Show me your secret(ed) weapons: a multifaceted approach reveals a wide arsenal of type III‐secreted effectors in the cucurbit pathogenic bacterium Acidovorax citrulli and novel effectors in the Acidovorax genus

Jiménez‐Guerrero, Irene; Pérez‐Montaño, Francisco; Da Silva, Gustavo Mateus; Wagner, Naama; Shkedy, Dafna; Zhao, Mei; Pizarro, Lorena; Bar, Maya; Walcott, Ron; Sessa, Guido; Pupko, Tal; Burdman, Saul

doi:10.1111/mpp.12877

Title: Show me your secret(ed) weapons: a multifaceted approach reveals a wide arsenal of type III‐secreted effectors in the cucurbit pathogenic bacterium Acidovorax citrulli and novel effectors in the Acidovorax genus

Journal Article · Wed Oct 23 00:00:00 EDT 2019 · Molecular Plant Pathology

DOI:https://doi.org/10.1111/mpp.12877· OSTI ID:1571542

Jiménez‐Guerrero, Irene ^[1]; Pérez‐Montaño, Francisco ^[2]; Da Silva, Gustavo Mateus ^[1]; Wagner, Naama ^[3]; Shkedy, Dafna ^[3]; Zhao, Mei ^[4]; Pizarro, Lorena ^[5]; Bar, Maya ^[5]; Walcott, Ron ^[4]; Sessa, Guido ^[6]; Pupko, Tal ^[3];

^[1]

Department of Plant Pathology and Microbiology The Robert H. Smith Faculty of Agriculture, Food and Environment The Hebrew University of Jerusalem Rehovot Israel
Department of Plant Pathology and Microbiology The Robert H. Smith Faculty of Agriculture, Food and Environment The Hebrew University of Jerusalem Rehovot Israel, Department of Microbiology University of Seville Seville Spain
The School of Molecular Cell Biology and Biotechnology The George S. Wise Faculty of Life Sciences Tel Aviv University Tel Aviv Israel
Department of Plant Pathology University of Georgia Athens GA USA
Department of Plant Pathology and Weed Research Agricultural Research Organization The Volcani Center Bet Dagan Israel
School of Plant Sciences and Food Security The George S. Wise Faculty of Life Sciences Tel Aviv University Tel Aviv Israel

Summary The cucurbit pathogenic bacterium Acidovorax citrulli requires a functional type III secretion system (T3SS) for pathogenicity. In this bacterium, as with Xanthomonas and Ralstonia spp . , an AraC‐type transcriptional regulator, HrpX, regulates expression of genes encoding T3SS components and type III‐secreted effectors (T3Es) . The annotation of a sequenced A. citrulli strain revealed 11 T3E genes. Assuming that this could be an underestimation, we aimed to uncover the T3E arsenal of the A. citrulli model strain, M6. Thorough sequence analysis revealed 51 M6 genes whose products are similar to known T3Es. Furthermore, we combined machine learning and transcriptomics to identify novel T3Es. The machine‐learning approach ranked all A. citrulli M6 genes according to their propensity to encode T3Es. RNA‐Seq revealed differential gene expression between wild‐type M6 and a mutant defective in HrpX: 159 and 28 genes showed significantly reduced and increased expression in the mutant relative to wild‐type M6, respectively. Data combined from these approaches led to the identification of seven novel T3E candidates that were further validated using a T3SS‐dependent translocation assay. These T3E genes encode hypothetical proteins that seem to be restricted to plant pathogenic Acidovorax species. Transient expression in Nicotiana benthamiana revealed that two of these T3Es localize to the cell nucleus and one interacts with the endoplasmic reticulum. This study places A. citrulli among the ‘richest’ bacterial pathogens in terms of T3E cargo. It also revealed novel T3Es that appear to be involved in the pathoadaptive evolution of plant pathogenic Acidovorax species.

