The tomato resistance gene Bs4 suppresses leaf watersoaking phenotypes induced by AvrHah1, a transcription activator-like effector from tomato-pathogenic xanthomonads.

Xanthomonas AvrHah1 basic helix-loop-helix (bHLH) domain transcription factor nucleotide-binding leucine-rich repeat (NLR) protein pectate lyase pectinesterase susceptibility (S) gene transcription-activator-like effector (TALE)

Journal

The New phytologist
ISSN: 1469-8137
Titre abrégé: New Phytol
Pays: England
ID NLM: 9882884

Informations de publication

Date de publication:
12 2022
Historique:
received: 17 12 2021
accepted: 19 08 2022
pubmed: 4 9 2022
medline: 5 11 2022
entrez: 3 9 2022
Statut: ppublish

Résumé

The Xanthomonas transcription activator-like effector (TALE) protein AvrBs3 transcriptionally activates the executor-type resistance (R) gene Bs3 from pepper (Capsicum annuum), thereby triggering a hypersensitive cell death reaction (HR). AvrBs3 also triggers an HR in tomato (Solanum lycopersicum) upon recognition by the nucleotide-binding leucine-rich repeat (NLR) R protein Bs4. Whether the executor-type R protein Bs3 and the NLR-type R protein Bs4 use common or distinct signalling components to trigger an HR remains unclear. CRISPR/Cas9-mutagenesis revealed, that the immune signalling node EDS1 is required for Bs4- but not for Bs3-dependent HR, suggesting that NLR- and executor-type R proteins trigger an HR via distinct signalling pathways. CRISPR/Cas9-mutagenesis also revealed that tomato Bs4 suppresses the virulence function of both TALEs, the HR-inducing AvrBs3 protein and of AvrHah1, a TALE that does not trigger an HR in tomato. Analysis of AvrBs3- and AvrHah1-induced host transcripts and disease phenotypes in CRISPR/Cas9-induced bs4 mutant plants indicates that both TALEs target orthologous transcription factor genes to promote disease in tomato and pepper host plants. Our studies display that tomato mutants lacking the TALE-sensing Bs4 protein provide a novel platform to either uncover TALE-induced disease phenotypes or genetically dissect components of executor-triggered HR.

Identifiants

pubmed: 36056465
doi: 10.1111/nph.18456
doi:

Substances chimiques

Transcription Activator-Like Effectors 0
Bacterial Proteins 0
Plant Proteins 0

Banques de données

RefSeq
['ABW22630.1', 'NP_001266190.2']

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

1856-1870

Informations de copyright

© 2022 The Authors. New Phytologist © 2022 New Phytologist Foundation.

