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--- bacteria:t3e:xopq [2020/07/03 19:25]
rkoebnik
+++ bacteria:t3e:xopq [2021/01/05 17:25] (current)
rkoebnik [References]
@@ Line 7: / Line 7: @@
 Class: XopQ\\
 Family: XopQ\\
-Prototype: XCV4438: Xanthomonas outer protein Q from //Xanthomonas euvesicatoria// pv. //euvesicatoria// strain 85-10 (aka //X. campestris// pv. //vesicatoria//, //Xcv//)\\
+Prototype: XCV4438 (//Xanthomonas euvesicatoria// pv. //euvesicatoria//, ex //Xanthomonas campestris// pv. //vesicatoria//; strain 85-10)\\
 RefSeq ID: [[https://www.ncbi.nlm.nih.gov/protein/WP_011349176.1|WP_011349176.1]] (464 aa)\\
 D structure: [[https://www.rcsb.org/structure/4kl0|4KL0]] (Yu //et al.//, 2013); [[https://www.rcsb.org/structure/4P5F|4P5F]] (Yu //et al.//, 2014)
 ===== Biological function =====
 === How discovered? ===
-XopQ was 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 XopQ::AvrBs2 fusion protein triggered a //Bs2//-dependent hypersensitive response (HR) in pepper leaves (Roden //et al//., 2004). XopQ was also identified in //X. campestris// pv. //campestris// (//Xcc//) strain 8004 as a candidate T3E due to the presence of a plant-inducible promoter (PIP) box in its gene, XC_3177 (Jiang //et al.//, 2009).
+XopQ was 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 //X. campestris// pv. //vesicatoria// (//Xcv//)strain 85-10. The XopQ::AvrBs2 fusion protein triggered a //Bs2//-dependent hypersensitive response (HR) in pepper leaves (Roden //et al//., 2004). XopQ was also identified in //X. campestris// pv. //campestris// (//Xcc//) strain 8004 as a candidate T3E due to the presence of a plant-inducible promoter (PIP) box in its gene, XC_3177 (Jiang //et al.//, 2009).
 === (Experimental) evidence for being a T3E ===
@@ Line 32: / Line 33: @@
   * Mutations of two potential active site residues, D116 and Y279, resulted in //Xoo//  mutants with reduced virulence on rice and reduced hypersensitive response (HR) on //Nicotiana benthamiana//, a nonhost. However, Arabidopsis lines expressing either xopQ or //xopQ// <sub>Y279A</sub>  were equally proficient at suppression of LipA-induced callose deposition (Gupta //et al.//, 2015).
   * Compatibility studies with //X. euvesicatoria//  pv. //perforans//  revealed that a double deletion of //avrBsT//  and //xopQ//  allows a host range expansion for //Nicotiana benthamiana//  (Schwartz //et al.//, 2015).
-  * XopQ mediated cell death suppression in //N. benthamiana//  during transient expression assays was later shown to result from an attenuation of //Agrobacterium//  ‐mediated protein expression rather than the reflecting a genuine XopQ virulence activity (Adlung & Bonas, 2017).
+  * The avirulence activity of XopQ derivatives did not correlate with macroscopically visible plant reactions upon transient expression in //N. benthamiana//. It was therefore speculated that //N. benthamiana//  might encode two resistance proteins for the recognition of XopQ (Adlung, 2016).
+  * Transient co-expression of XopQ::GFP and XopS::GFP in //N. benthamiana//  triggered cell death reactions, which were not observed when each effector was expressed alone. Bimolecular fluorescence complementation using split-YFP derivatives revealed that XopQ and XopS co-localize in the nucleus. These results suggested that both effectors may form a protein-protein complex i//n planta //  (Adlung, 2016).
+  * XopQ suppressed cell death reactions in //N. benthamiana//  that were triggered by three //Xcv//  type III effectors (XopB, XopJ, XopL), whereas cell death reactions triggered by AvrBsT were not suppressed by XopQ (Adlung, 2016).
+  * XopQ-mediated cell death suppression in //N. benthamiana//  during transient expression assays was later shown to result from an attenuation of //Agrobacterium//  ‐mediated protein expression rather than reflecting a genuine XopQ virulence activity (Adlung & Bonas, 2017).
