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--- bacteria:t3e:xopaj [2020/09/29 21:21] – lindsay.triplett_ct.gov
+++ bacteria:t3e:xopaj [2025/02/12 23:32] (current) – jfpothier
@@ Line 1: / Line 1: @@
-====== XopAJ ======
+====== The Type III Effector XopAJ from //Xanthomonas// ======
-Authors: [[https://www.researchgate.net/profile/Ralf_Koebnik|Ralf Koebnik]] & Trainees from the 2<sup>nd</sup>  EuroXanth Training School ([[https://www.researchgate.net/profile/Daiva_Burokiene|Daiva Burokienė]], [[https://www.researchgate.net/profile/ermic_Edyta|Edyta Đermić]], [[https://www.researchgate.net/profile/Dagmar_Stehlikova|Dagmar Stehlikova]], [[https://www.researchgate.net/profile/Mariya_Stoyanova|Mariya Stoyanova]])\\
+Authors: [[https://www.researchgate.net/profile/Ralf_Koebnik|Ralf Koebnik]] & Trainees from the 2<sup>nd</sup> EuroXanth Training School ([[https://www.researchgate.net/profile/Daiva_Burokiene|Daiva Burokienė]], [[https://www.researchgate.net/profile/ermic_Edyta|Edyta Đermić]], [[https://www.researchgate.net/profile/Dagmar_Stehlikova|Dagmar Stehlikova]], [[https://www.researchgate.net/profile/Mariya_Stoyanova|Mariya Stoyanova]])\\
 Internal reviewer: [[https://www.researchgate.net/profile/Joel_Pothier2|Joël F. Pothier]]\\
-Expert reviewer: Lindsay Triplett
+Expert reviewer: [[https://www.researchgate.net/profile/Lindsay_Triplett|Lindsay Triplett]]
 Class: XopAJ\\
 Family: XopAJ\\
-Prototype: XopAJ (//Xanthomonas oryzae// pv. //oryzicola//; strain BLS256)\\
+Prototype: AvrRxo1 (//Xanthomonas oryzae// pv. //oryzicola//; strain BLS256)\\
-RefSeq ID: [[https://www.ncbi.nlm.nih.gov/protein/WP_014504815.1|WP_014504815.1 ]] (obsolete version suggested to be replaced by [[https://www.ncbi.nlm.nih.gov/protein/WP_153816726.1|WP_153816726.1]]) (421 aa)\\
+GenBank ID: [[https://www.ncbi.nlm.nih.gov/protein/AAQ97593.1|AAQ97593.1 ]] (421 aa)\\
+RefSeq ID: [[https://www.ncbi.nlm.nih.gov/protein/WP_014504815.1|WP_014504815.1 ]] (421 aa)\\
 Synonym: AvrRxo1\\
 D structure: [[https://www.rcsb.org/structure/4Z8Q|4Z8Q]], [[https://www.rcsb.org/structure/4Z8T|4Z8T]], [[https://www.rcsb.org/structure/4Z8U|4Z8U]], [[https://www.rcsb.org/structure/4Z8V|4Z8V]] (Han //et al.//, 2015)
@@ Line 25: / Line 26: @@
 === Phenotypes ===
-  * When introduced into //Xoo//, clones containing //avrRxo1//  induced an HR on maize with //Rxo1//, but not on maize without //Rxo1//  (Zhao //et al.//, 2004).
+  * When introduced into //Xoo//, clones containing //avrRxo1// induced an HR on maize with //Rxo1//, but not on maize without //Rxo1// (Zhao //et al.//, 2004).
-  * //Rxo1//  has a nucleotide-binding site-leucine-rich repeat structure, similar to many previously identified //R//  genes (Zhao //et al.//, 2005). //Rxo1//  functions after transfer as a transgene to rice, demonstrating the feasibility of nonhost //R//  gene transfer between cereals (Zhao //et al.//, 2005; Xie //et al.//, 2007).