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Sponsoring Organization:: USDOE

OSTI ID:: 1571542

Alternate ID(s):: OSTI ID: 1571543

Journal Information:: Molecular Plant Pathology, Journal Name: Molecular Plant Pathology Vol. 21 Journal Issue: 1; ISSN 1464-6722

Publisher:: Wiley-BlackwellCopyright Statement

Country of Publication:: United Kingdom

Language:: English

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References (81)

Opening the Ralstonia solanacearum type III effector tool box: insights into host cell subversion mechanisms Deslandes, Laurent; Genin, Stephane Current Opinion in Plant Biology, Vol. 20 https://doi.org/10.1016/j.pbi.2014.05.002	journal	August 2014
Nicotiana benthamiana : Its History and Future as a Model for Plant–Pathogen Interactions Goodin, Michael M.; Zaitlin, David; Naidu, Rayapati A. Molecular Plant-Microbe Interactions, Vol. 21, Issue 8 https://doi.org/10.1094/MPMI-21-8-1015	journal	August 2008
Mechanisms of ROS Regulation of Plant Development and Stress Responses Huang, Honglin; Ullah, Farhan; Zhou, Dao-Xiu Frontiers in Plant Science, Vol. 10 https://doi.org/10.3389/fpls.2019.00800	journal	June 2019
Analyses of the secretomes of Erwinia amylovora and selected hrp mutants reveal novel type III secreted proteins and an effect of HrpJ on extracellular harpin levels Nissinen, Riitta M.; Ytterberg, A. Jimmy; Bogdanove, Adam J. Molecular Plant Pathology, Vol. 8, Issue 1 https://doi.org/10.1111/j.1364-3703.2006.00370.x	journal	January 2007
Cutadapt removes adapter sequences from high-throughput sequencing reads Martin, Marcel EMBnet.journal, Vol. 17, Issue 1 https://doi.org/10.14806/ej.17.1.200	journal	May 2011
MEME-ChIP: motif analysis of large DNA datasets Machanick, Philip; Bailey, Timothy L. Bioinformatics, Vol. 27, Issue 12 https://doi.org/10.1093/bioinformatics/btr189	journal	April 2011
STAR: ultrafast universal RNA-seq aligner Dobin, Alexander; Davis, Carrie A.; Schlesinger, Felix Bioinformatics, Vol. 29, Issue 1 https://doi.org/10.1093/bioinformatics/bts635	journal	October 2012
Photoactivation of GFP reveals protein dynamics within the endoplasmic reticulum membrane Runions, John; Brach, Thorsten; Kühner, Sebastian Journal of Experimental Botany, Vol. 57, Issue 1 https://doi.org/10.1093/jxb/eri289	journal	October 2005
HrpG regulates type II secretory proteins in Xanthomonas axonopodis pv. citri Yamazaki, Akihiro; Hirata, Hisae; Tsuyumu, Shinji Journal of General Plant Pathology, Vol. 74, Issue 2 https://doi.org/10.1007/s10327-008-0075-7	journal	February 2008
prhJ and hrpG, two new components of the plant signal-dependent regulatory cascade controlled by PrhA in Ralstonia solanacearum Brito, Belen; Marenda, Marc; Barberis, Patrick Molecular Microbiology, Vol. 31, Issue 1 https://doi.org/10.1046/j.1365-2958.1999.01165.x	journal	January 1999
Four new derivatives of the broad-host-range cloning vector pBBR1MCS, carrying different antibiotic-resistance cassettes Kovach, Michael E.; Elzer, Philip H.; Steven Hill, D. Gene, Vol. 166, Issue 1 https://doi.org/10.1016/0378-1119(95)00584-1	journal	December 1995
The vapB–vapC Operon of Acidovorax citrulli Functions as a Bona-fide Toxin–Antitoxin Module Shavit, Reut; Lebendiker, Mario; Pasternak, Zohar Frontiers in Microbiology, Vol. 6 https://doi.org/10.3389/fmicb.2015.01499	journal	January 2016
