signal, that was randomly inserted into the genome of //Xcv //strain 85-10. The XopC::AvrBs2 fusion protein triggered a //Bs2//-dependent hypersensitive response (HR) in pepper leaves (Roden //et al//., 2004).
+XopC was discovered in //X. campestris// pv. //vesicatoria// (//Xcv//) in a cDNA-AFLP screen (Noël //et al//., 2001). XopC was also identified in a genetic screen, using a Tn//5//-based transposon construct harboring the coding sequence for the HR-inducing domain of AvrBs2, but devoid of the effectors' T3SS signal, that was randomly inserted into the genome of //Xcv//strain 85-10. The XopC::AvrBs2 fusion protein triggered a //Bs2//-dependent hypersensitive response (HR) in pepper leaves (Roden //et al//., 2004).
 === (Experimental) evidence for being a T3E ===
@@ Line 27: / Line 31: @@
 The //xopC// gene was shown to be expressed in a //hrpG//- and //hrpX//-dependent manner. No PIP box was identified in the promoter region (Noël //et al//., 2001; Noël //et al//., 2003).
-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 //xopC//, were significantly reduced in the //Xanthomonas oryzae// pv. //oryzae// Δ//xrvC// mutant compared with those in the wild-type strain PXO99<sup>A</sup>  (Liu //et al.//, 2016).
+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 //xopC//, were significantly reduced in the //Xanthomonas oryzae// pv. //oryzae// Δ//xrvC// mutant compared with those in the wild-type strain PXO99<sup>A</sup> (Liu //et al.//, 2016).
 === Phenotypes ===
-  * A deletion of //xopC//  did not affect pathogenicity or bacterial growth in plants (Noël //et al//., 2003).
+  * A deletion of //xopC// did not affect pathogenicity or bacterial growth in plants (Noël //et al//., 2003).
-  * Roden et al. did not find significant growth defects of a //Xcv//  Δ//xopC//  mutant in susceptible pepper and tomato leaves (Roden et al., 2004)
+  * Roden et al. did not find significant growth defects of a //Xcv// Δ//xopC// mutant in susceptible pepper and tomato leaves (Roden //et al.//, 2004)
-  * Later, 86 //Solanaceae//  lines mainly of the genus //Nicotiana//  were screened for phenotypical reactions after //Agrobacterium tumefaciens//-mediated transient expression of 21 different //Xcv//  effectors. Transient expression of XopC exclusively induced plant reactions in lines of the genus //Solanum//  (Adlung //et al//., 2006). //Xcv//  85-10 strain deleted for //xopC//  induced weaker reactions than the wild type in //S. americanum//, which could be complemented by ectopic expression of //xopC//. Deletion of //xopC//  did not aﬀect visible reactions in //N. benthamiana//  and //N. tabacum//  to infection with //Xcv//. Thus, XopC contributes to //Xcv//-induced phenotypes in certain non-host plants (Adlung //et al//., 2006).
+  * Later, 86 //Solanaceae// lines mainly of the genus //Nicotiana// were screened for phenotypical reactions after //Agrobacterium tumefaciens//-mediated transient expression of 21 different //Xcv// effectors. Transient expression of XopC exclusively induced plant reactions in lines of the genus //Solanum// (Adlung //et al//., 2006). //Xcv// 85-10 strain deleted for //xopC// induced weaker reactions than the wild type in //S. americanum//, which could be complemented by ectopic expression of //xopC//. Deletion of //xopC// did not aﬀect visible reactions in //N. benthamiana// and //N. tabacum// to infection with //Xcv//. Thus, XopC contributes to //Xcv//-induced phenotypes in certain non-host plants (Adlung //et al//., 2006).
-  * The absence of //xopC//  in the genome of //Xcv//  led to an accelerated AvrBs1-induced HR in resistant pepper plants, if the plants were additionally stressed by exogenous application of salicylic acid (SA). This phenotype was complemented by //xopC//, but not by a //xopC//  derivative carrying a mutation in the predicted HAD-like hydrolase sequence (Herzfeld, 2013).
+  * The absence of //xopC// in the genome of //Xcv// led to an accelerated AvrBs1-induced HR in resistant pepper plants, if the plants were additionally stressed by exogenous application of salicylic acid (SA). This phenotype was complemented by //xopC//, but not by a //xopC// derivative carrying a mutation in the predicted HAD-like hydrolase sequence (Herzfeld, 2013).
