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Comparative genomics reveals the in planta-secreted Verticillium dahliae Av2 effector protein recognized in tomato plants that carry the V2 resistance locus.

Identifieur interne : 000195 ( Main/Exploration ); précédent : 000194; suivant : 000196

Comparative genomics reveals the in planta-secreted Verticillium dahliae Av2 effector protein recognized in tomato plants that carry the V2 resistance locus.

Auteurs : Edgar A. Chavarro-Carrero [Pays-Bas] ; Jasper P. Vermeulen [Pays-Bas] ; David E Torres [Pays-Bas] ; Toshiyuki Usami [Japon] ; Henk J. Schouten [Pays-Bas] ; Yuling Bai [Pays-Bas] ; Michael F. Seidl [Pays-Bas] ; Bart P H J. Thomma [Pays-Bas, Allemagne]

Source :

RBID : pubmed:33078534

Abstract

Plant pathogens secrete effector molecules during host invasion to promote colonization. However, some of these effectors become recognized by host receptors to mount a defence response and establish immunity. Recently, a novel resistance was identified in wild tomato, mediated by the single dominant V2 locus, to control strains of the soil-borne vascular wilt fungus Verticillium dahliae that belong to race 2. With comparative genomics of race 2 strains and resistance-breaking race 3 strains, we identified the avirulence effector that activates V2 resistance, termed Av2. We identified 277 kb of race 2-specific sequence comprising only two genes encoding predicted secreted proteins that are expressed during tomato colonization. Subsequent functional analysis based on genetic complementation into race 3 isolates and targeted deletion from the race 1 isolate JR2 and race 2 isolate TO22 confirmed that one of the two candidates encodes the avirulence effector Av2 that is recognized in V2 tomato plants. Two Av2 allelic variants were identified that encode Av2 variants that differ by a single acid. Thus far, a role in virulence could not be demonstrated for either of the two variants.

DOI: 10.1111/1462-2920.15288
PubMed: 33078534


Affiliations:


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Le document en format XML

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<div type="abstract" xml:lang="en">Plant pathogens secrete effector molecules during host invasion to promote colonization. However, some of these effectors become recognized by host receptors to mount a defence response and establish immunity. Recently, a novel resistance was identified in wild tomato, mediated by the single dominant V2 locus, to control strains of the soil-borne vascular wilt fungus Verticillium dahliae that belong to race 2. With comparative genomics of race 2 strains and resistance-breaking race 3 strains, we identified the avirulence effector that activates V2 resistance, termed Av2. We identified 277 kb of race 2-specific sequence comprising only two genes encoding predicted secreted proteins that are expressed during tomato colonization. Subsequent functional analysis based on genetic complementation into race 3 isolates and targeted deletion from the race 1 isolate JR2 and race 2 isolate TO22 confirmed that one of the two candidates encodes the avirulence effector Av2 that is recognized in V2 tomato plants. Two Av2 allelic variants were identified that encode Av2 variants that differ by a single acid. Thus far, a role in virulence could not be demonstrated for either of the two variants.</div>
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<ReferenceList>
<Title>References</Title>
<Reference>
