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bacteria:t3e:xopn [2020/08/09 15:31] – jvicentebacteria:t3e:xopn [2025/02/24 11:51] (current) – [Biological function] rkoebnik
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-====== XopN ======+====== The Type III Effector XopN from //Xanthomonas// ======
  
 Author: [[https://www.researchgate.net/profile/Jakub_Pecenka|Jakub Pečenka]]\\ Author: [[https://www.researchgate.net/profile/Jakub_Pecenka|Jakub Pečenka]]\\
-Internal reviewer: [[https://www.researchgate.net/profile/Joana_Vicente2|Joana G. Vicente]]\\ +Internal reviewer: [[https://www.researchgate.net/profile/Joana_Vicente2|Joana G. Vicente]]
-Expert reviewer: FIXME+
  
 Class: XopN\\ Class: XopN\\
 Family: XopN\\ Family: XopN\\
 Prototype: XopN (//Xanthomonas euvesicatoria// pv. //euvesicatoria//, ex //Xanthomonas campestris// pv. //vesicatoria//; strain 85-10)\\ Prototype: XopN (//Xanthomonas euvesicatoria// pv. //euvesicatoria//, ex //Xanthomonas campestris// pv. //vesicatoria//; strain 85-10)\\
-RefSeq ID: [[https://www.ncbi.nlm.nih.gov/protein/NP_643095|NP_643095]] (733 aa)\\+GenBank ID: [[https://www.ncbi.nlm.nih.gov/protein/AAV74202.1|AAV74202.1]] (733 aa)\\ 
 +RefSeq ID: [[https://www.ncbi.nlm.nih.gov/protein/WP_011348010.1|WP_011348010.1]] (733 aa)\\
 3D structure: unknown - similar to phosphatase 2a (pr65/A) (Roden //et al//., 2004). 3D structure: unknown - similar to phosphatase 2a (pr65/A) (Roden //et al//., 2004).
 +
 ===== Biological function ===== ===== Biological function =====
  
 === How discovered? === === How discovered? ===
  
-XopN 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 XopN::AvrBs2 fusion protein triggered a //Bs2//-dependent hypersensitive response (HR) in pepper leaves (Roden //et al//., 2004).+XopN 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 XopN::AvrBs2 fusion protein triggered a //Bs2//-dependent hypersensitive response (HR) in pepper leaves (Roden //et al//., 2004).
 === (Experimental) evidence for being a T3E === === (Experimental) evidence for being a T3E ===
  
-Type III-dependent secretion was confirmed using a calmodulin-dependent adenylate cyclase reporter assay, with a Δ//hrpF// mutant strain serving as negative control (Roden //et al.//, 2004).+Type III-dependent secretion was confirmed using a calmodulin-dependent adenylate cyclase reporter assay, with a Δ//hrpF// mutant strain serving as negative control (Roden //et al.//, 2004). 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 === === Regulation ===
  
-Start codon of //xopN// was found downstream if a conserved cis-regulatory element, the plant-inducible promoter (PIP) box (TTCGG-N15-TTCTG). //xopN// is regulated by //hrpX// and //hrpG// genes (Cheong //et al//., 2013; Jiang //et al//., 2008).+Start codon of //xopN// was found downstream of a conserved cis-regulatory element, the plant-inducible promoter (PIP) box (TTCGG-N15-TTCTG). //xopN// is regulated by //hrpX// and //hrpG// genes (Jiang //et al//., 2008; Cheong //et al//., 2013).
  
-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 //Xanthomonas oryzae// pv. //oryzae// Δ//xrvC// mutant compared with those in the wild-type strain PXO99<sup>A</sup>  , but this did not apply to //xopN// (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//) were significantly reduced in the //Xanthomonas oryzae// pv. //oryzae// Δ//xrvC// mutant compared with those in the wild-type strain PXO99<sup>A</sup> , but this did not apply to //xopN// (Liu //et al.//, 2016).
 === Phenotypes === === Phenotypes ===
  