   * A Δ//xopN//–Δ//xopQ //double knock-out mutant in //X. phaseoli//  pv. //manihotis//  (//Xpm//) was less aggressive in the cassava host plant than its single mutation counterparts. In addition, //in planta //  bacterial growth was reduced at 5 dpi in the double mutant with respect to the wild-type strain CIO151 and individual knock-out strains. The phenotype of the double mutant could be complemented when transforming a plasmid containing //xopQ//. These results confirmed that //xopN //and// xopQ //are functionally redundant in //Xpm//  (Medina //et al.//, 2017).
   * A reverse genetics screen identified Recognition of XopQ 1 (Roq1), a nucleotide-binding leucine-rich repeat (NLR) protein with a Toll-like interleukin-1 receptor (TIR) domain, which mediates XopQ recognition in //N. benthamiana//. Roq1 orthologs appear to be present only in the //Nicotiana//  genus. Expression of Roq1 was found to be sufficient for XopQ recognition in both the closely-related //Nicotiana sylvestris//  and the distantly-related beet plant (//Beta vulgaris//) (Schultink //et al.//, 2017).
   * Roq1 is able to recognize XopQ alleles from various //Xanthomonas//  species, as well as HopQ1 from //Pseudomonas//, demonstrating widespread potential application in protecting crop plants from these pathogens (Schultink //et al.//, 2017).
+  * The coiled-coil NLR protein N requirement gene 1 (NRG) interacts with EDS1 and acts downstream of Roq1 and EDS1 to mediate XopQ/HopQ1-triggered ETI. In addition, Roq1, EDS1, and NRG1 mediate XopQ-triggered transcriptional changes in //N. benthamiana//  and regulate resistance to //Xanthomonas//  and //Pseudomonas//  species that carry the effectors XopQ or HopQ1. This study suggests that NRG1 may be a conserved key component in TNL-mediated signaling pathways (Qi //et al.//, 2018).
+  * Roq1 is also involved in the recognition of RipB, the homolog of XopQ in //Ralstonia solanacearum//: The RipB‐induced resistance against //R. solanacearum//  was abolished in Roq1‐silenced plants (Nakano & Mukaihara, 2019).
   * Effectors that interact with 14–3–3 proteins may provide plant-pathogenic bacteria with the ability to modulate PTI as well as ETI. Suppression of immune responses induced by a //xopN//–//xopQ//–//xopX//–//xopZ//  quadruple mutant by the XopQ effector may be both suppression of ETI as well as suppression of DTI (damage-triggered immunity) caused by the release of DAMPs by the quadruple mutant strain (Deb //et al//., 2019).
+  * Roq1 was found to confer immunity to //Xanthomonas//  (containing XopQ), //P. syringae//  (containing the XopQ homolog HopQ1), and //Ralstonia//  (containing the XopQ homolog RipB) when expressed in tomato (Thomas //et al.//, 2020).
+  * Strong resistance to //Xanthomonas euvesicatoria//  pv. //perforans//  was observed with transgenic tomato plants expressing Roq1 from //N. benthamiana//  in three seasons of field trials with both natural and artificial inoculation. The Roq1 gene can therefore be used to provide safe, economical, and effective control of these pathogens in tomato and other crop species and reduce or eliminate the need for traditional chemical controls (Thomas //et al.//, 2020).
+  * 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).
 === Localization ===
@@ Line 52: / Line 62: @@
 === Interaction partners ===
-Using protein-protein interaction studies in yeast and in planta, XopQ<sub>Xcv</sub>  was shown to physically interacts with the 14–3–3 protein TFT4 from tomato (//Solanum lycopersicum//) (Teper //et al.//, 2014). Yeast 2-hybrid assays revealed that XopQ<sub>Xcv</sub>  interacts with multiple, but perhaps not all 14–3–3 protein isoforms. A mutation in the putative 14–3–3 binding site of XopQ (S65A) impaired interaction of the effector with TFT4 from pepper and tomato (//Capsicum annuum//) and its virulence function //in planta//.
+Using protein-protein interaction studies in yeast and in planta, XopQ<sub>Xcv</sub>  was shown to physically interacts with the 14–3–3 protein TFT4 from tomato (//Solanum lycopersicum//) (Teper //et al.//, 2014). A mutation in the putative 14–3–3 binding site of XopQ (S65A) impaired interaction of the effector with TFT4 from pepper and tomato (//Capsicum annuum//) and its virulence function //in planta//  (Teper //et al.//, 2014). Yeast 2-hybrid assays revealed that XopQ<sub>Xcv</sub>  interacts with multiple, but perhaps not all 14–3–3 protein isoforms (Teper //et al.//, 2014; Dubrov //et al.//, 2018).