<Citation>Alexander, L.J. (1962) Susceptibility of certain Verticillium-resistant tomato varieties to an Ohio isolate of the pathogen. Phytopathology 52: 998-1000.</Citation>
</Reference>
<Reference>
<Citation>Anh, V.L., Inoue, Y., Asuke, S., Vy, T.T.P., Anh, N.T., Wang, S., et al. (2018) Rmg8 and Rmg7, wheat genes for resistance to the wheat blast fungus, recognize the same avirulence gene AVR-Rmg8. Mol Plant Pathol 19: 1252-1256.</Citation>
</Reference>
<Reference>
<Citation>Baergen, K.D., Hewitt, J.D., and St. Clair, D.A. (1993) Resistance of tomato genotypes to four isolates of Verticillium dahliae race 2. HortScience 28: 833-836.</Citation>
</Reference>
<Reference>
<Citation>Bertels, F., Silander, O.K., Pachkov, M., Rainey, P.B., and Van Nimwegen, E. (2014) Automated reconstruction of whole-genome phylogenies from short-sequence reads. Mol Biol Evol 31: 1077-1088.</Citation>
</Reference>
<Reference>
<Citation>Bourras, S., Kunz, L., Xue, M., Praz, C.R., Müller, M.C., Kälin, C., et al. (2019) The AvrPm3-Pm3 effector-NLR interactions control both race-specific resistance and host-specificity of cereal mildews on wheat. Nat Commun 10: 1-16.</Citation>
</Reference>
<Reference>
<Citation>Bourras, S., McNally, K.E., Ben-David, R., Parlange, F., Roffler, S., Praz, C.R., et al. (2015) Multiple avirulence loci and allele-specific effector recognition control the Pm3 race-specific resistance of wheat to powdery mildew. Plant Cell 27: 2991-3012.</Citation>
</Reference>
<Reference>
<Citation>Brown, J.K.M. (2015) Durable resistance of crops to disease: a Darwinian perspective. Annu Rev Phytopathol 53: 513-539.</Citation>
</Reference>
<Reference>
<Citation>Chen, J., Upadhyaya, N.M., Ortiz, D., Sperschneider, J., Li, F., Bouton, C., et al. (2017) Loss of AvrSr50 by somatic exchange in stem rust leads to virulence for Sr50 resistance in wheat. Science 358: 1607-1610.</Citation>
</Reference>
<Reference>
<Citation>Cirulli, M. (1969) Un isolato di Verticillium dahliae Kleb. virulento verso varietà resistenti di Pomodoro. Phytopathol Mediterr 8: 132-136.</Citation>
</Reference>
<Reference>
<Citation>Cook, D.E., Kramer, M., Seidl, M.F., and Thomma, B.P. (2020) Chromatin features define adaptive genomic regions in a fungal plant pathogen. BioRxiv https://dx.doi.org/10.1101/2020.01.27.921486.</Citation>
</Reference>
<Reference>
<Citation>Cook, D.E., Mesarich, C.H., and Thomma, B.P.H.J. (2015) Understanding plant immunity as a surveillance system to detect invasion. Annu Rev Phytopathol 53: 541-563.</Citation>
</Reference>
<Reference>
<Citation>Dangl, J.L., Horvath, D.M., and Staskawicz, B.J. (2013) Pivoting the plant immune system. Science 341: 745-751.</Citation>
</Reference>
<Reference>
<Citation>Dangl, J.L., and Jones, J.D.G. (2001) Plant pathogens and integrated defence responses to infection. Nature 411: 826-833.</Citation>
</Reference>
<Reference>
<Citation>Darvill, A.G., and Albersheim, P. (1984) Phytoalexins and their elicitors-a defense against microbial infection in plants. Annu Rev Plant Physiol 35: 243-275.</Citation>
</Reference>
<Reference>
<Citation>de Jonge, R., Bolton, M.D., Kombrink, A., Van Den Berg, G.C.M., Yadeta, K.A., and Thomma, B.P.H.J. (2013) Extensive chromosomal reshuffling drives evolution of virulence in an asexual pathogen. Genome Res 23: 1271-1282.</Citation>
</Reference>
<Reference>
<Citation>de Jonge, R., van Esse, H.P., Maruthachalam, K., Bolton, M.D., Santhanam, P., Saber, M.K., et al. (2012) Tomato immune receptor Ve1 recognizes effector of multiple fungal pathogens uncovered by genome and RNA sequencing. Proc Natl Acad Sci U S A 109: 5110-5115.</Citation>