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   * Its homolog XopN <sub>Xcc</sub>  was found as well to be required for full virulence on Chinese radish (Jiang //et al//., 2008).   * Its homolog XopN <sub>Xcc</sub>  was found as well to be required for full virulence on Chinese radish (Jiang //et al//., 2008).
   * XopN has been shown to play a role in host defence systems causing the reduction of PAMP-triggered immune responses and reduce the callose deposition in the host tissue. Moreover the deletion of //xopN//  open reading frame (ORF) reduced the //Xcv//  strain virulence exhibited by lower bacterial spot symptoms occurrence (Kim //et al//., 2009).   * XopN has been shown to play a role in host defence systems causing the reduction of PAMP-triggered immune responses and reduce the callose deposition in the host tissue. Moreover the deletion of //xopN//  open reading frame (ORF) reduced the //Xcv//  strain virulence exhibited by lower bacterial spot symptoms occurrence (Kim //et al//., 2009).
-  * XopN has been shown to be required for maximal pathogenicity of //X. axonopodis//  pv. //punicae//  (//Xap//) in pomegranate (Kumar and Mondal, 2013). The deletion of XopN from Xap caused higher accumulation of reactive oxygen species showing that XopN suppresses ROS-mdeiated defense responses during blight pathogenesis in pomegranate (Kumar //et al.//, 2016). +  * The role of XopN in X. oryzae pv. oryzae is dependent on leaf stage (Cheong et al., 2013). 
-  * 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). +  * XopN has been shown to be required for maximal pathogenicity of //X. axonopodis//  pv. //punicae//  (//Xap//) in pomegranate (Kumar and Mondal, 2013). The deletion of XopN from Xap caused higher accumulation of reactive oxygen species showing that XopN suppresses ROS-mediated defense responses during blight pathogenesis in pomegranate (Kumar //et al.//, 2016). 
-  * XopN was shown to contribute significantly to //X. oryzae//  pv. //oryzae//  (Xoo) virulence on a susceptible rice variety Nipponbare. XopN was shown to be highly translocated to suppress rice defense responses (Mo //et al.//, 2020).+  * 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). 
 +  * //Agrobacterium//  mediated transient transfer of the gene for XopN resulted in suppression of rice innate immune responses induced by LipA, a hydrolitic enzyme secreted by //X. oryzae//  pv. //oryzae//  (Xoo), but a //xopN// <sup>//-// </sup>   mutant of //Xoo//retains the ability to suppress these innate immune responses indicating other functionally redundant proteins; XopQ, XopX and XopZ were shown to be suppressors of LipA induced innate immune responses; mutation in any one of the //xopN, xopQ, xopX or xopZ//  genes causes partial virulence deficiency (Sinha et al., 2013). XopN was shown to contribute significantly to //X. oryzae//  pv. //oryzae//  (Xoo) virulence on a susceptible rice variety Nipponbare. XopN was shown to be highly translocated to suppress rice defense responses (Mo //et al.//, 2020). 
 +  * XopN and AvrBS2 were shown to significantly contribute to virulence of //X. oryzae//  pv. //oryzicola//  (Xoc GX01) (Liao //et al.//, 2020).
  
 === Localization === === Localization ===
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 === Enzymatic function === === Enzymatic function ===
  
-Unknown – Kim //et al//. (2009) did not confirm that XopN is an enzyme (Kim //et al//., 2009).+XopN binds TARK1, a tomato atypical receptor kinase required for PTI. Taylor //et al.//  (2012) showed that XopN promotes TARK1/TFT1 complex formation //in vitro//  and //in planta//  by functioning as a molecular scaffold.TFT proteins are involved in immune signaling during //X. euvesicatoria//  infection and can interact with multiple effectors including XopN (Dubrow //et al.//, 2018). TARK1 was shown to interact with proteins predicted to be associated with stomatal closure (Guzman et al., 2020). 
 + 
 +Three effectors (XopZ, XopN and XopV) were shown to be able to supress the peptidoglycan-triggered MAPK activation and a triple mutant of Xoo lacking these genes showed additively reduced virulence (Long et al., 2018).
  
 === Interaction partners === === Interaction partners ===
  
-XopN interact with two types of proteins in tomato: Tomato Atypical Receptor-like Kinase1 (TARK1) and four Tomato Fourteen-Three-Three isoforms (TFT1, TFT3, TFT5, and TFT6) (Kim //et al//., 2009).+XopN interact with two types of proteins in tomato: Tomato Atypical Receptor-like Kinase1 (TARK1) and four Tomato Fourteen-Three-Three isoforms (TFT1, TFT3, TFT5, and TFT6) (Kim //et al//., 2009). XopN interacts with the tomato 14-3-3 isoform TFT1 that functions in PTI and is a XopN virulence target (Taylor //et al.//, 2012). 
 + 
 +Two rice proteins, OsVOZ2 and a putative thiamine synthase (OsXNP) were identified as targets of XopN<sub>KXO85</sub>  by yeast two-hybrid screening (Cheong et al., 2012).
  