+  * //Rxo1// has a nucleotide-binding site-leucine-rich repeat structure, similar to many previously identified //R// genes (Zhao //et al.//, 2005). //Rxo1// functions after transfer as a transgene to rice, demonstrating the feasibility of nonhost //R// gene transfer between cereals (Zhao //et al.//, 2005; Xie //et al.//, 2007).
-  * AvrRxo1 is cytotoxic when expressed in yeast and caused chlorosis and patches of cell death in the infiltrated leaf areas upon transient expression in tomato and //Nicotiana benthamiana//  (Salomon //et al.//, 2011).
+  * AvrRxo1 is cytotoxic when expressed in yeast and caused chlorosis and patches of cell death in the infiltrated leaf areas upon transient expression in tomato and //Nicotiana benthamiana// (Salomon //et al.//, 2011).
-  * Variants of AvrRxo1 were found to suppress the HR caused by the non-host resistance recognition of //Xoo//  by //N. benthamiana//  (Liu //et al.//, 2014).
+  * Variants of AvrRxo1 were found to suppress the HR caused by the non-host resistance recognition of //Xoo// by //N. benthamiana// (Liu //et al.//, 2014).
-  * Among four //avrRxo1//  alleles from different //Xoc//  strains, toxicity is abolished by a single amino acid substitution at residue 344 in two AvrRxo1 variants (Liu //et al.//, 2014).
+  * Among four //avrRxo1// alleles from different //Xoc// strains, toxicity is abolished by a single amino acid substitution at residue 344 in two AvrRxo1 variants (Liu //et al.//, 2014).
   * The ATP/GTP binding site motif A and the NLS are required for both the avirulence activity and the suppression of non-host resistance (Liu //et al.//, 2014).
   * AvrRxo1 has a T4 polynucleotide kinase domain and a structure homologous to that of Zeta toxins, and expression of AvrRxo1 suppresses bacterial growth in a manner dependent on the kinase motif (Han //et al.//, 2015).
   * The gene product of the adjacent gene, AvrRxo1-ORF2 aka Arc1, suppresses the bacteriostatic activity of AvrRxo1 in bacterial cells (Han //et al.//, 2015).
-  * AvrRxo1 and its binding partner Arc1 function as a toxin-antitoxin system when expressed in //Escherichia coli//  (Triplett //et al.//, 2016). Bacterial toxicity is dependent on bacterial growth rate and conferred by diverse AvrRxo1 homologs from //X. euvesicatoria//, //B. andropogonis//, and //X. translucens//.
+  * AvrRxo1 and its binding partner Arc1 function as a toxin-antitoxin system when expressed in //Escherichia coli// (Triplett //et al.//, 2016). Bacterial toxicity is dependent on bacterial growth rate and conferred by diverse AvrRxo1 homologs from //X. euvesicatoria//, //B. andropogonis//, and //X. translucens//.
-  * XopAJ<sub>Xcv85-10</sub>  inhibited activation of a PTI-inducible promoter by the bacterial peptide elf18 in Arabidopsis protoplasts and by flg22 in tomato protoplasts. This effector inhibited flg22-induced callose deposition //in planta//  and enhanced disease symptoms caused by attenuated// Pseudomonas syringae//  bacteria (Popov //et al.//, 2016).
+  * XopAJ<sub>Xcv85-10</sub> inhibited activation of a PTI-inducible promoter by the bacterial peptide elf18 in Arabidopsis protoplasts and by flg22 in tomato protoplasts. This effector inhibited flg22-induced callose deposition //in planta// and enhanced disease symptoms caused by attenuated //Pseudomonas syringae// bacteria (Popov //et al.//, 2016).