</Reference>
<Reference>
<Citation>Depotter, J.R.L., Shi-Kunne, X., Missonnier, H., Liu, T., Faino, L., van den Berg, G.C.M., et al. (2019) Dynamic virulence-related regions of the plant pathogenic fungus Verticillium dahliae display enhanced sequence conservation. Mol Ecol 28: 3482-3495.</Citation>
</Reference>
<Reference>
<Citation>Deseret News and Telegram. (1955). From Jungles Of Peru. Deseret News and Telegram.</Citation>
</Reference>
<Reference>
<Citation>Diwan, N., Fluhr, R., Eshed, Y., Zamir, D., and Tanksley, S.D. (1999) Mapping of Ve in tomato: a gene conferring resistance to the broad-spectrum pathogen Verticillium dahliae race 1. Theor Appl Genet 98: 315-319.</Citation>
</Reference>
<Reference>
<Citation>Dobinson, K.F., Tenuta, G.K., and Lazarovits, G. (1996) Occurrence of race 2 of Verticillium dahliae in processing tomato fields in southwestern Ontario. Can J Plant Pathol 18: 55-58.</Citation>
</Reference>
<Reference>
<Citation>Dodds, P.N., and Rathjen, J.P. (2010) Plant immunity: towards an integrated view of plant-pathogen interactions. Nat Rev Genet 11: 539-548.</Citation>
</Reference>
<Reference>
<Citation>Du, J., Verzaux, E., Chaparro-Garcia, A., Bijsterbosch, G., Keizer, L.C.P., Zhou, J., et al. (2015) Elicitin recognition confers enhanced resistance to Phytophthora infestans in potato. Nat Plants 1: 1-5.</Citation>
</Reference>
<Reference>
<Citation>Faino, L., Seidl, M.F., Datema, E., van den Berg, G.C.M., Janssen, A., Wittenberg, A.H.J., and Thomma, B.P.H.J. (2015) Single-molecule real-time sequencing combined with optical mapping yields completely finished fungal genome. mBio 6: 1-11.</Citation>
</Reference>
<Reference>
<Citation>Faino, L., Seidl, M.F., Shi-Kunne, X., Pauper, M., Van den, G.C., Wittenberg, A.H., and Thomma, B.P.H.J. (2016) Transposons passively and actively contribute to evolution of the two-speed genome of a fungal pathogen. Genome Res 26: 1091-1100.</Citation>
</Reference>
<Reference>
<Citation>Fan, R., Cockerton, H.M., Armitage, A.D., Bates, H., Cascant-Lopez, E., Antanaviciute, L., et al. (2018) Vegetative compatibility groups partition variation in the virulence of Verticillium dahliae on strawberry. PLoS One 13: 1-21.</Citation>
</Reference>
<Reference>
<Citation>Flor, H.H. (1942) Inheritance of pathogenicity in Melampsora lini. Phytopathology 32: 653-669.</Citation>
</Reference>
<Reference>
<Citation>Fradin, E.F., and Thomma, B.P.H.J. (2006) Physiology and molecular aspects of Verticillium wilt diseases caused by V. dahliae and V. albo-atrum. Mol Plant Pathol 7: 71-86.</Citation>
</Reference>
<Reference>
<Citation>Fradin, E.F., Zhang, Z., Juarez Ayala, J.C., Castroverde, C.D.M., Nazar, R.N., Robb, J., et al. (2009) Genetic dissection of Verticillium wilt resistance mediated by tomato Ve1. Plant Physiol 150: 320-332.</Citation>
</Reference>
<Reference>
<Citation>Gout, L., Kuhn, M.L., Vincenot, L., Bernard-Samain, S., Cattolico, L., Barbetti, M., et al. (2007) Genome structure impacts molecular evolution at the AvrLm1 avirulence locus of the plant pathogen Leptosphaeria maculans. Environ Microbiol 9: 2978-2992.</Citation>
</Reference>
<Reference>
<Citation>Gibriel, H.A.Y., Li, J., Zhu, L., Seidl, M.F., and Thomma, B.P.H.J. (2019) Verticillium dahliae strains that infect the same host plant display highly divergent effector catalogs. BioRxiv https://dx.doi.org/10.1101/528729.</Citation>
</Reference>
<Reference>
