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--- bacteria:t3e:xopl [2024/10/28 12:39] – [References] rkoebnik
+++ bacteria:t3e:xopl [2025/02/13 12:36] (current) – jfpothier
@@ Line 16: / Line 16: @@
 === How discovered? ===
-XopL was first identified in //X. campestris// pv. //campestris // (//Xcc//) strain 8004 as a candidate T3E due to the presence of a plant-inducible promoter (PIP) box upstream of the CDS, XC_4273 (Jiang //et al.//, 2009). The CDS //XC_4273//, re-called XopXccLR (LR = leucine-rich repeat) or XopL<sub>Xcc</sub> for the purposes of this article, in //Xcc //8004 was suggested to be a T3E as it harboured a N-terminal region possessing a translocation signal that was able to target proteins into plant cells (Jiang //et al.//, 2009). It was also shown to be required for Xcc proliferation in hosts plant (Jiang //et al.//, 2009). It was only a few years later that the analysis of the genome sequence of //X.// //campestris// pv. //vesicatoria// (Xcv) strain 85-10 (synonymous with //X. euvesicatoria //85-10; //Xe// 85-10) led to the identification of XCV3220 (//xopL<sub>Xe</sub> //) as a new T3E candidate gene and to its more complete characterization (Singer// et al//., 2013). This revealed XopLXe as an E3 ubiquitin ligase with a novel fold (XL-box), capable of interacting with the plant host ubiquitination cascade (Singer //et al.//, 2023).
+XopL was first identified in //X. campestris// pv. //campestris// (//Xcc//) strain 8004 as a candidate T3E due to the presence of a plant-inducible promoter (PIP) box upstream of the CDS, //XC_4273// (Jiang //et al.//, 2009). The CDS //XC_4273//, re-called XopXccLR (LR = leucine-rich repeat) or XopL<sub>Xcc</sub> for the purposes of this article, in //Xcc// 8004 was suggested to be a T3E as it harboured a N-terminal region possessing a translocation signal that was able to target proteins into plant cells (Jiang //et al.//, 2009). It was also shown to be required for //Xcc// proliferation in hosts plant (Jiang //et al.//, 2009). It was only a few years later that the analysis of the genome sequence of //X.// //campestris// pv. //vesicatoria// (//Xcv//) strain 85-10 (synonymous with //X. euvesicatoria// 85-10; //Xe// 85-10) led to the identification of XCV3220 (//xopL<sub>Xe</sub> //) as a new T3E candidate gene and to its more complete characterization (Singer //et al//., 2013). XopL<sub>Xe</sub> was shown to have E3 ubiquitin ligase activity, conferred by a ligase domain with a novel fold (XL-box), capable of interacting with the plant host ubiquitination cascade (Singer //et al.//, 2023).
 === (Experimental) evidence for being a T3E ===
-XopL<sub>Xcc</sub> possesses features that are typical of T3Es: the promoter region of xopL<sub>Xcc8004</sub> gene contains a perfect plant inducible promoter (PIP) box followed by a 10 box similar sequence (TTCGC-N<sub>15</sub>-TTCGC-N<sub>31</sub>-ACGACA) and LRRs motif is characteristic of specific T3Es in pathogenic bacteria (Yan //et al//., 2019). Using an AvrBs1 reporter fusion, XopL<sub>Xcc</sub> was shown to be translated into plant cells in a //hrpF-// and //hpaB//-dependent manner (Jiang //et al//., 2009). XopL<sub>Xe</sub> contains a PIP box (plant inducible promoter) in its promoter (TTCG-N<sub>16</sub>-TTCG; genome position 3669238-261) and co-regulation with the T3S system was confirmed by RT-PCR (Singer //et al.//, 2013). Type III-dependent secretion and translocation was confirmed by //in vitro //secretion and //in vivo //translocation assays (Singer// et al.//, 2013).
+XopL<sub>Xcc</sub> possesses features that are typical of T3Es: the promoter region of the //xopL<sub>Xcc</sub>// gene contains a perfect plant inducible promoter (PIP) box followed by a 10 box similar sequence (TTCGC-N<sub>15</sub>-TTCGC-N<sub>31</sub>-ACGACA) and an LRR motif characteristic of T3Es in pathogenic bacteria (Yan //et al//., 2019). Using an AvrBs1 reporter fusion, XopL<sub>Xcc</sub> was shown to be translocated into plant cells in a //hrpF-// and //hpaB//-dependent manner (Jiang //et al//., 2009). XopL<sub>Xe</sub> also contains a PIP box (plant inducible promoter) in its promoter (TTCG-N<sub>16</sub>-TTCG; genome position 3669238-261) and co-regulation with the T3S system was confirmed by RT-PCR (Singer //et al.//, 2013). Type III-dependent secretion and translocation was confirmed by //in vitro//secretion and //in vivo//translocation assays (Singer //et al.//, 2013).