-  * AvrRxo1 is a kinase that converts NAD to 3'-NADP and NAADP to 3'-NAADP. Mutation of the catalytic aspartic acid residue D<sub>193</sub>  abolished AvrRxo1 kinase activity and several phenotypes of AvrRxo1, including toxicity in yeast, bacteria, and plants, suppression of the flg22-triggered ROS burst, and ability to trigger an //R//  gene-mediated hypersensitive response in rice. A mutation in the Walker A ATP-binding motif, which reduced 3'-NADP production by roughly 90%, abolished the toxicity of AvrRxo1 in bacteria, yeast, and plants. However, this mutation did not abolish the virulence enhancement, ROS suppression, or HR-triggering phenotypes of AvrRxo1. These results demonstrate that AvrRxo1 kinase activity is required for all the known phenotypes of AvrRxo1, but that toxicity is dose-dependent (Shidore //et al.//, 2017).
+  * AvrRxo1 is a kinase that converts NAD to 3'-NADP and NAADP to 3'-NAADP. Mutation of the catalytic aspartic acid residue D<sub>193</sub> abolished AvrRxo1 kinase activity and several phenotypes of AvrRxo1, including toxicity in yeast, bacteria, and plants, suppression of the flg22-triggered ROS burst, and ability to trigger an //R// gene-mediated hypersensitive response in rice. A mutation in the Walker A ATP-binding motif, which reduced 3'-NADP production by roughly 90%, abolished the toxicity of AvrRxo1 in bacteria, yeast, and plants. However, this mutation did not abolish the virulence enhancement, ROS suppression, or HR-triggering phenotypes of AvrRxo1. These results demonstrate that AvrRxo1 kinase activity is required for all the known phenotypes of AvrRxo1, but that toxicity is dose-dependent (Shidore //et al.//, 2017).
   * AvrRxo1 targets the cysteine protease RD21A, which is required for drought-induced immunity (Liu //et al.//, 2020).
+  * AvrRxo1 enhances //Xoc// virulence and inhibits stomatal immunity by targeting and degrading rice OsPDX1 (pyridoxal phosphate synthase), thereby reducing vitamin B6 (VB6) levels in rice (Liu //et al.//, 2022).
 === Localization ===
-Transient expression of //avrRxo1//  in onion cells after biolistic delivery revealed that the protein product was associated with the plasma membrane (Zhao //et al.//, 2004). However, later studies using fluorescently-tagged AvrRxo1 indicate localization in the nucleus and cytoplasm as well (Liu //et al//., 2014, Triplett// et al.//, 2016, Liu //et al.//, 2020).
+Transient expression of //avrRxo1// in onion cells after biolistic delivery revealed that the protein product was associated with the plasma membrane (Zhao //et al.//, 2004). However, later studies using fluorescently-tagged AvrRxo1 indicate localization in the nucleus and cytoplasm as well (Liu //et al//., 2014, Triplett //et al.//, 2016, Liu //et al.//, 2020).
 === Enzymatic function ===
-AvrRxo1 has a T4 polynucleotide kinase domain (Han //et al.//, 2015; Wu //et al//., 2015).
+AvrRxo1 has a T4 polynucleotide kinase domain (Han //et al.//, 2015; Wu //et al//., 2015). AvrRxo1 is an ATP-dependent protease (Liu //et al.//, 2022).