<Citation>Gibriel, H.A.Y., Thomma, B.P.H.J., and Seidl, M.F. (2016) The age of effectors: genome-based discovery and applications. Phytopathology 106: 1206-1212.</Citation>
</Reference>
<Reference>
<Citation>Hahne, F., and Ivanek, R. (2016) Visualizing genomic data using Gviz and Bioconductor. Methods Mol Biol 1418: 335-351.</Citation>
</Reference>
<Reference>
<Citation>Inami, K., Yoshioka-Akiyama, C., Morita, Y., Yamasaki, M., Teraoka, T., and Arie, T. (2012) A genetic mechanism for emergence of races in Fusarium oxysporum f. sp. lycopersici: inactivation of avirulence gene AVR1 by transposon insertion. PLoS One 7: 1-10.</Citation>
</Reference>
<Reference>
<Citation>Inoue, Y., Vy, T.T.P., Yoshida, K., Asano, H., Mitsuoka, C., Asuke, S., et al. (2017) Evolution of the wheat blast fungus through functional losses in a host specificity determinant. Science 357: 80-83.</Citation>
</Reference>
<Reference>
<Citation>Jones, J.D.G., and Dangl, J.L. (2006) The plant immune system. Nature 444: 323-329.</Citation>
</Reference>
<Reference>
<Citation>Joosten, M.H.A.J., Cozijnsen, T.J., and de Wit, P.J.G.M. (1994) Host resistance to a fungal tomato pathogen lost by a single base-pair change in an avirulence gene. Trends Genet 10: 117.</Citation>
</Reference>
<Reference>
<Citation>Kema, G.H.J., Mirzadi Gohari, A., Aouini, L., Gibriel, H.A.Y., Ware, S.B., Van Den Bosch, F., et al. (2018) Stress and sexual reproduction affect the dynamics of the wheat pathogen effector AvrStb6 and strobilurin resistance. Nat Genet 50: 375-380.</Citation>
</Reference>
<Reference>
<Citation>Klosterman, S.J., Atallah, Z.K., Vallad, G.E., and Subbarao, K.V. (2009) Diversity, pathogenicity, and management of Verticillium species. Annu Rev Phytopathol 47: 39-62.</Citation>
</Reference>
<Reference>
<Citation>Koren, S., Walenz, B.P., Berlin, K., Miller, J.R., Bergman, N.H., and Phillippy, A.M. (2017) Canu: scalable and accurate long-read assembly via adaptive k-mer weighting and repeat separation. Genome Res 27: 722-736.</Citation>
</Reference>
<Reference>
<Citation>Langmead, B., and Salzberg, S.L. (2012) Fast gapped-read alignment with bowtie 2. Nat Methods 9: 357-359.</Citation>
</Reference>
<Reference>
<Citation>Lauge, R., Joosten, M.H.A.J., Haanstra, J.P.W., Goodwin, P.H., Lindhout, P., and de Wit, P.J.G.M. (1998) Successful search for a resistance gene in tomato targeted against a virulence factor of a fungal pathogen. Proc Natl Acad Sci U S A 95: 9014-9018.</Citation>
</Reference>
<Reference>
<Citation>Li, H. (2013) Aligning sequence reads, clone sequences and assembly contigs with BWA-MEM. ArXiv 00: 1-3.</Citation>
</Reference>
<Reference>
<Citation>Li, H. (2018) Minimap2: pairwise alignment for nucleotide sequences. Bioinformatics 34: 3094-3100.</Citation>
</Reference>
<Reference>
<Citation>Li, H., and Durbin, R. (2009) Fast and accurate short read alignment with burrows-wheeler transform. Bioinformatics 25: 1754-1760.</Citation>
</Reference>
<Reference>
<Citation>Li, H., Handsaker, B., Wysoker, A., Fennell, T., Ruan, J., Homer, N., et al. (2009) The sequence alignment/map format and SAMtools. Bioinformatics 25: 2078-2079.</Citation>
</Reference>
<Reference>
<Citation>Lu, X., Kracher, B., Saur, I.M.L., Bauer, S., Ellwood, S.R., Wise, R., et al. (2016) Allelic barley MLA immune receptors recognize sequence-unrelated avirulence effectors of the powdery mildew pathogen. Proc Natl Acad Sci U S A 113: E6486-E6495.</Citation>
</Reference>
<Reference>
<Citation>Luderer, R., Takken, F.L.W., de Wit, P.J.G.M., and Joosten, M.H.A.J. (2002) Cladosporium fulvum overcomes Cf-2-mediated resistance by producing truncated AVR2 elicitor proteins. Mol Microbiol 45: 875-884.</Citation>