 === Regulation ===
@@ Line 26: / Line 27: @@
 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 //xopL//, 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).
-The expression of //xopL// <sub>Xcc8004</sub> gene is positively regulated by HrpG/HrpX (Yan //et al//., 2019).
+The expression of //xopL<sub>Xcc</sub>// gene is positively regulated by HrpG/HrpX (Yan //et al//., 2019).
 === Phenotypes ===
-  * XopL<sub>//Xe// </sub>  from //X. euvesicatoria//  85-10 (previously referred to as //X. campestris //pv. //euvesicatoria//; //Xcv//) displays E3 ubiquitin ligase activity (Singer //et al.//, 2013).
+  * XopL<sub>//Xe//</sub>  from //X. euvesicatoria//  85-10 (previously referred to as //X. campestris// pv. //euvesicatoria//; //Xcv//) displays E3 ubiquitin ligase activity (Singer //et al.//, 2013).
-  * XopL//<sub>Xe </sub> //inhibits expression of the elf18- and flg22-induced defense gene pNHL10 in Arabidopsis mesophyll protoplasts independent of E3 ligase function (Singer //et al.//, 2013).
+  * XopL//<sub>Xe</sub>// inhibits expression of the elf18- and flg22-induced defense gene pNHL10 in //Arabidopsis// mesophyll protoplasts independent of E3 ligase function (Singer //et al.//, 2013).
-  * XopL//<sub>Xe</sub> //  suppresses ABA responsive reporter //pRD29b:GUS //and PTI reporter //pFRK1:LUC//  in Arabidopsis protoplasts (Popov //et al//., 2016).
+  * XopL//<sub>Xe</sub>// suppresses ABA responsive reporter //pRD29b:GUS// and PTI reporter //pFRK1:LUC// in //Arabidopsis// protoplasts (Popov //et al//., 2016).
-  * XopL//<sub>Xcc</sub> //  interferes with innate immunity (Yan //et al.//, 2019; Huang //et al.//, 2024) and SA signaling in Arabidopsis (Huang //et al.//, 2024).
+  * XopL//<sub>Xcc</sub>// interferes with innate immunity (Yan //et al.//, 2019; Huang //et al.//, 2024a) and SA signaling in //Arabidopsis// (Huang //et al.//, 2024).
-  * XopL//<sub>Xe</sub> //  triggers cell death in //Nicotiana benthamiana//  in an E3 ligase dependant manner (Singer //et al.//, 2013). XopL<sub>Xoc</sub>  from //X. oryzae//  pv. //oryzicola //and XopL<sub>Xoo</sub>  from //X. oryzae //pv. //oryzae//  PX099A also cause cell death in this model (Ma //et al.//, 2020).
+  * XopL//<sub>Xe</sub>// triggers cell death in //Nicotiana benthamiana// in an E3 ligase dependant manner (Singer //et al.//, 2013). XopL<sub>Xoc</sub> from //X. oryzae// pv. //oryzicola// and XopL<sub>Xoo</sub> from //X. oryzae// pv. //oryzae// PX099A also cause cell death in this model (Ma //et al.//, 2020).
-  * Distantly related XopL homolog XopL//<sub>Xcc</sub> //  from //Xcc//  8004 failed to cause plant cell death. (Ortmann //et al.//, 2023).
+  * Distantly related XopL homolog XopL//<sub>Xcc</sub>// from //Xcc// 8004 failed to cause plant cell death. (Ortmann //et al.//, 2023).
-  * XopL//<sub>Xcc</sub> //  is required for full virulence and growth of //Xcc//  8004 in the host plant Chinese radish (Jiang //et al.//, 2009) but not in Arabidopsis (Huang et al, 2024. However a mutant for 17 effectors (Δ//17E//) supplemented with //xopL<sub>Xcc</sub> //  did grow better than Δ//17E//.
