Table of Contents

Type III effectors

Link to the original Xanthomonas //Resource @ xanthomonas.org

Multi-FASTA-formatted list of type III effectors from Xanthomonas

List of type III effectors in Xanthomonas (for download from NCBI)

Pseudomonas–Plant Interaction website (Lindeberg et al., 2005)

RalstoT3Edb (Peeters et al., 2013; Sabbagh et al., 2019)

Review papers on type III effectors

Software, databases and websites for type III effectors

Empty template - Example 1: XopAU - Example 2: XopB

Xanthomonas type III effectors

Class Family Synonyms Related proteins RefSeq ID (GenBank ID) Function / Features
AvrBs1 AvrBs1 AvrA WP_011037255.1
AvrBs2 AvrBs2 WP_039418336.1 Glycerophosphodiester phosphodiesterase domain
AvrBs3 AvrBs3 PthA, PthB, PthN, PthXo, AvrXa7, AvrXa27, TALE RipTAL WP_011052943.1 TAL effector repeat; Transcription activator in eukaryotic host cell; Nuclear localization
XopB XopB HopD1 (HopPtoD1, AvrPphD1), RipD WP_039417318.1
XopC XopC1 RipC2 WP_011347616.1 Phosphoribosyltransferase domain; Haloacid dehalogenase-like hydrolase
XopC XopC2 RipC1 WP_041183113.1
XopD XopD WP_228949438.1 C48-family SUMO cysteine protease (Ulp1 protease family); EAR motif; DNA binding; Nuclear localization
XopE XopE1 AvrXacE1 HopX (AvrPphE), RipE1 WP_011345998.1 Putative transglutaminase
XopE XopE2 AvrXacE3, AvrXccE1 HopX (AvrPphE), RipE1 WP_011347479.1 Putative transglutaminase
XopE XopE3 AvrXacE2 HopX (AvrPphE), RipE1 WP_011052114.1 Putative transglutaminase
XopE XopE4 RipE1 WP_244170787.1 Putative transglutaminase
XopE XopE5 HopX (AvrPphE), RipE1 WP_260607984.1 Putative transglutaminase
XopF XopF1 Hpa4 WP_011346095.1
XopF XopF2 WP_011348008.1
XopF XopF3 WP_039005675.1
XopG XopG1 HopH (HopPtoH), RipAX2 WP_011346758.1 Peptidase_M91 superfamily; HEXXH motif, typical of zinc metallopeptidases
XopG XopG2 HopH (HopPtoH), RipAX2 WP_011038360.1 Peptidase_M91 superfamily; HEXXH motif, typical of zinc metallopeptidases
XopG XopG3 HopH (HopPtoH), RipAX1 WP_084217840.1 Peptidase_M91 superfamily; HEXXH motif, typical of zinc metallopeptidases
XopH XopH1 AvrBs1.1, AvrBs7 HopAO1 (HopPtoD2), RipBL WP_011345706.1 Protein tyrosine phosphatase-like phytase; Tyrosine-specific protein phosphatase
XopH XopH2 HopAO1 (HopPtoD2), RipBL WP_010377341.1 Protein tyrosine phosphatase-like phytase; Tyrosine-specific protein phosphatase
XopI XopI1 WP_011346406.1 F-box domain
XopI XopI2 WP_010367684.1 F-box domain
XopJ XopJ1 HopZ1, RipP1 WP_011347382.1 Ser/Thr acetyltransferase
XopJ XopJ2 AvrBsT HopZ1, RipP1 WP_074052319.1 Ser/Thr acetyltransferase
XopJ XopJ3 AvrRxv HopZ1, RipP1 WP_011346137.1 Ser/Thr acetyltransferase
XopJ XopJ4 AvrXv4 HopZ1, RipP1 (formerly PopP1) WP_008572727.1 Ser/Thr acetyltransferase
XopJ XopJ5 AvrXccB HopZ1, RipK, RipP1 WP_228442257.1 Ser/Thr acetyltransferase
XopJ XopJ6 RipP2 (formerly PopP2) WP_196765268.1 Ser/Thr acetyltransferase