Transcript assembly and quantification by RNA-Seq reveals unannotated transcripts and isoform switching during cell differentiation Trapnell, Cole; Williams, Brian A.; Pertea, Geo Nature Biotechnology, Vol. 28, Issue 5 https://doi.org/10.1038/nbt.1621	journal	May 2010
Behind the lines–actions of bacterial type III effector proteins in plant cells Büttner, Daniela FEMS Microbiology Reviews, Vol. 40, Issue 6 https://doi.org/10.1093/femsre/fuw026	journal	August 2016
Combined prediction of Tat and Sec signal peptides with hidden Markov models Bagos, Pantelis G.; Nikolaou, Elisanthi P.; Liakopoulos, Theodore D. Bioinformatics, Vol. 26, Issue 22 https://doi.org/10.1093/bioinformatics/btq530	journal	September 2010
Acidovorax citrulli: generating basic and applied knowledge to tackle a global threat to the cucurbit industry: Acidovorax citrulli Burdman, Saul; Walcott, Ron Molecular Plant Pathology, Vol. 13, Issue 8 https://doi.org/10.1111/j.1364-3703.2012.00810.x	journal	June 2012
Differential expression analysis for sequence count data Anders, Simon; Huber, Wolfgang Genome Biology, Vol. 11, Issue 10 https://doi.org/10.1186/gb-2010-11-10-r106	journal	October 2010
The TAL Effector AvrBs3 from Xanthomonas campestris pv. vesicatoria Contains Multiple Export Signals and Can Enter Plant Cells in the Absence of the Type III Secretion Translocon Scheibner, Felix; Marillonnet, Sylvestre; Büttner, Daniela Frontiers in Microbiology, Vol. 8 https://doi.org/10.3389/fmicb.2017.02180	journal	November 2017
LocSigDB: a database of protein localization signals Negi, S.; Pandey, S.; Srinivasan, S. M. Database, Vol. 2015, Issue 0 https://doi.org/10.1093/database/bav003	journal	January 2015
Integrated Regulation of the Type III Secretion System and Other Virulence Determinants in Ralstonia solanacearum Valls, Marc; Genin, Stéphane; Boucher, Christian PLoS Pathogens, Vol. 2, Issue 8 https://doi.org/10.1371/journal.ppat.0020082	journal	January 2006
Repertoire, unified nomenclature and evolution of the Type III effector gene set in the Ralstonia solanacearum species complex Peeters, Nemo; Carrère, Sébastien; Anisimova, Maria BMC Genomics, Vol. 14, Issue 1 https://doi.org/10.1186/1471-2164-14-859	journal	January 2013
SignalP 4.0: discriminating signal peptides from transmembrane regions Petersen, Thomas Nordahl; Brunak, Søren; von Heijne, Gunnar Nature Methods, Vol. 8, Issue 10 https://doi.org/10.1038/nmeth.1701	journal	September 2011
Molecular, Physiological, and Host-Range Characterization of Acidovorax avenae subsp. citrulli Isolates from Watermelon and Melon in Israel Burdman, Saul; Kots, Nadia; Kritzman, Giora Plant Disease, Vol. 89, Issue 12 https://doi.org/10.1094/PD-89-1339	journal	December 2005
Plant–bacterial pathogen interactions mediated by type III effectors Feng, Feng; Zhou, Jian-Min Current Opinion in Plant Biology, Vol. 15, Issue 4 https://doi.org/10.1016/j.pbi.2012.03.004	journal	August 2012
Specific Binding of the Xanthomonas campestris pv. vesicatoria AraC-Type Transcriptional Activator HrpX to Plant-Inducible Promoter Boxes Koebnik, R.; Kruger, A.; Thieme, F. Journal of Bacteriology, Vol. 188, Issue 21 https://doi.org/10.1128/JB.00795-06	journal	August 2006
The Elements of Statistical Learning Hastie, Trevor; Friedman, Jerome; Tibshirani, Robert Springer Series in Statistics https://doi.org/10.1007/978-0-387-21606-5	book	January 2001
Evolution of Plant Pathogenesis in Pseudomonas syringae : A Genomics Perspective O'Brien, Heath E.; Thakur, Shalabh; Guttman, David S. Annual Review of Phytopathology, Vol. 49, Issue 1 https://doi.org/10.1146/annurev-phyto-072910-095242	journal	September 2011