+  * XopL//<sub>Xcc</sub>// is required for full virulence and growth of //Xcc// 8004 in the host plant Chinese radish (Jiang //et al.//, 2009) but not in //Arabidopsis// (Huang et al, 2024). However a mutant for 17 effectors (Δ//17E//) supplemented with //xopL<sub>Xcc</sub> // did grow better than Δ//17E//.
-  * XopL//<sub>Xcc</sub> //  constituative overexpression in Arabidopsis let to enhance Xcc 8004 virulence and suppressed callose deposition and oxidative burst (Huang //et al.//, 2024)
+  * XopL//<sub>Xcc</sub>// constitutive overexpression in //Arabidopsis// led to enhanced //Xcc// 8004 virulence and suppressed callose deposition and oxidative burst (Huang //et al.//, 2024).
-  * XopL//<sub>Xe</sub> //  is required for full virulence of //Xe//  85-10 on tomato (Leong et al., 2022).
+  * XopL//<sub>Xe</sub>// is required for full virulence of //Xe// 85-10 on tomato (Leong et al., 2022).
-  * XopL//<sub>Xap</sub> //  supports //X. axonopodis //pv.// punicae //multiplication in pomegranate by suppressing plant immune responses including plant cell death (Soni //et al//., 2017).
+  * XopL//<sub>Xap</sub>// supports //X. axonopodis //pv.// punicae //multiplication in pomegranate by suppressing plant immune responses including plant cell death (Soni //et al//., 2017).
-  * Transient expression of XopL//<sub>Xe</sub> //, led to a nearly complete elimination of stromules and the relocation of plastids to the nucleus and further characterization revealed that the E3 ligase activity is essential for two plastid phenotypes (//Erickson et al//., 2018).
+  * Transient expression of XopL//<sub>Xe</sub> //, led to a nearly complete elimination of stromules and the relocation of plastids to the nucleus and further characterization revealed that the E3 ligase activity is essential for the two plastid phenotypes (//Erickson et al//., 2018).
-  * //Xe //85-10 suppresses host autophagy by utilizing type-III effector XopL//<sub>Xe</sub> //. Intriguingly, XopL//<sub>Xe</sub> //  is targeted for degradation by defense-related selective autophagy mediated by NBR1/Joka2, revealing a complex antagonistic interplay between XopL and the host autophagy machinery (Leong// et al.//, 2022).
+  * //Xe //85-10 suppresses host autophagy by utilizing type-III effector XopL//<sub>Xe</sub> //. Intriguingly, XopL//<sub>Xe</sub>// is targeted for degradation by defense-related selective autophagy mediated by NBR1/Joka2, revealing a complex antagonistic interplay between XopL and the host autophagy machinery (Leong// et al.//, 2022).
 === Localization ===
 Several localization patterns have been reported for XopL proteins in epidermal cells with some strain dependent differences. XopLs are most often tagged at the C-terminus, with the exception of the studies by Leong //et al//., 2022 and Yan //et al.//, 2019.
-  * __Cytosolic localization__  has been reported for XopL//<sub>Xe</sub> //  (Erickson //et al.//, 2018), XopL//<sub>Xcc</sub> //  (Yan //et al//., 2019; Ortmann //et al//. 2023), XopL<sub>//Xoo// </sub>  (Ma //et al//., 2020; Ortmann //et al//., 2023), and XopL//<sub>Xac</sub> //  from //X. citri //pv. citri (Ortmann et al. 2023) in //N. benthamiana//.
+  * __Cytosolic localization__ has been reported for XopL//<sub>Xe</sub>// (Erickson //et al.//, 2018), XopL//<sub>Xcc</sub>// (Yan //et al//., 2019; Ortmann //et al//. 2023), XopL<sub>//Xoo//</sub> (Ma //et al//., 2020; Ortmann //et al//., 2023), and XopL//<sub>Xac</sub> //  from //X. citri// pv. //citri// (Ortmann et al. 2023) in //N. benthamiana//.
-  * __Nuclear localization__  was reported for XopL//<sub>Xe</sub> //, XopL<sub>//Xcc// </sub>  (Yan //et al.//, 2019; Ortmann //et al//., 2023) and XopL//<sub>Xac</sub> //  in //N. benthamiana//  (Ortmann et al. 2023), but not for XopL//<sub>Xoo</sub> //  in //N. benthamiana //or XopL//<sub>Xap</sub> //  from //X. axonopodis//  pv. //punicae//  in Arabidopsis protoplasts (Soni //et al.//, 2017; Ortmann //et al.,//  2023).