+Bimolecular fluorescence complementation assays upon transient expression in //N. benthamiana//  using split-YFP derivatives revealed that XopQ may interact with itself and also with XopS, maybe forming a large protein complex i//n planta //  (Adlung, 2016).
 Roq1, a nucleotide-binding leucine-rich repeat (NLR) protein with a Toll-like interleukin-1 receptor (TIR) domain, was found to co-immunoprecipitate with XopQ, suggesting a physical association between the two proteins (Schultink //et al.//, 2017).
-XopQ<sub>Xoo</sub>  was shown to interact in yeast and in planta with two rice 14–3–3 proteins, Gf14f and Gf14g (Deb //et al//., 2019). A serine to alanine mutation (S65A) of a 14–3–3 interaction motif in XopQ abolished the ability of XopQ to interact with the two 14–3–3 proteins and to suppress innate immunity.
+XopQ<sub>Xoo</sub>  was shown to interact in yeast and i//n planta//  with two rice 14–3–3 proteins, Gf14f and Gf14g (Deb //et al//., 2019). A serine to alanine mutation (S65A) of a 14–3–3 interaction motif in XopQ abolished the ability of XopQ to interact with the two 14–3–3 proteins and to suppress innate immunity.
+Yeast two-hybrid, bimolecular fluorescence complementation (BiFC) and co-IP assays indicated that XopQ and XopX interact with each other (Deb et al., 2020).
 ===== Conservation =====
@@ Line 62: / Line 76: @@
 === In xanthomonads ===
-XopQ is a widely conserved across //Xanthomonas//  ssp., such as //X. campestris//,// X. citri//, //X. euvesicatoria//, //X. oryzae//  (Roden //et al//., 2004; Furutani et al., 2009; Hajri et al., 2009). Since the G+C content of the //xopQ//  gene is similar to that of the //Xcv////hrp//  gene cluster, it may be a member of a “core” group of //Xanthomonas//  spp. effectors (Roden //et al//., 2004).
+XopQ is a widely conserved across //Xanthomonas//  ssp., such as //X. campestris//,// X. citri//, //X. euvesicatoria//, //X. oryzae//  (Roden //et al//., 2004; Furutani et al., 2009; Hajri et al., 2009; Thomas //et al.//, 2020). Since the G+C content of the //xopQ//  gene is similar to that of the //Xcv////hrp//  gene cluster, it may be a member of a “core” group of //Xanthomonas//  spp. effectors (Roden //et al//., 2004).
 === In other plant pathogens/symbionts ===
-XopQ shares homology with the //Ralstonia solanacearum//  effector RipB and the //Pseudomonas syringae//  pv. //tomato//  effector HolPtoQ/HopQ (Roden //et al//., 2004; Büttner & Bonas, 2010).
+XopQ shares homology with the //Ralstonia solanacearum//  effector RipB and the //Pseudomonas syringae//  pv. //tomato//  effector HolPtoQ/HopQ (Roden //et al//., 2004; Büttner & Bonas, 2010). Unlike most recognized effectors, alleles of XopQ/HopQ1 are highly conserved and present in most plant-pathogenic strains of //Xanthomonas//  and //P. syringae//, and the homolog of XopQ/HopQ1, named RipB, is present in most Ralstonia strains (Thomas //et al.//, 2020).