Direct biochemical evidence for type III secretion-dependent translocation of the AvrBs2 effector protein into plant cells Casper-Lindley, C.; Dahlbeck, D.; Clark, E. T. Proceedings of the National Academy of Sciences, Vol. 99, Issue 12 https://doi.org/10.1073/pnas.122220299	journal	June 2002
Two Xanthomonas Extracellular Polygalacturonases, PghAxc and PghBxc, Are Regulated by Type III Secretion Regulators HrpX and HrpG and Are Required for Virulence Wang, Lifeng; Rong, Wei; He, Chaozu Molecular Plant-Microbe Interactions, Vol. 21, Issue 5 https://doi.org/10.1094/MPMI-21-5-0555	journal	May 2008
Allelic Variants of the Pseudomonas syringae Type III Effector HopZ1 Are Differentially Recognized by Plant Resistance Systems Zhou, Huanbin; Morgan, Robyn L.; Guttman, David S. Molecular Plant-Microbe Interactions, Vol. 22, Issue 2 https://doi.org/10.1094/MPMI-22-2-0176	journal	February 2009
Advantages of combined transmembrane topology and signal peptide prediction--the Phobius web server Kall, L.; Krogh, A.; Sonnhammer, E. L. L. Nucleic Acids Research, Vol. 35, Issue Web Server https://doi.org/10.1093/nar/gkm256	journal	May 2007
Pathogen perception by NLRs in plants and animals: Parallel worlds Duxbury, Zane; Ma, Yan; Furzer, Oliver J. BioEssays, Vol. 38, Issue 8 https://doi.org/10.1002/bies.201600046	journal	June 2016
Bacterial Type III Secretion Systems: Specialized Nanomachines for Protein Delivery into Target Cells Galán, Jorge E.; Lara-Tejero, Maria; Marlovits, Thomas C. Annual Review of Microbiology, Vol. 68, Issue 1 https://doi.org/10.1146/annurev-micro-092412-155725	journal	September 2014
Deletions in the Repertoire of Pseudomonas syringae pv. tomato DC3000 Type III Secretion Effector Genes Reveal Functional Overlap among Effectors Kvitko, Brian H.; Park, Duck Hwan; Velásquez, André C. PLoS Pathogens, Vol. 5, Issue 4 https://doi.org/10.1371/journal.ppat.1000388	journal	April 2009
A Membrane Microdomain-Associated Protein, Arabidopsis Flot1, Is Involved in a Clathrin-Independent Endocytic Pathway and Is Required for Seedling Development Li, Ruili; Liu, Peng; Wan, Yinglang The Plant Cell, Vol. 24, Issue 5 https://doi.org/10.1105/tpc.112.095695	journal	May 2012
Evidence for HrpXo-Dependent Expression of Type II Secretory Proteins in Xanthomonas oryzae pv. oryzae Furutani, A.; Tsuge, S.; Ohnishi, K. Journal of Bacteriology, Vol. 186, Issue 5 https://doi.org/10.1128/JB.186.5.1374-1380.2004	journal	February 2004
NEW EMBO MEMBER'S REVIEW: Getting across--bacterial type III effector proteins on their way to the plant cell Buttner, D. The EMBO Journal, Vol. 21, Issue 20 https://doi.org/10.1093/emboj/cdf536	journal	October 2002
Widespread distribution and fitness contribution of Xanthomonas campestris avirulence gene avrBs2 Kearney, Brian; Staskawicz, Brian J. Nature, Vol. 346, Issue 6282 https://doi.org/10.1038/346385a0	journal	July 1990
HrpXv, an AraC-type regulator, activates expression of five of the six loci in the hrp cluster of Xanthomonas campestris pv. vesicatoria. Wengelnik, K.; Bonas, U. Journal of Bacteriology, Vol. 178, Issue 12 https://doi.org/10.1128/JB.178.12.3462-3469.1996	journal	June 1996
Phytopathogen type III effector weaponry and their plant targets Block, Anna; Li, Guangyong; Fu, Zheng Qing Current Opinion in Plant Biology, Vol. 11, Issue 4 https://doi.org/10.1016/j.pbi.2008.06.007	journal	August 2008