</Reference>
<Reference>
<Citation>Meile, L., Croll, D., Brunner, P.C., Plissonneau, C., Hartmann, F.E., McDonald, B.A., and Sánchez-Vallet, A. (2018) A fungal avirulence factor encoded in a highly plastic genomic region triggers partial resistance to septoria tritici blotch. New Phytol 219: 1048-1061.</Citation>
</Reference>
<Reference>
<Citation>Mesarich, C.H., Griffiths, S.A., van der Burgt, A., Ökmen, B., Beenen, H.G., Etalo, D.W., et al. (2014) Transcriptome sequencing uncovers the Avr5 avirulence gene of the tomato leaf mold pathogen Cladosporium fulvum. Mol Plant Microbe Interact 27: 846-857.</Citation>
</Reference>
<Reference>
<Citation>Na, R., and Gijzen, M. (2016) Escaping host immunity: new tricks for plant pathogens. PLoS Pathog 12: 1-6.</Citation>
</Reference>
<Reference>
<Citation>Niu, X., Zhao, X., Ling, K.S., Levi, A., Sun, Y., and Fan, M. (2016) The FonSIX6 gene acts as an avirulence effector in the Fusarium oxysporum f. sp. Niveum - watermelon pathosystem. Sci Rep 6: 1-7.</Citation>
</Reference>
<Reference>
<Citation>Ökmen, B., Etalo, D.W., Joosten, M.H.A.J., Bouwmeester, H.J., de Vos, R.C.H., Collemare, J., and de Wit, P.J.G.M. (2013) Detoxification of α-tomatine by Cladosporium fulvum is required for full virulence on tomato. New Phytol 198: 1203-1214.</Citation>
</Reference>
<Reference>
<Citation>Pallaghy, P.K., Norton, R.S., Nielsen, K.J., and Craik, D.J. (1994) A common structural motif incorporating a cystine knot and a triple-stranded β-sheet in toxic and inhibitory polypeptides. Protein Sci 3: 1833-1839.</Citation>
</Reference>
<Reference>
<Citation>Parlange, F., Daverdin, G., Fudal, I., Kuhn, M.L., Balesdent, M.H., Blaise, F., et al. (2009) Leptosphaeria maculans avirulence gene AvrLm4-7 confers a dual recognition specificity by the Rlm4 and Rlm7 resistance genes of oilseed rape, and circumvents Rlm4-mediated recognition through a single amino acid change. Mol Microbiol 71: 851-863.</Citation>
</Reference>
<Reference>
<Citation>Pegg, G.F., and Dixon, G.R. (1969) The reactions of susceptible and resistant tomato cultivars to strains of Verticillium albo-atrum. Ann Appl Biol 63: 389-400.</Citation>
</Reference>
<Reference>
<Citation>Petersen, T.N., Brunak, S., Von Heijne, G., and Nielsen, H. (2011) SignalP 4.0: discriminating signal peptides from transmembrane regions. Nat Methods 8: 785-786.</Citation>
</Reference>
<Reference>
<Citation>Petit-Houdenot, Y., Degrave, A., Meyer, M., Blaise, F., Ollivier, B., Marais, C.L., et al. (2019) A two genes - for - one gene interaction between Leptosphaeria maculans and Brassica napus. New Phytol 223: 397-411.</Citation>
</Reference>
<Reference>
<Citation>Plissonneau, C., Daverdin, G., Ollivier, B., Blaise, F., Degrave, A., Fudal, I., et al. (2016) A game of hide and seek between avirulence genes AvrLm4-7 and AvrLm3 in Leptosphaeria maculans. New Phytol 209: 1613-1624.</Citation>
</Reference>
<Reference>
<Citation>Praz, C.R., Bourras, S., Zeng, F., Sánchez-Martín, J., Menardo, F., Xue, M., et al. (2016) AvrPm2 encodes an RNase-like avirulence effector which is conserved in the two different specialized forms of wheat and rye powdery mildew fungus. New Phytol 213: 1301-1314.</Citation>
</Reference>
<Reference>
<Citation>Quinlan, A.R., and Hall, I.M. (2010) BEDTools: a flexible suite of utilities for comparing genomic features. Bioinformatics 26: 841-842.</Citation>
</Reference>
<Reference>