Références

Balint-Kurti P. 2019. The plant hypersensitive response: concepts, control and consequences. Molecular Plant Pathology 20: 1163-1178.
Ballvora A, Pierre M, Van den Ackerveken G, Schornack S, Rossier O, Ganal M, Lahaye T, Bonas U. 2001a. Genetic mapping and functional analysis of the tomato Bs4 locus, governing recognition of the Xanthomonas campestris pv. vesicatoria AvrBs4 protein. Molecular Plant-Microbe Interactions 14: 629-638.
Ballvora A, Schornack S, Baker BJ, Ganal M, Bonas U, Lahaye T. 2001b. Chromosome landing at the tomato Bs4 locus. Molecular Genetics and Genomics 266: 639-645.
Belhaj K, Chaparro-Garcia A, Kamoun S, Nekrasov V. 2013. Plant genome editing made easy: targeted mutagenesis in model and crop plants using the CRISPR/Cas system. Plant Methods 9: 39-47.
Binder A, Lambert J, Morbitzer R, Popp C, Ott T, Lahaye T, Parniske M. 2014. A modular plasmid assembly kit for multigene expression, gene silencing and silencing rescue in plants. PLoS ONE 9: e88218.
Boch J, Bonas U, Lahaye T. 2014. TAL effectors - pathogen strategies and plant resistance engineering. New Phytologist 204: 823-832.
Boch J, Scholze H, Schornack S, Landgraf A, Hahn S, Kay S, Lahaye T, Nickstadt A, Bonas U. 2009. Breaking the code of DNA binding specificity of TAL-type III effectors. Science 326: 1509-1512.
Bogdanove AJ, Schornack S, Lahaye T. 2010. TAL effectors: finding plant genes for disease and defense. Current Opinion in Plant Biology 13: 394-401.
Bonas U, Stall RE, Staskawicz B. 1989. Genetic and structural characterization of the avirulence gene avrBs3 from Xanthomonas campestris pv. vesicatoria. Molecular & General Genetics 218: 127-136.
Bresson J, Bieker S, Riester L, Doll J, Zentgraf U. 2018. A guideline for leaf senescence analyses: from quantification to physiological and molecular investigations. Journal of Experimental Botany 69: 769-786.
Concordet JP, Haeussler M. 2018. Crispor: intuitive guide selection for CRISPR/Cas9 genome editing experiments and screens. Nucleic Acids Research 46: W242-W245.
Dongus JA, Parker JE. 2021. EDS1 signalling: at the nexus of intracellular and surface receptor immunity. Current Opinion in Plant Biology 62: 102039.
Donnelly MLL, Hughes LE, Luke G, Mendoza H, ten Dam E, Gani D, Ryan MD. 2001. The ‘cleavage’ activities of foot-and-mouth disease virus 2A site-directed mutants and naturally occurring ‘2A-like’ sequences. Journal of General Virology 82: 1027-1041.
El Kasmi F, Horvath D, Lahaye T. 2018. Microbial effectors and the role of water and sugar in the infection battle ground. Current Opinion in Plant Biology 44: 98-107.
Holmes DR, Morbitzer R, Wunderlich M, Sun H, El Kasmi F, Schneeberger K, Lahaye T. 2020. A shortcut in forward genetics: concurrent discovery of mutant phenotype and causal mutation in Arabidopsis M2 families via MAD-mapping. bioRxiv. doi: 10.1101/2020.06.29.177808.
Jacobs TB, LaFayette PR, Schmitz RJ, Parrott WA. 2015. Targeted genome modifications in soybean with CRISPR/Cas9. BMC Biotechnology 15: 16.
Jouffroy O, Saha S, Mueller L, Quesneville H, Maumus F. 2016. Comprehensive repeatome annotation reveals strong potential impact of repetitive elements on tomato ripening. BMC Genomics 17: 624.
Kay S, Boch J, Bonas U. 2005. Characterization of AvrBs3-like effectors from a Brassicacae pathogen reveals virulence and avirulence activities and a protein with a novel repeat architecture. Molecular Plant-Microbe Interactions 18: 838-848.
Kay S, Hahn S, Marois E, Hause G, Bonas U. 2007. A bacterial effector acts as a plant transcription factor and induces a cell size regulator. Science 318: 648-651.
Koseoglou E, van der Wolf JM, Visser RGF, Bai Y. 2021. Susceptibility reversed: modified plant susceptibility genes for resistance to bacteria. Trends in Plant Science 27: 69-79.
Lacerda ALM, Fonseca LN, Blawid R, Boiteux LS, Ribeiro SG, Brasileiro ACM. 2015. Reference gene selection for qPCR analysis in tomato-bipartite begomovirus interaction and validation in additional tomato-virus pathosystems. PLoS ONE 10: e0136820.
Lorkovic ZJ, Kirk DAW, Lambermon MHL, Filipowicz W. 2000. Pre-mRNA splicing in higher plants. Trends in Plant Science 5: 160-167.
Min J, Shin S, Jeon E, Park J, Hyun J, Harn C. 2015. Pepper, chili (Capsicum annuum). In: Wang K, ed. Agrobacterium protocols. New York, NY, USA: Springer, 311-320.
Morbitzer R, Elsaesser J, Hausner J, Lahaye T. 2011. Assembly of custom TALE-type DNA binding domains by modular cloning. Nucleic Acids Research 39: 5790-5799.
Newberry EA, Bhandari R, Minsavage GV, Timilsina S, Jibrin MO, Kemble J, Sikora EJ, Jones JB, Potnis N. 2019. Independent evolution with the gene flux originating from multiple Xanthomonas species explains genomic heterogeneity in Xanthomonas perforans. Applied and Environmental Microbiology 85: e00885-19.