XopK XopK WP_027703763.1
XopL XopL RipAC (formerly PopC) WP_218498620.1 LRR motif; LRR domain
XopM XopM WP_011346113.1
XopN XopN HopAU1 WP_011348010.1 ARM/HEAT repeat
XopO XopO HopK1 (HopPtoK, HolPtoAB) N-terminal domain, AvrRps4 WP_011346566.1 AvrRps4 C-terminal region
XopP XopP RipH3 (formerly Hlk) WP_104613784.1
XopQ XopQ HopQ1 (HolPtoQ), RipB WP_011349176.1 Inosine/uridine-preferring nucleoside hydrolase
XopR XopR WP_011260681.1
XopS XopS WP_039418869.1
XopT XopT WP_199285673.1 Plectin-repeat
XopU XopU WP_011408937.1
XopV XopV RipAD WP_011409498.1
XopW XopW WP_228329674.1
XopX XopX HopAE1 (HolPsyAE), RipBI WP_011346212.1
XopY XopY WP_011408080.1
XopZ XopZ1 HopAS1 WP_011259177.1
XopZ XopZ2 HopAS1 WP_039421390.1
XopAA XopAA Ecf HopAE1 (HolPsyAE), weakly related to RipBI WP_041855088.1 Early chlorosis factor; Proteasome/cyclosome repeat
XopAB XopAB weakly related to XopN WP_011409110.1
XopAC XopAC AvrAC RipAC (formerly PopC) WP_011269629.1 LRR motif; LRR domain; Fido domain; Vascular hypersensitivity in Arabidopsis landrace Col-0
XopAD XopAD RipS3 WP_011409710.1 SKWP repeat protein; Armadillo-like helical repeat; Armadillo-type fold; RelA/SpoT superfamily
XopAE XopAE HpaF/HpaG RipAC (formerly PopC) WP_011050288.1 LRR motif; LRR domain
XopAF XopAF1 AvrXv3 HopAF1 (HopPtoJ), RipBD WP_008577605.1
XopAF XopAF2 HopAF1 (HopPtoJ), RipBD WP_227479740.1
XopAG XopAG1 AvrGf1 HopG1 (HopPtoG), HolPtoW, RipO1 WP_272820829.1
XopAG XopAG2 AvrGf2 HopG1 (HopPtoG), HolPtoW, RipO1 WP_007970248.1
XopAH XopAH AvrXccC AvrB/AvrC (AvrPphC) WP_011037263.1 AvrB/AvrC-family avirulence protein
XopAI XopAI HopO1 (HopPtoO, HopPtoS), HopAI1 (HolPtoAI) WP_011052119.1 NAD:arginine ADP-ribosyltransferase
XopAJ XopAJ AvrRxo1 WP_014504815.1 P-loop containing nucleoside triphosphate hydrolase
XopAK XopAK HopK1 (HopPtoK, HolPtoAB) C-terminal domain, RipBQ WP_269466020.1
XopAL XopAL1 Eop3, weakly similar to HopX, RipE2 WP_274360846.1
XopAL XopAL2 Eop3, RS_T3E_Hyp14 WP_012437264.1
XopAM XopAM HopR1, RipR WP_012438997.1 AvrE-family effector
XopAN XopAN
XopAO XopAO AvrRpm1, RipBA WP_162267513.1
XopAP XopAP RipAL WP_236504155.1 α/β hydrolase fold; Class-3 lipase
XopAQ XopAQ RipAH/RipAG WP_233366621.1
XopAR XopAR RipBE (APO95022.1)
XopAS XopAS HopAS1 WP_229015407.1
XopAT XopAT (AEL06363.1)
XopAU XopAU WP_041855031.1 Serine/threonine kinase; Protein kinase domain; ATP-binding site
XopAV XopAV1 WP_065628638.1
XopAV XopAV2 WP_011269951.1
XopAW XopAW WP_011348129.1 Calcium-binding protein; EF-hand domain; Calcium-binding site
XopAX XopAX WP_041854960.1
XopAY XopAY
XopAZ XopAZ WP_104549896.1 SlpA superfamily; FKBP-type peptidyl-prolyl cis-trans isomerase
XopBA XopBA HopW1, RipBP WP_227478587.1
XopBB XopBB HopF2 (AvrPphF) WP_251761698.1
XopBC = XopAV class
XopBD = XopAT class
XopBE = XopC class
XopBF = XopAV class
XopBG XopBG WP_145953988.1