<Citation>Robert, X., and Gouet, P. (2014) Deciphering key features in protein structures with the new ENDscript server. Nucleic Acids Res 42: 320-324.</Citation>
</Reference>
<Reference>
<Citation>Robinson, D.B. (1957) Verticillium Wilt of Potato in Relation to Symptoms, Epidemiology and Variability of the Pathogen, Madison, WI: University of Wisconsin Agricultural Experiment Station Results Bulletin, p. 49.</Citation>
</Reference>
<Reference>
<Citation>Robinson, J.T., Thorvaldsdóttir, H., Winckler, W., Guttman, M., Lander, E.S., Getz, G., and Mesirov, J.P. (2011) Integrative Genome Viewer. Nat Biotechnol 29: 24-26.</Citation>
</Reference>
<Reference>
<Citation>Rovenich, H., Boshoven, J.C., and Thomma, B.P.H.J. (2014) Filamentous pathogen effector functions: of pathogens hosts and microbiomes. Curr Opin Plant Biol 20: 96-103.</Citation>
</Reference>
<Reference>
<Citation>Salcedo, A., Rutter, W., Wang, S., Akhunova, A., Bolus, S., Chao, S., et al. (2017) Variation in the AvrSr35 gene determines Sr35 resistance against wheat stem rust race Ug99. Science 358: 1604-1606.</Citation>
</Reference>
<Reference>
<Citation>Santhanam, P., Van Esse, H.P., Albert, I., Faino, L., Nürnberger, T., and Thomma, B.P.H.J. (2013) Evidence for functional diversification within a fungal Nep1-like protein family. Mol Plant Microbe Interact 26: 278-286.</Citation>
</Reference>
<Reference>
<Citation>Saur, I.M.L., Bauer, S., Kracher, B., Lu, X., Franzeskakis, L., Müller, M.C., et al. (2019) Multiple pairs of allelic MLA immune receptor-powdery mildew AVRa effectors argue for a direct recognition mechanism. EeLife 8: 1-31.</Citation>
</Reference>
<Reference>
<Citation>Schaible, L., Cannon, O.S., and Waddoups, V. (1951) Inheritance of resistance to Verticillium wilt in a tomato cross. Phytopathology 41: 986-990.</Citation>
</Reference>
<Reference>
<Citation>Schmidt, S.M., Lukasiewicz, J., Farrer, R., van Dam, P., Bertoldo, C., and Rep, M. (2016) Comparative genomics of Fusarium oxysporum f. sp. melonis reveals the secreted protein recognized by the Fom-2 resistance gene in melon. New Phytol 209: 307-318.</Citation>
</Reference>
<Reference>
<Citation>Shan, W., Cao, M., Leung, D., and Tyler, B.M. (2004) The Avr1b locus of Phytophthora sojae encodes an elicitor and a regulator required for avirulence on soybean plants carrying resistance gene Rps1b. Mol Plant Microbe Interact 17: 394-403.</Citation>
</Reference>
<Reference>
<Citation>Shi-Kunne, X., Faino, L., van den Berg, G.C.M., Thomma, B.P.H.J., and Seidl, M.F. (2018) Evolution within the fungal genus Verticillium is characterized by chromosomal rearrangement and gene loss. Environ Microbiol 20: 1362-1373.</Citation>
</Reference>
<Reference>
<Citation>Snelders, N., Rovenich, H., Petti, G., Rocafort, M., Vorholt, J., Mesters, J., et al. (2020) A plant pathogen utilizes effector proteins for microbiome manipulation. BioRxiv https://dx.doi.org/10.1101/2020.01.30.926725.</Citation>
</Reference>
<Reference>
<Citation>Song, Y., Zhang, Z., Seidl, M.F., Majer, A., Jakse, J., Javornik, B., and Thomma, B.P.H.J. (2017) Broad taxonomic characterization of Verticillium wilt resistance genes reveals an ancient origin of the tomato Ve1 immune receptor. Mol Plant Pathol 18: 195-209.</Citation>
</Reference>
<Reference>
<Citation>Stamatakis, A. (2014) RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30: 1312-1313.</Citation>
</Reference>
<Reference>
<Citation>Stanke, M., Tzvetkova, A., and Morgenstern, B. (2006) AUGUSTUS at EGASP: using EST, protein and genomic alignments for improved gene prediction in the human genome. Genome Biol 7: 1-8.</Citation>