-  * Virus-induced gene silencing (VIGS) of OAS-TL in planta abolished the acceleration of AvrBs1-mediated HR formation induced by the absence of //xopC//  in //Xcv//  in resistant pepper plants dependent on SA. These data suggest, that the induction of the AvrBs1-dependent HR in resistant pepper plants is SA-stress dependently delayed by XopC, which is reliant on a HAD-like hydrolase domain in XopC. This delay is mediated by the XopC plant interaction partner OAS-TL. Furthermore, expression analysis showed an increased accumulation of β-1,3-Glucanase transcript in //Xcv//-infected, resistant pepper plants by the presence of //xopC//. These findings indicated that XopC influences different mechnisms of the plant metabolism (Herzfeld, 2013).
+  * Virus-induced gene silencing (VIGS) of OAS-TL in planta abolished the acceleration of AvrBs1-mediated HR formation induced by the absence of //xopC// in //Xcv// in resistant pepper plants dependent on SA. These data suggest, that the induction of the AvrBs1-dependent HR in resistant pepper plants is SA-stress dependently delayed by XopC, which is reliant on a HAD-like hydrolase domain in XopC. This delay is mediated by the XopC plant interaction partner OAS-TL. Furthermore, expression analysis showed an increased accumulation of β-1,3-Glucanase transcript in //Xcv//-infected, resistant pepper plants by the presence of //xopC//. These findings indicated that XopC influences different mechnisms of the plant metabolism (Herzfeld, 2013).
+  * XopC2 of //X. citri// pv. //punicae// was found to contribute to the bacterial blight development on pomegranate fruit plants. Xap //ΔxopC2// was demonstrated to cause reduced the blight lesions when inflitrated on pomegranate leaves, induce defense responses like callose deposition, ROS production and upregulate immune-responsive genes in its natural host plants (Mondal //et al.//, 2020).
+  * Ectopic expression of XopC2 was found to promote jasmonate signaling and stomatal opening in transgenic rice plants, which were more susceptible to //X. oryzae// pv. //oryzicola// infection (Wang //et al.//, 2021).
 === Localization ===
-XopC localises to the plant cell cytoplasm and the nucleus (Herzfeld, 2013).
+XopC localises to the plant cell cytoplasm (Mondal //et al.//, 2020) and the nucleus (Herzfeld, 2013).
 === Enzymatic function ===
-XopC contains a predicted phosphoribosyl transferase domain and a putative haloacid dehalogenase (HAD)-like hydrolase domain in its C-terminal end. Phenotype of point mutation in catalytic domain have shown that HAD-like hydrolase activity is required for the XopC deleterious effect in yeast (Salomon //et al//., 2011).
+XopC contains a predicted phosphoribosyl transferase domain and a putative haloacid dehalogenase (HAD)-like hydrolase domain in its C-terminal end. Phenotype of point mutation in catalytic domain have shown that HAD-like hydrolase activity is required for the XopC deleterious effect in yeast (Salomon //et al//., 2011). XopC2 represents a family of atypical kinases that specifically phosphorylate OSK1, a universal adaptor protein of the Skp1-Cullin-F-box ubiquitin ligase complexes (Wang //et al.//, 2021).
 === Interaction partners ===
-Yeast-2-hybrid studies revealed a XopC interactor, which also interacted with XopC in planta. The interactor localises to the plant cell cytoplasm and carries typical features of plant cytosolic O-acetylserine (thiol)lyases (OAS-TL). It shows OAS-TL activity in vivo and in vitro. The latter one is enhanced by adding XopC (Herzfeld, 2013).
+Yeast-2-hybrid studies revealed a XopC interactor, which also interacted with XopC //in planta//. The interactor localises to the plant cell cytoplasm and carries typical features of plant cytosolic //O//-acetylserine (thiol)lyases (OAS-TL). It shows OAS-TL activity //in vivo// and //in vitro//. The latter one is enhanced by adding XopC (Herzfeld, 2013).
 ===== Conservation =====
@@ Line 52: / Line 58: @@
 === In xanthomonads ===
-Close, full-length homologs (>90% sequence identity) of XopC1 have only been found in several strains of clade-2 xanthomonads, such as //X. citri//, //X. euvesicatoria//, //X. fragariae//, //X. gardneri//, //X. hortorum//, and //X. phaseoli//  (BLASTP and TBLASTN performed in June 2020).
+Close, full-length homologs (>90% sequence identity) of XopC1 have only been found in several strains of clade-2 xanthomonads, such as //X. citri//, //X. euvesicatoria//, //X. fragariae//, //X. gardneri//, //X. hortorum//, and //X. phaseoli// (BLASTP and TBLASTN performed in June 2020).