-AvrRxo1 is a phosphotransferase that produces two novel metabolites by phosphorylating nicotinamide/nicotinic acid adenine dinucleotide at the adenosine 3'-hydroxyl group. Both products of AvrRxo1, 3'-NADP and 3'-nicotinic acid adenine dinucleotide phosphate (3'-NAADP), had been used before as inhibitors or signaling molecules but were regarded as "artificial" compounds until then (Schuebel //et al.//, 2016). AvrRxo1 has weak phosphorylation activity on some other nucleotides including ATP (Scheubel //et al. //2016)
+AvrRxo1 is a phosphotransferase that produces two novel metabolites by phosphorylating nicotinamide/nicotinic acid adenine dinucleotide at the adenosine 3'-hydroxyl group. Both products of AvrRxo1, 3'-NADP and 3'-nicotinic acid adenine dinucleotide phosphate (3'-NAADP), had been used before as inhibitors or signaling molecules but were regarded as "artificial" compounds until then (Schuebel //et al.//, 2016). AvrRxo1 has weak phosphorylation activity on some other nucleotides including ATP (Scheubel //et al.// 2016)
-AvrRxo1 phosphorylates NAD //in planta//, and its kinase catalytic sites are necessary for toxicity, suppression of PAMP-triggered immunity, and activation of Rxo1-mediated resistance (Shidore //et al.//, 2017). In a metabolomic profile, 3'-NADP accumulated upon expression of AvrRxo1 in //E. coli//, yeast, //N. benthamiana//  and in rice leaves infected with //avrRxo1//-expressing strains of //X. oryzae//, suggesting that the AvrRxo1 product is not utilized or degraded by the cell (Shidore //et al.//, 2017). 3'-NADP was the only metabolite observed to accumulate in an //avrRxo1//-dependent manner, and it is not known whether NAADP is phosphorylated by AvrRxo1 //in planta // (Shidore //et al.//, 2017).
+AvrRxo1 phosphorylates NAD //in planta//, and its kinase catalytic sites are necessary for toxicity, suppression of PAMP-triggered immunity, and activation of Rxo1-mediated resistance (Shidore //et al.//, 2017). In a metabolomic profile, 3'-NADP accumulated upon expression of AvrRxo1 in //E. coli//, yeast, //N. benthamiana// and in rice leaves infected with //avrRxo1//-expressing strains of //X. oryzae//, suggesting that the AvrRxo1 product is not utilized or degraded by the cell (Shidore //et al.//, 2017). 3'-NADP was the only metabolite observed to accumulate in an //avrRxo1//-dependent manner, and it is not known whether NAADP is phosphorylated by AvrRxo1 //in planta// (Shidore //et al.//, 2017).
 === Interaction partners ===
@@ Line 56: / Line 58: @@
 The gene product of the adjacent gene, AvrRxo1-ORF2 aka Arc1, binds AvrRxo1, but binding is structurally different from typical effector-binding chaperones, in that it has a distinct fold containing a novel kinase-binding domain (Han //et al.//, 2015).
-AvrRxo1 interacts with the //Arabidopsis thaliana//  ubiquitin E3 ligase SINAT4 and the cysteine protease RD21A during transient expression in //N. benthamiana. //Interaction enhanced SINAT4 activity and promoted the degradation of RD21A //in vivo, //in a manner dependent on the AvrRxo1 ATP-binding motif (Liu //et al.//, 2020).
+AvrRxo1 interacts with the //Arabidopsis thaliana// ubiquitin E3 ligase SINAT4 and the cysteine protease RD21A during transient expression in //N. benthamiana//. Interaction enhanced SINAT4 activity and promoted the degradation of RD21A //in vivo//, in a manner dependent on the AvrRxo1 ATP-binding motif (Liu //et al.//, 2020).
+AvrRxo1 interacts with OsPDX1.2 in a yeast two-hybrid assay and in planta, as assessed by split YFP and coIP assays (Liu //et al.//, 2022).
 ===== Conservation =====
@@ Line 64: / Line 68: @@
 Yes (e.g. //X. alfalfae//, //X. axonopodis//, //X. bromi//, //X. euvesicatoria//, //X. oryzae//, //X. translucens//).
-AvrRxo1 appears to be widely conserved in Asian strains of //Xoc//  but much less present in African strains, which implies that deployment of //Rxo1//-containing varieties may not be an appropriate breeding strategy for controlling bacterial leaf streak disease in Africa (Wonni //et al.//, 2014).
+AvrRxo1 appears to be widely conserved in Asian strains of //Xoc// but much less present in African strains, which implies that deployment of //Rxo1//-containing varieties may not be an appropriate breeding strategy for controlling bacterial leaf streak disease in Africa (Wonni //et al.//, 2014).