Avirulence or type III-secreted proteins that are not considered effectors in a narrow sense

Name Synonyms Related proteins RefSeq ID (GenBank ID) Function / Features Reference
AvrXccA1 AvrXca WP_011039290.1 Avirulence protein, perhaps not a T3E Parker et al., 1993
AvrXccA2 WP_274318562.1 Avirulence protein, perhaps not a T3E
HpaA WP_011346100.1 Type III secretion control protein, perhaps not a T3E Lorenz et al., 2008
HpaT WP_058196718.1 Putative translocon protein, not a T3E Pesce et al., 2017
HrpB2 WP_008575450.1 Putative inner rod protein, not a T3E Rossier et al., 2000; Scheibner et al., 2016
HrpE HrpE1 WP_011346098.1 Major subunit of the Hrp pilus Weber et al., 2005; Weber & Koebnik, 2005; Weber & Koebnik, 2006; Gottig et al., 2018
HrpF RipF (formerly PopF) WP_011346092.1 Putative translocon protein, not a T3E Huguet & Bonas, 1997; Meyer et al., 2006
HrpW RipW (formerly PopW) WP_005926112.1 Pectate lyase, perhaps not a T3E Charkowski et al., 1998; Li et al., 2010
XopA Hpa1/HpaG WP_011346111.1 Harpin, perhaps not a T3E Zhu et al., 2000; Kim et al., 2004; Sgro et al., 2012; Wang et al., 2018

References

Charkowski AO, Alfano JR, Preston G, Yuan J, He SY, Collmer A (1998). The Pseudomonas syringae pv. tomato HrpW protein has domains similar to harpins and pectate lyases and can elicit the plant hypersensitive response and bind to pectate. J. Bacteriol. 180: 5211-5217. DOI: 10.1128/JB.180.19.5211-5217.1998

Gottig N, Vranych CV, Sgro GG, Piazza A, Ottado J (2018). HrpE, the major component of the Xanthomonas type three protein secretion pilus, elicits plant immunity responses. Sci. Rep. 8: 9842. DOI: 10.1038/s41598-018-27869-1

Huguet E, Bonas U (1997). HrpF of Xanthomonas campestris pv. vesicatoria encodes an 87-kDa protein with homology to NoIX of Rhizobium fredii. Mol. Plant Microbe Interact. 10: 488-498. DOI: 10.1094/MPMI.1997.10.4.488

Kim JG, Jeon E, Oh J, Moon JS, Hwang I (2004). Mutational analysis of Xanthomonas harpin HpaG identifies a key functional region that elicits the hypersensitive response in nonhost plants. J. Bacteriol. 186: 6239-6247. DOI: 10.1128/JB.186.18.6239-6247.2004

Li JG, Liu HX, Cao J, Chen LF, Gu C, Allen C, Guo JH (2010). PopW of Ralstonia solanacearum, a new two-domain harpin targeting the plant cell wall. Mol. Plant Pathol. 11: 371-381. DOI: 10.1111/j.1364-3703.2010.00610.x

Lindeberg M, Stavrinides J, Chang JH, Alfano JR, Collmer A, Dangl JL, Greenberg JT, Mansfield JW, Guttman DS (2005). Proposed guidelines for a unified nomenclature and phylogenetic analysis of type III Hop effector proteins in the plant pathogen Pseudomonas syringae. Mol. Plant Microbe Interact. 18: 275-282. DOI: 10.1094/MPMI-18-0275

Lorenz C, Kirchner O, Egler M, Stuttmann J, Bonas U, Büttner D (2008). HpaA from Xanthomonas is a regulator of type III secretion. Mol. Microbiol. 69: 344-360. DOI: 10.1111/j.1365-2958.2008.06280.x