 ===== Conservation ===== ===== Conservation =====
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 === In xanthomonads === === In xanthomonads ===
  
-Yes (//e.g.//, //X. axonopodis//, //X//. //campestris//, //X//. //citri//,// X//. //oryzae//). Since the G+C content of the //xopN//  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).+Yes (//e.g.//, //X. axonopodis//, //X//. //campestris//, //X//. //citri//, //X//. //oryzae//). Since the G+C content of the //xopN// 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 === === In other plant pathogens/symbionts ===
  
-Yes (//e.g.//, //Pseudomonas//  spp.) (Kim //et al//., 2009).+Yes (//e.g.//, //Pseudomonas// spp.) (Kim //et al//., 2009).
  
 ===== References ===== ===== References =====
  
-Cheong H, Kim CY, Jeon JS, Lee BM, Sun Moon J, Hwang I (2013). //Xanthomonas oryzae//  pv. //oryzae//  type III effector XopN targets OsVOZ2 and a putative thiamine synthase as a virulence factor in rice. PloS ONE 8: e73346. DOI: [[https://doi.org/10.1371/journal.pone.0073346|10.1371/journal.pone.0073346]].+Cheong H, Kim CY, Jeon JS, Lee BM, Sun Moon J, Hwang I (2013). //Xanthomonas oryzae// pv. //oryzae// type III effector XopN targets OsVOZ2 and a putative thiamine synthase as a virulence factor in rice. PloS ONE 8: e73346. DOI: [[https://doi.org/10.1371/journal.pone.0073346|10.1371/journal.pone.0073346]]. 
 + 
 +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]] 
 + 
 +Guzman AR, Kim JG, Taylor KW, Lanver D, Mudgett MB (2020). Tomato Atypical Receptor Kinase1 is involved in the regulation of preinvasion defense. Plant Physiol. 183: 1306-1318. DOI: [[https://doi.org/10.1104/pp.19.01400|10.1104/pp.19.01400]] 
 + 
 +Jiang B, He Y, Cen W, Wei H, Jiang G, Jiang W, Hang X, Feng J, Lu G, Tang D, Tang J (2008). The type III secretion effector XopXccN of //Xanthomonas campestris// pv. //campestris// is required for full virulence. Res. Microbiol. 159: 216-220. DOI: [[https://doi.org/10.1016/j.resmic.2007.12.004|10.1016/j.resmic.2007.12.004]] 
 + 
 +Kim JG, Li X, Roden JA, Taylor KW, Aakre CD, Su B, Landone S, Kirik A, Chen Y, Baranage G, Martin BG, Mudgett BM, McLane H (2009). //Xanthomonas// T3S effector XopN suppresses PAMP-triggered immunity and interacts with a tomato atypical receptor-like kinase and TFT1. Plant Cell 21: 1305-1323. DOI: [[https://doi.org/10.1105/tpc.108.063123|10.1105/tpc.108.063123]] 
 + 
 +Kumar R, Mondal KK (2013). XopN-T3SS effector modulates in planta growth of //Xanthomonas axonopodis// pv. //punicae// and cell-wall-associated immune response to induce bacterial blight in pomegranate. Physiol. Mol. Plant Pathol. 84: 36-43. DOI: [[https://doi.org/10.1016/j.pmpp.2013.06.002|10.1016/j.pmpp.2013.06.002]]
  
-Jiang B, He Y, Cen W, Wei H, Jiang G, Jiang W, Hang X, Feng J, Lu G, Tang D, Tang J (2008). The type III secretion effector XopXccN of //Xanthomonas campestris//  pv. //campestris//  is required for full virulence. Res. Microbiol. 159: 216-220. DOI: [[https://doi.org/10.1016/j.resmic.2007.12.004|10.1016/j.resmic.2007.12.004]]+Kumar R, Soni M, Mondal KK (2016). XopN-T3SS effector of //Xanthomonas axonopodis// pv. //punicae// localizes to the plasma membrane and modulates ROS accumulation events during blight pathogenesis in pomegranate. Microbiol. Res. 193: 111-120. DOI: [[https://doi.org/10.1016/j.micres.2016.10.001|10.1016/j.micres.2016.10.001]]
  