-AvrRxo1 is conserved in nearly all strains of //X. euvesicatoria//, but is incompletely distributed in other species surveyed (Triplett et al. 2016, Barak et al. 2016). Strains with inactivated //avrRxo1//  genes were frequently observed to harbor sequence insertions in the toxic //avrRxo1//  gene, while the toxin-protective //arc1//  gene remained intact (Triplett //et al.,//  2016).
+AvrRxo1 is conserved in nearly all strains of //X. euvesicatoria//, but is incompletely distributed in other species surveyed (Triplett et al. 2016, Barak et al. 2016). Strains with inactivated //avrRxo1// genes were frequently observed to harbor sequence insertions in the toxic //avrRxo1// gene, while the toxin-protective //arc1// gene remained intact (Triplett //et al.,// 2016).
 === In other plant pathogens/symbionts ===
-Yes (//Acidovorax//  spp., //Paraburkholderia andropogonis//) (Triplett //et al.//, 2016).
+Yes (//Acidovorax// spp., //Paraburkholderia andropogonis//) (Triplett //et al.//, 2016).
-Homologs of the //avrRxo1:arc1//  operon in which the avrRxo1 homolog lacks a type III secretion signal are found in other environmental microbes, including the filamentous myxobacteria //Cystobacter fuscus//  and uncultured candidate //Saccharimonas//  and //Parcubacteria// spp. (Triplett// et al.//  2016).
+Homologs of the //avrRxo1:arc1// operon in which the avrRxo1 homolog lacks a type III secretion signal are found in other environmental microbes, including the filamentous myxobacteria //Cystobacter fuscus// and uncultured candidate //Saccharimonas// and //Parcubacteria// spp. (Triplett //et al.// 2016).
+===== Conservation =====
+=== In xanthomonads ===
+Yes (e.g. //X. alfalfae//, //X. axonopodis//, //X. bromi//, //X. euvesicatoria//, //X. oryzae//, //X. translucens//).
+AvrRxo1 appears to be widely conserved in Asian strains of //Xoc// but much less present in African strains, which implies that deployment of //Rxo1//-containing varieties may not be an appropriate breeding strategy for controlling bacterial leaf streak disease in Africa (Wonni //et al.//, 2014).
+AvrRxo1 is conserved in nearly all strains of //X. euvesicatoria//, but is incompletely distributed in other species surveyed (Triplett et al. 2016, Barak et al. 2016). Strains with inactivated //avrRxo1// genes were frequently observed to harbor sequence insertions in the toxic //avrRxo1// gene, while the toxin-protective //arc1// gene remained intact (Triplett //et al.,// 2016).
+=== In other plant pathogens/symbionts ===
+Yes (//Acidovorax// spp., //Paraburkholderia andropogonis//) (Triplett //et al.//, 2016).
+Homologs of the //avrRxo1:arc1// operon in which the avrRxo1 homolog lacks a type III secretion signal are found in other environmental microbes, including the filamentous myxobacteria //Cystobacter fuscus// and uncultured candidate //Saccharimonas// and //Parcubacteria// spp. (Triplett //et al.// 2016).