+  * __Nuclear localization__ was reported for XopL//<sub>Xe</sub>//, XopL<sub>//Xcc//</sub> (Yan //et al.//, 2019; Ortmann //et al//., 2023) and XopL//<sub>Xac</sub>// in //N. benthamiana// (Ortmann et al. 2023), but not for XopL//<sub>Xoo</sub>// in //N. benthamiana// or XopL//<sub>Xap</sub>// from //X. axonopodis// pv. //punicae// in //Arabidopsis// protoplasts (Soni //et al.//, 2017; Ortmann //et al.,// 2023).
-  * __Plasma membrane localization__  has been reported for XopL<sub>//Xap// </sub>  transiently expressed in //N. benthmiana//  (Soni //et al//  ., 2017) and XopL//<sub>Xcc</sub> //  expressed in Arabidopsis protoplasts (Huang //et al//. 2024; Yan //et al.//  , 2019) and //N. benthamiana//  leaves (Yan //et al//., 2019).
+  * __Plasma membrane localization__ has been reported for XopL<sub>//Xap//</sub> transiently expressed in //N. benthmiana// (Soni //et al//., 2017) and XopL//<sub>Xcc</sub>// expressed in //Arabidopsis// protoplasts (Huang //et al//. 2024b; Yan //et al.// , 2019) and //N. benthamiana// leaves (Yan //et al//., 2019).
-  * __Microtubule localization__  has been reported for XopL//<sub>Xe</sub> //, XopL<sub>//Xoo// </sub>  and XopL//<sub>Xac</sub> //, whereas the distantly related XopL//<sub>Xcc</sub> //  failed to localize to microtubules (Ortmann //et al.//, 2023).
+  * __Microtubule localization__ has been reported for XopL//<sub>Xe</sub>//, XopL<sub>//Xoo//</sub> and XopL//<sub>Xac</sub>//, whereas the distantly related XopL//<sub>Xcc</sub>// failed to localize to microtubules in //N. benthamiana// (Ortmann //et al.//, 2023).
-  * __Autophagosome localization__  has been reported for XopL//<sub>Xe</sub> //  (co-localizes with autophagy markers RFP-ATG8e and SH3P2-RFP; Leong //et al//., 2022).
+  * __Autophagosome localization__ has been reported for XopL//<sub>Xe</sub>// (co-localizes with autophagy markers RFP-ATG8e and SH3P2-RFP; Leong //et al//., 2022).
 === Enzymatic function ===
-XopL<sub>Xe</sub>  contains 9 leucine-rich repeats (LRRs). Mutation of amino acids in the central cavity of the XL-box disrupt E3 ligase activity and prevent XopL-induced plant cell death. The lack of cysteine residues in the XL-box suggest that thioester-linked ubiquitin-E3 ligase intermediates are not formed during XopL-mediated ubiquitination. Suppression of PAMP responses solely depends on the N-terminal LRR domain (Singer //et al//., 2013).
+XopL<sub>Xe</sub> harbours an unstructured N-terminus, followed by three alpha helices, an leucine-rich repeat (LRR) domain and an XL-box. Mutation of amino acids in the central cavity of the XL-box disrupt E3 ligase activity and prevent XopL-induced plant cell death. The lack of cysteine residues in the XL-box suggest that thioester-linked ubiquitin-E3 ligase intermediates are not formed during XopL-mediated ubiquitination. Suppression of PAMP responses solely depends on the N-terminal LRR domain (Singer //et al//., 2013), while microtubule binding relies on a proline-rich region in the unstructured region and the alpha-helical region (Ortman //et al//., 2023).
 === Interaction partners ===
-XopL<sub>Xe</sub>  interacts with and degrades the autophagy component SH3P2 via its E3 ligase activity to promote infection (Leong //et al.//, 2022). XopL<sub>Xoo</sub>  interacts with and degrades ferredoxin from //N. benthamiana//, part of the electron transport chain (Ma //et al.//, 2020). XopLXcc interaction with proton pump interactor 1 (PPI1) in Arabidopsis (Huang //et al//., 2024b).