Nowack MK, Holmes DR, Lahaye T. 2022. TALE-induced cell death executers - an origin outside immunity? Trends in Plant Science 27: 536-548.
Pérez-Bueno ML, Pineda M, Barón M. 2019. Phenotyping plant responses to biotic stress by chlorophyll fluorescence imaging. Frontiers in Plant Science 10: 1135.
Pruitt RN, Gust AA, Nürnberger T. 2021a. Plant immunity unified. Nature Plants 7: 382-383.
Pruitt RN, Locci F, Wanke F, Zhang L, Saile SC, Joe A, Karelina D, Hua C, Fröhlich K, Wan WL et al. 2021b. The EDS1-PAD4-ADR1 node mediates Arabidopsis pattern-triggered immunity. Nature 598: 495-499.
Razifard H, Ramos A, Della Valle AL, Bodary C, Goetz E, Manser EJ, Li X, Zhang L, Visa S, Tieman D et al. 2020. Genomic evidence for complex domestication history of the cultivated tomato in Latin America. Molecular Biology and Evolution 37: 1118-1132.
Read AC, Hutin M, Moscou MJ, Rinaldi FC, Bogdanove AJ. 2020. Cloning of the rice Xo1 resistance gene and interaction of the Xo1 protein with the defense-suppressing Xanthomonas effector Tal2h. Molecular Plant-Microbe Interactions 33: 1189-1195.
Rodriguez-Leal D, Lemmon ZH, Man J, Bartlett ME, Lippman ZB. 2017. Engineering quantitative trait variation for crop improvement by genome editing. Cell 171: 470-480.
Römer P, Hahn S, Jordan T, Strauß T, Bonas U, Lahaye T. 2007. Plant-pathogen recognition mediated by promoter activation of the pepper Bs3 resistance gene. Science 318: 645-648.
Schornack S, Ballvora A, Gürlebeck D, Peart J, Baulcombe D, Baker B, Ganal M, Bonas U, Lahaye T. 2004. The tomato resistance protein Bs4 is a predicted non-nuclear TIR-NB-LRR protein that mediates defense responses to severely truncated derivatives of AvrBs4 and overexpressed AvrBs3. The Plant Journal 37: 46-60.
Schornack S, Minsavage GV, Stall RE, Jones JB, Lahaye T. 2008. Characterization of AvrHah1 a novel AvrBs3-like effector from Xanthomonas gardneri with virulence and avirulence activity. New Phytologist 179: 546-556.
Schornack S, Peter K, Bonas U, Lahaye T. 2005. Expression levels of avrBs3-like genes affect recognition specificity in tomato Bs4 but not in pepper Bs3 mediated perception. Molecular Plant-Microbe Interactions 18: 1215-1225.
Schwartz AR, Morbitzer R, Lahaye T, Staskawicz BJ. 2017. TALE-induced bHLH transcription factors that activate a pectate lyase contribute to water soaking in bacterial spot of tomato. Proceedings of the National Academy of Sciences, USA 114: E897-E903.
Shearer LA, Anderson LK, de Jong H, Smit S, Goicoechea JL, Roe BA, Hua A, Giovannoni JJ, Stack SM. 2014. Fluorescence in situ hybridization and optical mapping to correct scaffold arrangement in the tomato genome. G3 Genes Genomes Genetics 4: 1395-1405.
Stemmer M, Thumberger T, Keyer MD, Wittbrodt J, Mateo JL. 2015. CCTop: an intuitive, flexible and reliable CRISPR/Cas9 target prediction tool. PLoS ONE 10: e0124633.
Strauß T, Van Poecke R, Strauß A, Römer P, Minsavage GV, Singh S, Wolf C, Strauß A, Kim S, Lee H-A et al. 2012. RNA-seq pinpoints a Xanthomonas TAL-effector activated resistance gene in a large crop genome. Proceedings of the National Academy of Sciences, USA 109: 19480-19485.
Streubel J, Pesce C, Hutin M, Koebnik R, Boch J, Szurek B. 2013. Five phylogenetically close rice SWEET genes confer TAL effector-mediated susceptibility to Xanthomonas oryzae pv. oryzae. New Phytologist 200: 808-819.
Tran TT, Doucoure H, Hutin M, Nino LMJ, Szurek B, Cunnac S, Koebnik R. 2018. Efficient enrichment cloning of TAL effector genes from Xanthomonas. MethodsX 5: 1027-1032.
Wittmann J, Brancato C, Berendzen KW, Dreiseikelmann B. 2016. Development of a tomato plant resistant to Clavibacter michiganensis using the endolysin gene of bacteriophage CMP1 as a transgene. Plant Pathology 65: 496-502.
Wu TD, Watanabe CK. 2005. Gmap: a genomic mapping and alignment program for mRNA and EST sequences. Bioinformatics 21: 1859-1875.
Xia XH, Cheng XH, Li R, Yao JN, Li ZG, Cheng YL. 2021. Advances in application of genome editing in tomato and recent development of genome editing technology. Theoretical and Applied Genetics 134: 2727-2747.
Zhang J, Coaker G, Zhou JM, Dong X. 2020. Plant immune mechanisms: from reductionistic to holistic points of view. Molecular Plant 13: 1358-1378.
Zhang J, Yin Z, White F. 2015. TAL effectors and the executor R genes. Frontiers in Plant Science 6: 641.
Zhou JM, Zhang Y. 2020. Plant immunity: danger perception and signaling. Cell 181: 978-989.
Zuo J, Niu QW, Chua NH. 2000. Technical advance: an estrogen receptor-based transactivator XVE mediates highly inducible gene expression in transgenic plants. The Plant Journal 24: 265-273.