-The distantly related XopC2 has homologs in //X. citri//, //X. euvesicatoria//, //X. oryzae//, //X. phaseoli//, and //X. translucens//  (BLASTP and TBLASTN performed in June 2020)
+The distantly related XopC2 has homologs in //X. citri//, //X. axonopodis//, //X. euvesicatoria//, //X. oryzae//, //X. phaseoli//, and //X. translucens// (BLASTP and TBLASTN performed in June 2020)
 === In other plant pathogens/symbionts ===
-XopC1: //Ralstonia solanacearum//  (RipC2), //Trinickia caryophylli//  (//Paraburkholderia caryophylli//), //Xylophilus ampelinus//  (BLASTP and TBLASTN performed in June 2020).
+XopC1: //Ralstonia solanacearum// (RipC2), //Trinickia caryophylli// (//Paraburkholderia caryophylli//), //Xylophilus ampelinus// (BLASTP and TBLASTN performed in June 2020).
-XopC2: //Acidovorax//  ssp., //Pseudomonas cissicola//, //Ralstonia solanacearum//  (RipC1) (BLASTP and TBLASTN performed in June 2020).
+XopC2: //Acidovorax// ssp., //Pseudomonas cissicola//, //Ralstonia solanacearum// (RipC1) (BLASTP and TBLASTN performed in June 2020).
+===== Conservation =====
+=== In xanthomonads ===
+Close, full-length homologs (>90% sequence identity) of XopC1 have only been found in several strains of clade-2 xanthomonads, such as //X. citri//, //X. euvesicatoria//, //X. fragariae//, //X. gardneri//, //X. hortorum//, and //X. phaseoli// (BLASTP and TBLASTN performed in June 2020).
+The distantly related XopC2 has homologs in //X. citri//, //X. axonopodis//, //X. euvesicatoria//, //X. oryzae//, //X. phaseoli//, and //X. translucens// (BLASTP and TBLASTN performed in June 2020)
+=== In other plant pathogens/symbionts ===
+XopC1: //Ralstonia solanacearum// (RipC2), //Trinickia caryophylli// (//Paraburkholderia caryophylli//), //Xylophilus ampelinus// (BLASTP and TBLASTN performed in June 2020).
+XopC2: //Acidovorax// ssp., //Pseudomonas cissicola// [a pathovar of //Xanthomonas citri//], //Ralstonia solanacearum// (RipC1) (BLASTP and TBLASTN performed in June 2020).
 ===== References =====
-Adlung N, Prochaska H, Thieme S, Banik A, Blüher D, John P, Nagel O, Schulze S, Gantner J, Delker C, Stuttmann J, Bonas U (2006). Non-host resistance induced by the //Xanthomonas//  effector XopQ is widespread within the genus //Nicotiana//  and functionally depends on EDS1. Front. Plant Sci. 30: 1796. DOI: [[https://doi.org/10.3389/fpls.2016.01796|10.3389/fpls.2016.01796]]
+Adlung N, Prochaska H, Thieme S, Banik A, Blüher D, John P, Nagel O, Schulze S, Gantner J, Delker C, Stuttmann J, Bonas U (2006). Non-host resistance induced by the //Xanthomonas// effector XopQ is widespread within the genus //Nicotiana// and functionally depends on EDS1. Front. Plant Sci. 30: 1796. DOI: [[https://doi.org/10.3389/fpls.2016.01796|10.3389/fpls.2016.01796]]
-Büttner D, Lorenz C, Weber E, Bonas U (2006). Targeting of two effector protein classes to the type III secretion system by a HpaC- and HpaB-dependent protein complex from //Xanthomonas campestris//  pv. //vesicatoria//. Mol Microbiol. 59: 513-527. DOI: [[https://doi.org/10.1111/j.1365-2958.2005.04924.x|10.1111/j.1365-2958.2005.04924.x]]
+Büttner D, Lorenz C, Weber E, Bonas U (2006). Targeting of two effector protein classes to the type III secretion system by a HpaC- and HpaB-dependent protein complex from //Xanthomonas campestris// pv. //vesicatoria//. Mol Microbiol. 59: 513-527. DOI: [[https://doi.org/10.1111/j.1365-2958.2005.04924.x|10.1111/j.1365-2958.2005.04924.x]]
 Herzfeld EM (2013). Identifizierung und Charakterisierung von dem pflanzlichen Interaktionspartner OAS-TL des Typ-III-Effektors XopC. Doctoral Thesis, Martin-Luther-Universität Halle-Wittenberg, Germany. PDF: [[https://opendata.uni-halle.de/handle/1981185920/7783|opendata.uni-halle.de/handle/1981185920/7783]]