Arginine/Lysine Residues in the Cytoplasmic Tail Promote ER Export of Plant Glycosylation Enzymes Schoberer, Jennifer; Vavra, Ulrike; Stadlmann, Johannes Traffic, Vol. 10, Issue 1 https://doi.org/10.1111/j.1600-0854.2008.00841.x	journal	October 2008
Differences in Pathogenicity between two Genetically Distinct Groups of Acidovorax avenae subsp. citrulli on Cucurbit Hosts Walcott, R. R.; Fessehaie, A.; Castro, A. C. Journal of Phytopathology, Vol. 152, Issue 5 https://doi.org/10.1111/j.1439-0434.2004.00841.x	journal	May 2004
Current Status of the Gene-For-Gene Concept Flor, H. H. Annual Review of Phytopathology, Vol. 9, Issue 1 https://doi.org/10.1146/annurev.py.09.090171.001423	journal	September 1971
A new mathematical model for relative quantification in real-time RT-PCR Pfaffl, M. W. Nucleic Acids Research, Vol. 29, Issue 9 https://doi.org/10.1093/nar/29.9.e45	journal	May 2001
The plant immune system Jones, Jonathan D. G.; Dangl, Jeffery L. Nature, Vol. 444, Issue 7117 https://doi.org/10.1038/nature05286	journal	November 2006
Genome-Scale Identification of Legionella pneumophila Effectors Using a Machine Learning Approach Burstein, David; Zusman, Tal; Degtyar, Elena PLoS Pathogens, Vol. 5, Issue 7 https://doi.org/10.1371/journal.ppat.1000508	journal	July 2009
A high-throughput, near-saturating screen for type III effector genes from Pseudomonas syringae Chang, J. H.; Urbach, J. M.; Law, T. F. Proceedings of the National Academy of Sciences, Vol. 102, Issue 7 https://doi.org/10.1073/pnas.0409660102	journal	February 2005
The Type III Secreted Effector DspE Is Required Early in Solanum tuberosum Leaf Infection by Pectobacterium carotovorum to Cause Cell Death, and Requires Wx(3–6)D/E Motifs Hogan, Clifford S.; Mole, Beth M.; Grant, Sarah R. PLoS ONE, Vol. 8, Issue 6 https://doi.org/10.1371/journal.pone.0065534	journal	June 2013
Comparative Analysis of Type III Secreted Effector Genes Reflects Divergence of Acidovorax citrulli Strains into Three Distinct Lineages Eckshtain-Levi, Noam; Munitz, Tamar; Živanović, Marija Phytopathology, Vol. 104, Issue 11 https://doi.org/10.1094/PHYTO-12-13-0350-R	journal	November 2014
Characterization of the Xanthomonas AvrXv4 Effector, a SUMO Protease Translocated into Plant Cells Roden, Julie; Eardley, Leah; Hotson, Andrew Molecular Plant-Microbe Interactions, Vol. 17, Issue 6 https://doi.org/10.1094/MPMI.2004.17.6.633	journal	June 2004
HrpG and HrpX Play Global Roles in Coordinating Different Virulence Traits of Xanthomonas axonopodis pv. citri Guo, Yinping; Figueiredo, Francisco; Jones, Jeffery Molecular Plant-Microbe Interactions, Vol. 24, Issue 6 https://doi.org/10.1094/MPMI-09-10-0209	journal	June 2011
Simple and rapid fluorimetric method for DNA microassay Kapuściński, Jan; Skoczylas, Bogna Analytical Biochemistry, Vol. 83, Issue 1 https://doi.org/10.1016/0003-2697(77)90533-4	journal	November 1977
HrpG, a Key hrp Regulatory Protein of Xanthomonas campestris pv. vesicatoria Is Homologous to Two-Component Response Regulators Wengelnik, Kai Molecular Plant-Microbe Interactions, Vol. 9, Issue 8 https://doi.org/10.1094/MPMI-9-0704	journal	January 1996
Gene-For-Gene Relationships Specifying Disease Resistance in Xanthomonas campestris pv. vesicatoria - Pepper Interactions Minsavage, G. V. Molecular Plant-Microbe Interactions, Vol. 3, Issue 1 https://doi.org/10.1094/MPMI-3-041	journal	January 1990