Meyer D, Cunnac S, Guéneron M, Declercq C, Van Gijsegem F, Lauber E, Boucher C, Arlat M (2006). PopF1 and PopF2, two proteins secreted by the type III protein secretion system of Ralstonia solanacearum, are translocators belonging to the HrpF/NopX family. J. Bacteriol. 188: 4903-4917. DOI: 10.1128/JB.00180-06

Parker JE, Barber CE, Fan MJ, Daniels MJ (1993). Interaction of Xanthomonas campestris with Arabidopsis thaliana: characterization of a gene from X. c. pv. raphani that confers avirulence to most A. thaliana accessions. Mol. Plant Microbe Interact. 6: 216-224. DOI: 10.1094/mpmi-6-216

Peeters N, Carrère S, Anisimova M, Plener L, Cazalé AC, Genin S (2013). Repertoire, unified nomenclature and evolution of the Type III effector gene set in the Ralstonia solanacearum species complex. BMC Genomics 14: 859. DOI: 10.1186/1471-2164-14-859

Pesce C, Jacobs JM, Berthelot E, Perret M, Vancheva T, Bragard C, Koebnik R (2017). Comparative genomics identifies a novel conserved protein, HpaT, in proteobacterial type III secretion systems that do not possess the putative translocon protein HrpF. Front. Microbiol. 8: 1177. DOI: 10.3389/fmicb.2017.01177

Rossier O, Van den Ackerveken G, Bonas U (2000). HrpB2 and HrpF from Xanthomonas are type III-secreted proteins and essential for pathogenicity and recognition by the host plant. Mol. Microbiol. 38: 828-838. DOI: 10.1046/j.1365-2958.2000.02173.x

Sabbagh CRR, Carrere S, Lonjon F, Vailleau F, Macho AP, Genin S, Peeters N (2019). Pangenomic type III effector database of the plant pathogenic Ralstonia spp. PeerJ 7: e7346. DOI: 10.7717/peerj.7346

Scheibner F, Schulz S, Hausner J, Marillonnet S, Büttner D (2016). Type III-dependent translocation of HrpB2 by a nonpathogenic hpaABC mutant of the plant-pathogenic bacterium Xanthomonas campestris pv. vesicatoria. Appl. Environ. Microbiol. 82: 3331-3347. DOI: 10.1128/AEM.00537-16

Sgro GG, Ficarra FA, Dunger G, Scarpeci TE, Valle EM, Cortadi A, Orellano EG, Gottig N, Ottado J (2012). Contribution of a harpin protein from Xanthomonas axonopodis pv. citri to pathogen virulence. Mol. Plant Pathol. 13: 1047-1059. DOI: 10.1111/j.1364-3703.2012.00814.x

Wang X, Zhang L, Ji H, Mo X, Li P, Wang J, Dong H (2018). Hpa1 is a type III translocator in Xanthomonas oryzae pv. oryzae. BMC Microbiol. 18: 105. DOI: 10.1186/s12866-018-1251-3

Weber E, Koebnik R (2005). Domain structure of HrpE, the Hrp pilus subunit of Xanthomonas campestris pv. vesicatoria. J. Bacteriol. 187: 6175-6186. DOI: 10.1128/JB.187.17.6175-6186.2005

Weber E, Koebnik R (2006). Positive selection of the Hrp pilin HrpE of the plant pathogen Xanthomonas. J. Bacteriol. 188: 1405-1410. DOI: 10.1128/JB.188.4.1405-1410.2006

Weber E, Ojanen-Reuhs T, Huguet E, Hause G, Romantschuk M, Korhonen TK, Bonas U, Koebnik R (2005). The type III-dependent Hrp pilus is required for productive interaction of Xanthomonas campestris pv. vesicatoria with pepper host plants. J. Bacteriol. 187: 2458-2468. DOI: 10.1128/JB.187.7.2458-2468.2005

Zhu W, MaGbanua MM, White FF (2000). Identification of two novel hrp-associated genes in the hrp gene cluster of Xanthomonas oryzae pv. oryzae. J. Bacteriol. 182: 1844-1853. DOI: 10.1128/JB.182.7.1844-1853.2000