 ===== References =====
@@ Line 78: / Line 98: @@
 Bahadur RP, Basak J (2014). Molecular modeling of protein-protein interaction to decipher the structural mechanism of nonhost resistance in rice. J. Biomol. Struct. Dyn. 32: 669-681. DOI: [[https://doi.org/10.1080/07391102.2013.787370|10.1080/07391102.2013.787370]]
-Han Q, Zhou C, Wu S, Liu Y, Triplett L, Miao J, Tokuhisa J, Deblais L, Robinson H, Leach JE, Li J, Zhao B (2015). Crystal structure of //Xanthomonas//  AvrRxo1-ORF1, a type III effector with a polynucleotide kinase domain, and its interactor AvrRxo1-ORF2. Structure 23: 1900-1909. DOI: [[https://doi.org/10.1016/j.str.2015.06.030|10.1016/j.str.2015.06.030]]
+Han Q, Zhou C, Wu S, Liu Y, Triplett L, Miao J, Tokuhisa J, Deblais L, Robinson H, Leach JE, Li J, Zhao B (2015). Crystal structure of //Xanthomonas// AvrRxo1-ORF1, a type III effector with a polynucleotide kinase domain, and its interactor AvrRxo1-ORF2. Structure 23: 1900-1909. DOI: [[https://doi.org/10.1016/j.str.2015.06.030|10.1016/j.str.2015.06.030]]
 Liu H, Chang Q, Feng W, Zhang B, Wu T, Li N, Yao F, Ding X, Chu Z (2014). Domain dissection of AvrRxo1 for suppressor, avirulence and cytotoxicity functions. PLoS One 9: e113875. DOI: [[https://doi.org/10.1371/journal.pone.0113875|10.1371/journal.pone.0113875]]
-Liu Y, Wang K, Cheng Q, Kong D, Zhang X, Wang Z, Wang Q, Qi X, Yan J, Chu J, Ling H, Li Q, Miao J, Zhao B (2020). Cysteine protease RD21A regulated by E3 ligase SINAT4 is required for drought-induced resistance to //Pseudomonas syringae//  in Arabidopsis. J. Exp. Bot., eraa255 (in press). DOI: [[https://doi.org/10.1093/jxb/eraa255|10.1093/jxb/eraa255]]
+Liu H, Lu C, Li Y, Wu T, Zhang B, Liu B, Feng W, Xu Q, Dong H, He S, Chu Z, Ding X (2022). The bacterial effector AvrRxo1 inhibits vitamin B6 biosynthesis to promote infection in rice. Plant Commun. 3: 100324. DOI: [[https://doi.org/10.1016/j.xplc.2022.100324|10.1016/j.xplc.2022.100324]]
-Popov G, Fraiture M, Brunner F, Sessa G (2016). Multiple //Xanthomonas euvesicatoria//  type III effectors inhibit flg22-triggered immunity. Mol. Plant Microbe Interact. 29: 651-660. DOI: [[https://doi.org/10.1094/MPMI-07-16-0137-R|10.1094/MPMI-07-16-0137-R]]
+Liu Y, Wang K, Cheng Q, Kong D, Zhang X, Wang Z, Wang Q, Qi X, Yan J, Chu J, Ling H, Li Q, Miao J, Zhao B (2020). Cysteine protease RD21A regulated by E3 ligase SINAT4 is required for drought-induced resistance to //Pseudomonas syringae// in //Arabidopsis//. J. Exp. Bot. 71: 5562-5576. DOI: [[https://doi.org/10.1093/jxb/eraa255|10.1093/jxb/eraa255]]
-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]]
+Popov G, Fraiture M, Brunner F, Sessa G (2016). Multiple //Xanthomonas euvesicatoria// type III effectors inhibit flg22-triggered immunity. Mol. Plant Microbe Interact. 29: 651-660. DOI: [[https://doi.org/10.1094/MPMI-07-16-0137-R|10.1094/MPMI-07-16-0137-R]]
+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]]
 Schuebel F, Rocker A, Edelmann D, Schessner J, Brieke C, Meinhart A (2016). 3'-NADP and 3'-NAADP, two metabolites formed by the bacterial type III effector AvrRxo1. J. Biol. Chem. 291: 22868-22880. DOI: [[https://doi.org/10.1074/jbc.M116.751297|10.1074/jbc.M116.751297]]
@@ Line 94: / Line 116: @@