 ===== References =====
-Adlung N (2016). Charakterisierung der Avirulenzaktivität von XopQ und Identifizierung möglicher Interaktoren von XopL aus //Xanthomonas campestris//  pv. //vesicatoria//. Doctoral Thesis. Martin-Luther-Universität Halle-Wittenberg, Germany. PDF: [[https://d-nb.info/1116951061/34|d-nb.info/1116951061/34]] FIXME
+Adlung N (2016). Charakterisierung der Avirulenzaktivität von XopQ und Identifizierung möglicher Interaktoren von XopL aus //Xanthomonas campestris// pv. //vesicatoria//. Doctoral Thesis. Martin-Luther-Universität Halle-Wittenberg, Germany. PDF: [[https://d-nb.info/1116951061/34|d-nb.info/1116951061/34]]
+Adlung N, Bonas U (2017). Dissecting virulence function from recognition: cell death suppression in //Nicotiana benthamiana// by XopQ/HopQ1-family effectors relies on EDS1-dependent immunity. Plant J. 91: 430-442. DOI: [[https://doi.org/10.1111/tpj.13578|10.1111/tpj.13578]]
-Adlung N, Bonas U (2017). Dissecting virulence function from recognition: cell death suppression in //Nicotiana benthamiana//  by XopQ/HopQ1-family effectors relies on EDS1-dependent immunity. Plant J. 91: 430-442. DOI: [[https://doi.org/10.1111/tpj.13578|10.1111/tpj.13578]]
+Adlung N, Prochaska H, Thieme S, Banik A, Blüher D, John P, Nagel O, Schulze S, Gantner J, Delker C, Stuttmann J, Bonas U (2016). Non-host resistance induced by the //Xanthomonas// effector XopQ is widespread within the genus //Nicotiana// and functionally depends on EDS1. Front. Plant Sci. 7: 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 (2016). Non-host resistance induced by the //Xanthomonas//  effector XopQ is widespread within the genus //Nicotiana//  and functionally depends on EDS1. Front. Plant Sci. 7: 1796. DOI: [[https://doi.org/10.3389/fpls.2016.01796|10.3389/fpls.2016.01796]]
+Büttner D, Bonas U (2010). Regulation and secretion of //Xanthomonas// virulence factors. FEMS Microbiol. Rev. 34: 107-133. DOI: [[https://doi.org/10.1111/j.1574-6976.2009.00192.x|10.1111/j.1574-6976.2009.00192.x]]
-Büttner D, Bonas U (2010). Regulation and secretion of //Xanthomonas//  virulence factors. FEMS Microbiol. Rev. 34: 107-133. DOI: [[https://doi.org/10.1111/j.1574-6976.2009.00192.x|10.1111/j.1574-6976.2009.00192.x]]
+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. 104: 332-350. DOI: [[https://doi.org/10.1111/tpj.14924|10.1111/tpj.14924]]
-Deb S, Gupta MK, Patel HK, Sonti RV (2019). //Xanthomonas oryzae//  pv. //oryzae//  XopQ protein suppresses rice immune responses through interaction with two 14-3-3 proteins but its phospho-null mutant induces rice immune responses and interacts with another 14-3-3 protein. Mol. Plant Pathol. 20: 976-989. DOI: [[https://doi.org/10.1111/mpp.12807|10.1111/mpp.12807]]
+Deb S, Gupta MK, Patel HK, Sonti RV (2019). //Xanthomonas oryzae// pv. //oryzae// XopQ protein suppresses rice immune responses through interaction with two 14-3-3 proteins but its phospho-null mutant induces rice immune responses and interacts with another 14-3-3 protein. Mol. Plant Pathol. 20: 976-989. DOI: [[https://doi.org/10.1111/mpp.12807|10.1111/mpp.12807]]
-Dubrow Z, Sunitha S, Kim JG, Aakre CD, Girija AM, Sobol G, Teper D, Chen YC, Ozbaki-Yagan N, Vance H, Sessa G, Mudgett MB (2018). Tomato 14-3-3 proteins are required for //Xv3//  disease resistance and interact with a subset of //Xanthomonas euvesicatoria //effectors. Mol. Plant Microbe Interact. 31: 1301-1311. DOI: [[https://doi.org/10.1094/MPMI-02-18-0048-R|10.1094/MPMI-02-18-0048-R]] FIXME
+Dubrow Z, Sunitha S, Kim JG, Aakre CD, Girija AM, Sobol G, Teper D, Chen YC, Ozbaki-Yagan N, Vance H, Sessa G, Mudgett MB (2018). Tomato 14-3-3 proteins are required for //Xv3// disease resistance and interact with a subset of //Xanthomonas euvesicatoria //effectors. Mol. Plant Microbe Interact. 31: 1301-1311. DOI: [[https://doi.org/10.1094/MPMI-02-18-0048-R|10.1094/MPMI-02-18-0048-R]]