A genetic screen to isolate type III effectors translocated into pepper cells during Xanthomonas infection Roden, J. A.; Belt, B.; Ross, J. B. Proceedings of the National Academy of Sciences, Vol. 101, Issue 47 https://doi.org/10.1073/pnas.0407383101	journal	November 2004
Expression of the Bs2 pepper gene confers resistance to bacterial spot disease in tomato Tai, T. H.; Dahlbeck, D.; Clark, E. T. Proceedings of the National Academy of Sciences, Vol. 96, Issue 24 https://doi.org/10.1073/pnas.96.24.14153	journal	November 1999
Type IV Pili Are Required for Virulence, Twitching Motility, and Biofilm Formation of Acidovorax avenae subsp. citrulli Bahar, Ofir; Goffer, Tal; Burdman, Saul Molecular Plant-Microbe Interactions, Vol. 22, Issue 8 https://doi.org/10.1094/MPMI-22-8-0909	journal	August 2009
An improved suicide vector for construction of chromosomal insertion mutations in bacteria Penfold, Robert J.; Pemberton, John M. Gene, Vol. 118, Issue 1 https://doi.org/10.1016/0378-1119(92)90263-O	journal	September 1992
Insights from the Genome Sequence of Acidovorax citrulli M6, a Group I Strain of the Causal Agent of Bacterial Fruit Blotch of Cucurbits Eckshtain-Levi, Noam; Shkedy, Dafna; Gershovits, Michael Frontiers in Microbiology, Vol. 7 https://doi.org/10.3389/fmicb.2016.00430	journal	April 2016
Multiple Approaches to a Complete Inventory of Pseudomonas syringae pv. tomato DC3000 Type III Secretion System Effector Proteins Schechter, Lisa M.; Vencato, Monica; Jordan, Katy L. Molecular Plant-Microbe Interactions, Vol. 19, Issue 11 https://doi.org/10.1094/MPMI-19-1180	journal	November 2006
Involvement of hrpX and hrpG in the Virulence of Acidovorax citrulli Strain Aac5, Causal Agent of Bacterial Fruit Blotch in Cucurbits Zhang, Xiaoxiao; Zhao, Mei; Yan, Jianpei Frontiers in Microbiology, Vol. 9 https://doi.org/10.3389/fmicb.2018.00507	journal	March 2018
Characterization of the cis-Acting Regulatory Element Controlling HrpB-Mediated Activation of the Type III Secretion System and Effector Genes in Ralstonia solanacearum Cunnac, S.; Boucher, C.; Genin, S. Journal of Bacteriology, Vol. 186, Issue 8 https://doi.org/10.1128/JB.186.8.2309-2318.2004	journal	April 2004
Complete Assembly of the Genome of an Acidovorax citrulli Strain Reveals a Naturally Occurring Plasmid in This Species Yang, Rongzhi; Santos Garcia, Diego; Pérez Montaño, Francisco Frontiers in Microbiology, Vol. 10 https://doi.org/10.3389/fmicb.2019.01400	journal	June 2019
Fiji: an open-source platform for biological-image analysis Schindelin, Johannes; Arganda-Carreras, Ignacio; Frise, Erwin Nature Methods, Vol. 9, Issue 7 https://doi.org/10.1038/nmeth.2019	journal	June 2012
Pathogenomics of the Ralstonia solanacearum Species Complex Genin, Stéphane; Denny, Timothy P. Annual Review of Phytopathology, Vol. 50, Issue 1 https://doi.org/10.1146/annurev-phyto-081211-173000	journal	September 2012
Bacterial fruit blotch: A threat to the cucurbit industry Bahar, Ofir; Burdman, Saul Israel Journal of Plant Sciences, Vol. 58, Issue 1 https://doi.org/10.1560/IJPS.58.1.19	journal	September 2010
Wound signalling in plants León, José; Rojo, Enrique; Sánchez‐Serrano, José J. Journal of Experimental Botany, Vol. 52, Issue 354 https://doi.org/10.1093/jexbot/52.354.1	journal	January 2001