-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]]
+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]]
+Mondal KK, Soni M, Verma G, Kulshreshtha A, Mrutyunjaya S, Kumar R ( 2020). //Xanthomonas axonopodis// pv. //punicae// depends on multiple non-TAL (Xop) T3SS effectors for its coveted growth inside the pomegranate plant through repressing the immune responses during bacterial blight development. Microbiol Res. 240: 126560 DOI: [[https://doi.org/10.1016/j.micres.2020.126560|10.1016/j.micres.2020.126560]]
+Noël L, Thieme F, Gäbler J, Büttner D, Bonas U (2003). XopC and XopJ, two novel type III effector proteins from //Xanthomonas campestris// pv. vesicatoria. J. Bacteriol. 185: 7092-7102. DOI: [[https://doi.org/10.1128/jb.185.24.7092-7102.2003|10.1128/jb.185.24.7092-7102.2003]]
+Noël L, Thieme F, Nennstiel D, Bonas U (2001). cDNA-AFLP analysis unravels a genome-wide //hrpG//-regulon in the plant pathogen //Xanthomonas campestris// pv. //vesicatoria//. Mol. Microbiol. 41: 1271-1281. DOI: [[https://doi.org/10.1046/j.1365-2958.2001.02567.x|10.1046/j.1365-2958.2001.02567.x]]
+Roden JA, Belt B, Ross JB, Tachibana T, Vargas J, Mudgett MB (2004). A genetic screen to isolate type III effectors translocated into pepper cells during //Xanthomonas// infection. Proc. Natl. Acad. Sci. USA 101: 16624-16629. DOI: [[https://doi.org/10.1073/pnas.0407383101|10.1073/pnas.0407383101]]
-Noël L, Thieme F, Gäbler J, Büttner D, Bonas U (2003). XopC and XopJ, two novel type III effector proteins from //Xanthomonas campestris//  pv. vesicatoria. J. Bacteriol. 185: 7092-7102. DOI: [[https://doi.org/10.1128/jb.185.24.7092-7102.2003|10.1128/jb.185.24.7092-7102.2003]]
+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: [[https://doi.org/10.1094/MPMI-09-10-0196|10.1094/MPMI-09-10-0196]]
-Noël L, Thieme F, Nennstiel D, Bonas U (2001). cDNA-AFLP analysis unravels a genome-wide //hrpG//-regulon in the plant pathogen //Xanthomonas campestris//  pv. //vesicatoria//. Mol. Microbiol. 41: 1271-1281. DOI: [[https://doi.org/10.1046/j.1365-2958.2001.02567.x|10.1046/j.1365-2958.2001.02567.x]]
+Szurek B, Rossier O, Hause G, Bonas U (2002). Type III-dependent translocation of the //Xanthomonas// AvrBs3 protein into the plant cell. Mol. Microbiol. 46: 13-23. DOI: [[https://doi.org/10.1046/j.1365-2958.2002.03139.x|10.1046/j.1365-2958.2002.03139.x]]
-Roden JA, Belt B, Ross JB, Tachibana T, Vargas J, Mudgett MB (2004). A genetic screen to isolate type III effectors translocated into pepper cells during //Xanthomonas//  infection. Proc. Natl. Acad. Sci. USA 101: 16624-16629. DOI: [[https://doi.org/10.1073/pnas.0407383101|10.1073/pnas.0407383101]]
+Wang S, Li S, Wang J, Li Q, Xin XF, Zhou S, Wang Y, Li D, Xu J, Luo ZQ, He SY, Sun W (2021). A bacterial kinase phosphorylates OSK1 to suppress stomatal immunity in rice. Nat. Commun.12: 5479. doi: [[https://doi.org/10.1038/s41467-021-25748-4|10.1038/s41467-021-25748-4]]
-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: [[https://doi.org/10.1094/MPMI-09-10-0196|10.1094/MPMI-09-10-0196]]
+===== Acknowledgements =====
-Szurek B, Rossier O, Hause G, Bonas U (2002). Type III-dependent translocation of the //Xanthomonas//  AvrBs3 protein into the plant cell. Mol. Microbiol. 46: 13-23. DOI:[[https://doi.org/10.1046/j.1365-2958.2002.03139.x|10.1016/j.jplph.2005.11.011]]
+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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