-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]]
+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]]
-Gupta MK, Nathawat R, Sinha D, Haque AS, Sankaranarayanan R, Sonti RV (2015). Mutations in the predicted active site of //Xanthomonas oryzae//  pv. //oryzae//  XopQ differentially affect virulence, suppression of host innate immunity, and induction of the HR in a nonhost plant. Mol. Plant Microbe Interact. 28:195-206. DOI: [[https://doi.org/10.1094/MPMI-09-14-0288-R|10.1094/MPMI-09-14-0288-R]]
+Gupta MK, Nathawat R, Sinha D, Haque AS, Sankaranarayanan R, Sonti RV (2015). Mutations in the predicted active site of //Xanthomonas oryzae// pv. //oryzae// XopQ differentially affect virulence, suppression of host innate immunity, and induction of the HR in a nonhost plant. Mol. Plant Microbe Interact. 28:195-206. DOI: [[https://doi.org/10.1094/MPMI-09-14-0288-R|10.1094/MPMI-09-14-0288-R]]
 Hajri A, Brin C, Hunault G, Lardeux F, Lemaire C, Manceau C, Boureau T, Poussier S (2009). A "repertoire for repertoire" hypothesis: repertoires of type three effectors are candidate determinants of host specificity in //Xanthomonas//. PLoS One 4: e6632. DOI: [[https://doi.org/10.1371/journal.pone.0006632|10.1371/journal.pone.0006632]]
-Jiang W, Jiang B, Xu R, Huang J, Wei H, Jiang GF, Cen WJ, Liu J, Ge YY, Li GH, Su LL, Hang XH, Tang DJ, Lu GT, Feng JX, He YQ, Tang JL (2009). Identification of six type III effector genes with the PIP box in //Xanthomonas campestris//  pv. //campestris//  and five of them contribute individually to full pathogenicity. Mol. Plant Microbe Interact. 22: 1401-1411. DOI: [[https://doi.org/10.1094/MPMI-22-11-1401|10.1094/MPMI-22-11-1401]]
+Jiang W, Jiang B, Xu R, Huang J, Wei H, Jiang GF, Cen WJ, Liu J, Ge YY, Li GH, Su LL, Hang XH, Tang DJ, Lu GT, Feng JX, He YQ, Tang JL (2009). Identification of six type III effector genes with the PIP box in //Xanthomonas campestris// pv. //campestris// and five of them contribute individually to full pathogenicity. Mol. Plant Microbe Interact. 22: 1401-1411. DOI: [[https://doi.org/10.1094/MPMI-22-11-1401|10.1094/MPMI-22-11-1401]]
-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]]
-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]]
+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]]
-Nakano M, Mukaihara T (2019). The type III effector RipB from //Ralstonia solanacearum//  RS1000 acts as a major avirulence factor in //Nicotiana benthamiana//  and other //Nicotiana//  species. Mol. Plant Pathol. 20: 1237-1251. DOI: [[https://doi.org/10.1111/mpp.12824|10.1111/mpp.12824]] FIXME
+Nakano M, Mukaihara T (2019). The type III effector RipB from //Ralstonia solanacearum// RS1000 acts as a major avirulence factor in //Nicotiana benthamiana// and other //Nicotiana// species. Mol. Plant Pathol. 20: 1237-1251. DOI: [[https://doi.org/10.1111/mpp.12824|10.1111/mpp.12824]]
-Qi T, Seong K, Thomazella DPT, Kim JR, Pham J, Seo E, Cho MJ, Schultink A, Staskawicz BJ (2018). NRG1 functions downstream of EDS1 to regulate TIR-NLR-mediated plant immunity in //Nicotiana benthamiana//. Proc. Natl. Acad. Sci. USA 115: E10979-E10987. DOI: [[https://doi.org/10.1073/pnas.1814856115|10.1073/pnas.1814856115]] FIXME
+Qi T, Seong K, Thomazella DPT, Kim JR, Pham J, Seo E, Cho MJ, Schultink A, Staskawicz BJ (2018). NRG1 functions downstream of EDS1 to regulate TIR-NLR-mediated plant immunity in //Nicotiana benthamiana//. Proc. Natl. Acad. Sci. USA 115: E10979-E10987. DOI: [[https://doi.org/10.1073/pnas.1814856115|10.1073/pnas.1814856115]]