Genome-Wide Analysis of Gene Expression in Ralstonia solanacearum Reveals That the hrpB Gene Acts as a Regulatory Switch Controlling Multiple Virulence Pathways Occhialini, Alessandra; Cunnac, Sébastien; Reymond, Nancie Molecular Plant-Microbe Interactions, Vol. 18, Issue 9 https://doi.org/10.1094/MPMI-18-0938	journal	September 2005
The type III effectors of Xanthomonas White, Frank F.; Potnis, Neha; Jones, Jeffrey B. Molecular Plant Pathology, Vol. 10, Issue 6 https://doi.org/10.1111/j.1364-3703.2009.00590.x	journal	November 2009
Gateway-compatible vectors for plant functional genomics and proteomics Earley, Keith W.; Haag, Jeremy R.; Pontes, Olga The Plant Journal, Vol. 45, Issue 4 https://doi.org/10.1111/j.1365-313X.2005.02617.x	journal	February 2006
Targeting of plant pattern recognition receptor-triggered immunity by bacterial type-III secretion system effectors Macho, Alberto P.; Zipfel, Cyril Current Opinion in Microbiology, Vol. 23 https://doi.org/10.1016/j.mib.2014.10.009	journal	February 2015
Functional characterization of the Xcs and Xps type II secretion systems from the plant pathogenic bacterium Xanthomonas campestris pv vesicatoria Szczesny, Robert; Jordan, Matthias; Schramm, Claudia New Phytologist, Vol. 187, Issue 4 https://doi.org/10.1111/j.1469-8137.2010.03312.x	journal	June 2010
Identification of Novel Coxiella burnetii Icm/Dot Effectors and Genetic Analysis of Their Involvement in Modulating a Mitogen-Activated Protein Kinase Pathway Lifshitz, Ziv; Burstein, David; Schwartz, Kierstyn Infection and Immunity, Vol. 82, Issue 9 https://doi.org/10.1128/IAI.01729-14	journal	June 2014
Revealing the inventory of type III effectors in Pantoea agglomerans gall-forming pathovars using draft genome sequences and a machine-learning approach : Inventory of Nissan, Gal; Gershovits, Michael; Morozov, Michael Molecular Plant Pathology, Vol. 19, Issue 2 https://doi.org/10.1111/mpp.12528	journal	February 2017
Investigating Intraspecific Variation of Acidovorax avenae subsp. citrulli Using DNA Fingerprinting and Whole Cell Fatty Acid Analysis Walcott, R. R.; Langston, D. B.; Sanders, F. H. Phytopathology, Vol. 90, Issue 2 https://doi.org/10.1094/PHYTO.2000.90.2.191	journal	February 2000
Expression and localization of HrpA1, a protein of Xanthomonas campestris pv. vesicatoria essential for pathogenicity and induction ofthe hypersensitive reaction. Wengelnik, K.; Marie, C.; Russel, M. Journal of Bacteriology, Vol. 178, Issue 4 https://doi.org/10.1128/jb.178.4.1061-1069.1996	journal	February 1996
The Sequence Alignment/Map format and SAMtools Li, H.; Handsaker, B.; Wysoker, A. Bioinformatics, Vol. 25, Issue 16 https://doi.org/10.1093/bioinformatics/btp352	journal	June 2009
Random Forests Breiman, Leo Machine Learning, Vol. 45, Issue 1, p. 5-32 https://doi.org/10.1023/A:1010933404324	journal	January 2001
*Unified nomenclature for broadly conserved hrp* genes of phytopathogenic bacteria** Bogdanove, Adam J.; Beer, Steven V.; Bonas, Ulla Molecular Microbiology, Vol. 20, Issue 3 https://doi.org/10.1046/j.1365-2958.1996.5731077.x	journal	May 1996
Regulation and secretion of Xanthomonas virulence factors Büttner, Daniela; Bonas, Ulla FEMS Microbiology Reviews, Vol. 34, Issue 2 https://doi.org/10.1111/j.1574-6976.2009.00192.x	journal	March 2010
Identification of novel X anthomonas euvesicatoria type III effector proteins by a machine-learning approach : Novel Teper, Doron; Burstein, David; Salomon, Dor Molecular Plant Pathology, Vol. 17, Issue 3 https://doi.org/10.1111/mpp.12288	journal	August 2015

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