</Reference>
<Reference>
<Citation>Staskawicz, B.J., Dahlbeck, D., and Keen, N.T. (1984) Cloned avirulence gene of Pseudomonas syringae pv. glycinea determines race-specific incompatibility on Glycine max (L.) Merr. Proc Natl Acad Sci U S A 81: 6024-6028.</Citation>
</Reference>
<Reference>
<Citation>Stergiopoulos, I., De Kock, M.J.D., Lindhout, P., and de Wit, P.J.G.M. (2007) Allelic variation in the effector genes of the tomato pathogen Cladosporium fulvum reveals different modes of adaptive evolution. Mol Plant Microbe Interact 20: 1271-1283.</Citation>
</Reference>
<Reference>
<Citation>Stukenbrock, E.H., and McDonald, B.A. (2008) The origins of plant pathogens in agro-ecosystems. Annu Rev Phytopathol 46: 75-100.</Citation>
</Reference>
<Reference>
<Citation>Takken, F.L.W., Luderer, R., Gabriëls, S.H.E.J., Westerink, N., Lu, R., De Wit, P.J.G.M., and Joosten, M.H.A.J. (2000) A functional cloning strategy, based on a binary PVX-expression vector, to isolate HR-inducing cDNAs of plant pathogens. Plant J 24: 275-283.</Citation>
</Reference>
<Reference>
<Citation>Takken, F.L.W., Thomas, C.M., Joosten, M.H.A.J., Golstein, C., Westerink, N., Hille, J., et al. (1999) A second gene at the tomato Cf-4 locus confers resistance to Cladosporium fulvum through recognition of a novel avirulence determinant. Plant J 20: 279-288.</Citation>
</Reference>
<Reference>
<Citation>Thomma, B.P.H.J., Nürnberger, T., and Joosten, M.H.A.J. (2011) Of PAMPs and effectors: the blurred PTI-ETI dichotomy. Plant Cell 23: 4-15.</Citation>
</Reference>
<Reference>
<Citation>Usami, T., Momma, N., Kikuchi, S., Watanabe, H., Hayashi, A., Mizukawa, M., et al. (2017) Race 2 of Verticillium dahliae infecting tomato in Japan can be split into two races with differential pathogenicity on resistant rootstocks. Plant Pathol 66: 230-238.</Citation>
</Reference>
<Reference>
<Citation>van Kan, J.A., van den Ackerveken, G.F., and de Wit, P.J. (1991) Cloning and characterization of cDNA of avirulence gene avr9 of the fungal pathogen Cladosporium fulvum, causal agent of tomato leaf mold. Mol Plant Microbe Interact 4: 52-59.</Citation>
</Reference>
<Reference>
<Citation>Vleeshouwers, V.G.A.A., and Oliver, R.P. (2014) Effectors as tools in disease resistance breeding against biotrophic, hemibiotrophic and necrotrophic plant pathogens. Mol Plant Microbe Interact 27: 196-206.</Citation>
</Reference>
<Reference>
<Citation>Wick, R. (2018). Porechop. URL https://github.com/rrwick/Porechop</Citation>
</Reference>
<Reference>
<Citation>Zhong, Z., Marcel, T.C., Hartmann, F.E., Ma, X., Plissonneau, C., Zala, M., et al. (2017) A small secreted protein in Zymoseptoria tritici is responsible for avirulence on wheat cultivars carrying the Stb6 resistance gene. New Phytol 214: 619-631.</Citation>
</Reference>
<Reference>
<Citation>Zhou, E., Jia, Y., Singh, P., Correll, J.C., and Lee, F.N. (2007) Instability of the Magnaporthe oryzae avirulence gene AVR-Pita alters virulence. Fungal Genet Biol 44: 1024-1034.</Citation>
</Reference>
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<name sortKey="Usami, Toshiyuki" sort="Usami, Toshiyuki" uniqKey="Usami T" first="Toshiyuki" last="Usami">Toshiyuki Usami</name>
</noRegion>
</country>
<country name="Allemagne">
<noRegion>
<name sortKey="Thomma, Bart P H J" sort="Thomma, Bart P H J" uniqKey="Thomma B" first="Bart P H J" last="Thomma">Bart P H J. Thomma</name>
</noRegion>
</country>
</tree>
</affiliations>
</record>

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