-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]]
+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]]
-Schultink A, Qi T, Lee A, Steinbrenner AD, Staskawicz B (2017). Roq1 mediates recognition of the //Xanthomonas//  and //Pseudomonas//  effector proteins XopQ and HopQ1. Plant J. 92: 787-795. DOI: [[https://doi.org/10.1111/tpj.13715|10.1111/tpj.13715]]
+Schultink A, Qi T, Lee A, Steinbrenner AD, Staskawicz B (2017). Roq1 mediates recognition of the //Xanthomonas// and //Pseudomonas// effector proteins XopQ and HopQ1. Plant J. 92: 787-795. DOI: [[https://doi.org/10.1111/tpj.13715|10.1111/tpj.13715]]
-Schwartz AR, Potnis N, Timilsina S, Wilson M, Patané J, Martins J Jr, Minsavage GV, Dahlbeck D, Akhunova A, Almeida N, Vallad GE, Barak JD, White FF, Miller SA, Ritchie D, Goss E, Bart RS, Setubal JC, Jones JB, Staskawicz BJ (2015). Phylogenomics of //Xanthomonas//  field strains infecting pepper and tomato reveals diversity in effector repertoires and identifies determinants of host specificity. Front. Microbiol. 6: 535. DOI: [[https://doi.org/10.3389/fmicb.2015.00535|10.3389/fmicb.2015.00535]]
+Schwartz AR, Potnis N, Timilsina S, Wilson M, Patané J, Martins J Jr, Minsavage GV, Dahlbeck D, Akhunova A, Almeida N, Vallad GE, Barak JD, White FF, Miller SA, Ritchie D, Goss E, Bart RS, Setubal JC, Jones JB, Staskawicz BJ (2015). Phylogenomics of //Xanthomonas// field strains infecting pepper and tomato reveals diversity in effector repertoires and identifies determinants of host specificity. Front. Microbiol. 6: 535. DOI: [[https://doi.org/10.3389/fmicb.2015.00535|10.3389/fmicb.2015.00535]]
-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: [[https://doi.org/10.1371/journal.pone.0075867|10.1371/journal.pone.0075867]]
+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: [[https://doi.org/10.1371/journal.pone.0075867|10.1371/journal.pone.0075867]]
-Teper D, SalomonD, Sunitha S, Kim JG, Mudgett MB, Sessa G. (2014). //Xanthomonas euvesicatoria//  type III effector XopQ interacts with tomato and pepper 14-3-3 isoforms to suppress effector-triggered immunity. Plant J. 77: 297-309. DOI: [[https://doi.org/10.1111/tpj.12391|10.1111/tpj.12391]]
+Teper D, SalomonD, Sunitha S, Kim JG, Mudgett MB, Sessa G. (2014). //Xanthomonas euvesicatoria// type III effector XopQ interacts with tomato and pepper 14-3-3 isoforms to suppress effector-triggered immunity. Plant J. 77: 297-309. DOI: [[https://doi.org/10.1111/tpj.12391|10.1111/tpj.12391]]
-Thomas NC, Hendrich CG, Gill US, Allen C, Hutton SF, Schultink A (2020). The immune receptor Roq1 confers resistance to the bacterial pathogens //Xanthomonas//, //Pseudomonas syringae//, and //Ralstonia//  in tomato. Front. Plant Sci. 11: 463. DOI: [[https://doi.org/10.3389/fpls.2020.00463|10.3389/fpls.2020.00463]] FIXME
+Thomas NC, Hendrich CG, Gill US, Allen C, Hutton SF, Schultink A (2020). The immune receptor Roq1 confers resistance to the bacterial pathogens //Xanthomonas//, //Pseudomonas syringae//, and //Ralstonia// in tomato. Front. Plant Sci. 11: 463. DOI: [[https://doi.org/10.3389/fpls.2020.00463|10.3389/fpls.2020.00463]]
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-Yu S, Hwang I, Rhee S (2014). The crystal structure of type III effector protein XopQ from //Xanthomonas oryzae//  complexed with adenosine diphosphate ribose. Proteins 82: 2910-2914. DOI: [[https://doi.org/10.1002/prot.24656|10.1002/prot.24656]]
+Yu S, Hwang I, Rhee S (2014). The crystal structure of type III effector protein XopQ from //Xanthomonas oryzae// complexed with adenosine diphosphate ribose. Proteins 82: 2910-2914. DOI: [[https://doi.org/10.1002/prot.24656|10.1002/prot.24656]]

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