+XopL<sub>Xe</sub> interacts with and degrades the autophagy component SH3P2 via its E3 ligase activity to promote infection (Leong //et al.//, 2022). XopL<sub>Xoo</sub> interacts with and degrades ferredoxin from //N. benthamiana//, part of the electron transport chain (Ma //et al.//, 2020). XopLXcc interaction with proton pump interactor 1 (PPI1) in //Arabidopsis// (Huang //et al//., 2024b).
 ===== Conservation =====
@@ Line 62: / Line 63: @@
 === In xanthomonads ===
-Yes (//e.g.//, //X. euvesicatoria//, //X. citri//, //X. axonopodis//, //X. oryzae//, //X. oryzicola//, //X//. //fragariae//, //X//. //perforans, X. gardneri//, //X. campestris//  pv. //campestris//, but not //X. campestris//  pv. //raphani//, in some //X. arboricola//  pathovars). See for example [[https://doi.org/10.1094/MPMI-22-11-1401|Table 2]] in Jiang //et al//. (2009) and [[https://doi.org/10.1371/journal.ppat.1003121.s001|Figure S1]] in Singer //et al//. (2013).
+Yes (//e.g.//, //X. euvesicatoria//, //X. citri//, //X. axonopodis//, //X. oryzae//, //X. oryzicola//, //X//. //fragariae//, //X//. //perforans, X. gardneri//, //X. campestris// pv. //campestris//, but not //X. campestris// pv. //raphani//, in some //X. arboricola// pathovars). See for example [[https://doi.org/10.1094/MPMI-22-11-1401|Table 2]] in Jiang //et al//. (2009) and [[https://doi.org/10.1371/journal.ppat.1003121.s001|Figure S1]] in Singer //et al//. (2013).
 === In other plant pathogens/symbionts ===
@@ Line 74: / Line 75: @@
 Erickson JL, Adlung N, Lampe C, Bonas U, Schattat MH (2018). The //Xanthomonas// effector XopL uncovers the role of microtubules in stromule extension and dynamics in //Nicotiana benthamiana//. Plant J. 93: 856-870. DOI:[[https://doi.org/10.1111/tpj.13813|10.1111/tpj.13813]]
-Huang J, Dong Y, Li N, He Y, Zhou H (2024a). The type III effector XopL//<sub>Xcc</sub> // in //Xanthomonas campestris// pv. //campestris// targets the proton pump interactor 1 and suppresses innate immunity in //Arabidopsis//. Int. J. Mol. Sci. 25: 9175. DOI: [[https://doi.org/10.3390/ijms25179175|10.3390/ijms25179175]]
+Huang J, Dong Y, Li N, He Y, Zhou H (2024a). The type III effector XopL//<sub>Xcc</sub>// in //Xanthomonas campestris// pv. //campestris// targets the proton pump interactor 1 and suppresses innate immunity in //Arabidopsis//. Int. J. Mol. Sci. 25: 9175. DOI: [[https://doi.org/10.3390/ijms25179175|10.3390/ijms25179175]]
 Huang J, Zhou H, Zhou M, Li N, Jiang B, He Y (2024b). Functional analysis of type III effectors in //Xanthomonas campestris// pv. //campestris// reveals distinct roles in modulating //Arabidopsis// innate immunity. Pathogens 13: 448. DOI: [[https://doi.org/10.3390/pathogens13060448|10.3390/pathogens13060448]]
@@ Line 84: / Line 85: @@
 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]]
-Ma W, Xu X, Cai L, Cao Y, Haq F, Alfano JR, Zu B, Zou L, Chen G (2020) //.// A //Xanthomonas oryzae// type III effector XopL causes cell death through mediating ferredoxin degradation in //Nicotiana benthamiana//. Phytopathol Res. 2: 16. DOI: 10.1186/s42483-020-00055-w
+Ma W, Xu X, Cai L, Cao Y, Haq F, Alfano JR, Zu B, Zou L, Chen G (2020). A //Xanthomonas oryzae// type III effector XopL causes cell death through mediating ferredoxin degradation in //Nicotiana benthamiana//. Phytopathol Res. 2: 16. DOI: 10.1186/s42483-020-00055-w
 Ortmann S, Marx J, Lampe C, Handrick V, Ehnert TM, Zinecker S, Reimers M, Bonas U, Erickson JL (2023). A conserved microtubule-binding region in //Xanthomonas// XopL is indispensable for induced plant cell death reactions. PLoS Pathog. 19: e1011263. DOI: [[https://doi.org/10.1371/journal.ppat.1011263|10.1371/journal.ppat.1011263]]

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