Auteurs

Kyrylo Schenstnyi (K)

University of Tübingen, ZMBP - General Genetics, Auf der Morgenstelle 32, 72076, Tuebingen, Germany.

Annett Strauß (A)

University of Tübingen, ZMBP - General Genetics, Auf der Morgenstelle 32, 72076, Tuebingen, Germany.

Angela Dressel (A)

University of Tübingen, ZMBP - General Genetics, Auf der Morgenstelle 32, 72076, Tuebingen, Germany.

Robert Morbitzer (R)

University of Tübingen, ZMBP - General Genetics, Auf der Morgenstelle 32, 72076, Tuebingen, Germany.

Markus Wunderlich (M)

University of Tübingen, ZMBP - General Genetics, Auf der Morgenstelle 32, 72076, Tuebingen, Germany.

Ana Gabriela Andrade (AG)

University of Tübingen, ZMBP - General Genetics, Auf der Morgenstelle 32, 72076, Tuebingen, Germany.

Trang-Thi-Thu Phan (TT)

University of Tübingen, ZMBP - General Genetics, Auf der Morgenstelle 32, 72076, Tuebingen, Germany.

Paloma de Los Angeles Aguilera (PLA)

University of Tübingen, ZMBP - General Genetics, Auf der Morgenstelle 32, 72076, Tuebingen, Germany.

Caterina Brancato (C)

University of Tübingen, ZMBP - Central Facilities, Auf der Morgenstelle 32, 72076, Tuebingen, Germany.

Kenneth Wayne Berendzen (KW)

University of Tübingen, ZMBP - Central Facilities, Auf der Morgenstelle 32, 72076, Tuebingen, Germany.

Thomas Lahaye (T)

University of Tübingen, ZMBP - General Genetics, Auf der Morgenstelle 32, 72076, Tuebingen, Germany.

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