-Kim JG, Li X, Roden JA, Taylor KW, Aakre CD, Su B, Landone S, Kirik A, Chen Y, Baranage G, Martin BG, Mudgett BM, McLane H (2009). //Xanthomonas//  T3S effector XopN suppresses PAMP-triggered immunity and interacts with a tomato atypical receptor-like kinase and TFT1. Plant Cell 21: 1305-1323. DOI: [[https://doi.org/10.1105/tpc.108.063123|10.1105/tpc.108.063123]]+Liao ZX, Li JY, Mo XY, Ni Z, Jiang W, He YQ, Huang S (2020). Type III effectors //xopN// and //avrBS2// contribute to the virulence of //Xanthomonas oryzae// pv. //oryzicola// strain GX01. Res. Microbiol. 171: 102-106. DOI: [[https://doi.org/10.1016/j.resmic.2019.10.002|10.1016/j.resmic.2019.10.002]]
  
-Kumar R, Mondal KK (2013). XopN-T3SS effector modulates in planta growth of Xanthomonas axonopodis pv. punicae and cell-wall-associated immune response to induce bacterial blight in pomegranate. Physiological and Mol. Plant Pathol. 84: 36-43. DOI: 10.1016/j.pmpp.2013.06.002+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]]
  
-Kumar R, Soni M, Mondal KK (2016). XopN-T3SS effector of //Xanthomonas axonopodis//  pv. //punicae//  localizes to the plasma membrane and modulates ROS accumulation events during blight pathogenesis in pomegranate. Microbiol. Res. 193: 111-120. DOI: [[https://doi.org/10.1016/j.micres.2016.10.001|10.1016/j.micres.2016.10.001]] FIXME  Information needs to be added to the profile.+Long J, Song C, Yan F, Zhou J, Zhou H, Yang B (2018). Non-TAL effectors from //Xanthomonas oryzae// pv. //oryzae// suppress peptidoglycan-triggered MAPK activation in rice. Front. Plant Sci. 9: 1857. doi: [[https://doi.org/10.3389/fpls.2018.01857|10.3389/fpls.2018.01857]]
  
-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: [[https://doi.org/10.1094/MPMI-10-14-0314-R|10.1094/MPMI-10-14-0314-R]] FIXME  Information needs to be added to the profile.+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]]
  
-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]]+Mo X, Zhang L, Liu Y, Wang X, Bai J, Lu K, Zou S, Dong H, Chen L (2020). Three proteins (Hpa2, HrpF and XopN) are concomitant type III translocators in bacterial blight pathogen of rice. Front. Microbiol. 11: 1601. DOI: [[https://doi.org/10.3389/fmicb.2020.01601|10.3389/fmicb.2020.01601]]
  
-Long J, Song C, Yan F, Zhou J, Zhou H, Yang B (2018). Non-TAL effectors from //Xanthomonas oryzae//  pv. //oryzae//  suppress peptidoglycan-triggered MAPK activation in rice. Front. Plant Sci. 9: 1857. doi: [[https://doi.org/10.3389/fpls.2018.01857|10.3389/fpls.2018.01857]] FIXME  Information needs to be added to the profile.+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]]
  
-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]]+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]]
  
-Mo X, Zhang L, Liu Y, Wang X, Bai J, Lu K, Zou S, Dong H, Chen L (2020). Three proteins (Hpa2, HrpF and XopN) are concomitant type III translocators in bacterial blight pathogen of rice. Frontiers in Microbiology 11: 1601. DOI=10.3389/fmicb.2020.01601+Taylor KW, Kim JG, Su XB, Aakre CD, Roden JA, Adams CM, Mudgett MB (2012). Tomato TFT1 is required for PAMP-triggered immunity and mutations that prevent T3S effector XopN from binding to TFT1 attenuate //Xanthomonas// virulence. PLoS Pathog. 8: e1002768. DOI: [[https://doi.org/10.1371/journal.ppat.1002768|10.1371/journal.ppat.1002768]]
  
-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]]+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]]
  
-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]] FIXME  Information needs to be added to the profile.+===== Acknowledgements =====
  
-Taylor KW, Kim JG, Su XB, Aakre CD, Roden JA, Adams CM, Mudgett MB (2012). Tomato TFT1 is required for PAMP-triggered immunity and mutations that prevent T3S effector XopN from binding to TFT1 attenuate //Xanthomonas//  virulence. PLoS Pathog. 8: e1002768. DOI: [[https://doi.org/10.1371/journal.ppat.1002768|10.1371/journal.ppat.1002768]] FIXME  Information needs to be added to the profile.+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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