 Triplett LR, Shidore T, Long J, Miao J, Wu S, Han Q, Zhou C, Ishihara H, Li J, Zhao B, Leach JE (2016). AvrRxo1 Is a bifunctional type III secreted effector and toxin-antitoxin system component with homologs in diverse environmental contexts. PLoS One 11: e0158856. DOI: [[https://doi.org/10.1371/journal.pone.0158856|10.1371/journal.pone.0158856]]
-Wonni I, Cottyn B, Detemmerman L, Dao S, Ouedraogo L, Sarra S, Tekete C, Poussier S, Corral R, Triplett L, Koita O, Koebnik R, Leach J, Szurek B, Maes M, Verdier V (2014). Analysis of //Xanthomonas oryzae//  pv. //oryzicola//  population in Mali and Burkina Faso reveals a high level of genetic and pathogenic diversity. Phytopathology 104: 520-531. DOI: [[https://doi.org/10.1094/PHYTO-07-13-0213-R|10.1094/PHYTO-07-13-0213-R]]
+Wonni I, Cottyn B, Detemmerman L, Dao S, Ouedraogo L, Sarra S, Tekete C, Poussier S, Corral R, Triplett L, Koita O, Koebnik R, Leach J, Szurek B, Maes M, Verdier V (2014). Analysis of //Xanthomonas oryzae// pv. //oryzicola// population in Mali and Burkina Faso reveals a high level of genetic and pathogenic diversity. Phytopathology 104: 520-531. DOI: [[https://doi.org/10.1094/PHYTO-07-13-0213-R|10.1094/PHYTO-07-13-0213-R]]
-Wu S (2015). Structural and functional characterization of a //Xanthomonas//  type III effector. PhD dissertation. Link: [[https://vtechworks.lib.vt.edu/handle/10919/73219|https://vtechworks.lib.vt.edu/handle/10919/73219]]
+Wu S (2015). Structural and functional characterization of a //Xanthomonas// type III effector. PhD dissertation. Link: [[https://vtechworks.lib.vt.edu/handle/10919/73219|https://vtechworks.lib.vt.edu/handle/10919/73219]]
-Xie XW, Yu J, Xu JL, Zhou YL, Li ZK (2007). Introduction of a non-host gene //Rxo1//  cloned from maize resistant to rice bacterial leaf streak into rice varieties. Sheng Wu Gong Cheng Xue Bao [Chinese J. Biotechnol.] 23: 607-611. DOI: [[https://doi.org/10.1016/S1872-2075(07)60039-9|10.1016/S1872-2075(07)60039-9]]
+Xie XW, Yu J, Xu JL, Zhou YL, Li ZK (2007). Introduction of a non-host gene //Rxo1// cloned from maize resistant to rice bacterial leaf streak into rice varieties. Sheng Wu Gong Cheng Xue Bao [Chinese J. Biotechnol.] 23: 607-611. DOI: [[https://doi.org/10.1016/S1872-2075(07)60039-9|10.1016/S1872-2075(07)60039-9]]
-Zhao B, Ardales EY, Raymundo A, Bai J, Trick HN, Leach JE, Hulbert SH (2004). The //avrRxo1//  gene from the rice pathogen //Xanthomonas oryzae//  pv. //oryzicola//  confers a nonhost defense reaction on maize with resistance gene //Rxo1//. Mol. Plant Microbe Interact. 17: 771-779. DOI: [[https://doi.org/10.1094/MPMI.2004.17.7.771|10.1094/MPMI.2004.17.7.771]]
+Zhao B, Ardales EY, Raymundo A, Bai J, Trick HN, Leach JE, Hulbert SH (2004). The //avrRxo1// gene from the rice pathogen //Xanthomonas oryzae// pv. //oryzicola// confers a nonhost defense reaction on maize with resistance gene //Rxo1//. Mol. Plant Microbe Interact. 17: 771-779. DOI: [[https://doi.org/10.1094/MPMI.2004.17.7.771|10.1094/MPMI.2004.17.7.771]]
 Zhao B, Lin X, Poland J, Trick H, Leach J, Hulbert S (2005). A maize resistance gene functions against bacterial streak disease in rice. Proc. Natl. Acad. Sci. USA 102: 15383-15388. DOI: [[https://doi.org/10.1073/pnas.0503023102|10.1073/pnas.0503023102]]
+===== 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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