{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,11,6]],"date-time":"2026-11-06T19:28:48Z","timestamp":1793993328333,"version":"4.8.0"},"reference-count":67,"publisher":"Springer Science and Business Media LLC","issue":"1","license":[{"start":{"date-parts":[[2023,9,6]],"date-time":"2023-09-06T00:00:00Z","timestamp":1693958400000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0"},{"start":{"date-parts":[[2023,9,6]],"date-time":"2023-09-06T00:00:00Z","timestamp":1693958400000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0"}],"funder":[{"name":"Swiss National Science Fondation","award":["IZCOZ0_189896"],"award-info":[{"award-number":["IZCOZ0_189896"]}]}],"content-domain":{"domain":["link.springer.com"],"crossmark-restriction":false},"short-container-title":["Sci Rep"],"abstract":"<jats:title>Abstract<\/jats:title><jats:p>Downy mildew (DM; <jats:italic>Plasmopara viticola<\/jats:italic>) is amongst the most severe fungal diseases in viticulture and the reason for the majority of fungicide applications. To reduce synthetic and copper-based fungicides, there is an urgent need for natural alternatives, which are being increasingly tested by the industry and the research community. However, their mode of action remains unclear. Therefore, our study aimed to investigate the transcriptomic changes induced by oregano essential oil vapour (OEOV) in DM-infected grapevines. OEOV was applied at different time points before and after DM infection to differentiate between a priming effect and a direct effect. Both pre-DM treatment with OEOV and post-infection treatment resulted in a significant reduction in DM sporulation. RNA-seq, followed by differential gene expression and weighted gene co-expression network analysis, identified co-expressed gene modules associated with secondary metabolism, pathogen recognition and response. Surprisingly, the molecular mechanisms underlying the efficiency of OEOV against DM appear to be independent of stilbene synthesis, and instead involve genes from a putative signalling pathway that has yet to be characterized. This study enhances our understanding of the molecular regulation of innate plant immunity and provides new insights into the mode of action of alternative natural antifungal agents.<\/jats:p>","DOI":"10.1038\/s41598-023-41981-x","type":"journal-article","created":{"date-parts":[[2023,9,6]],"date-time":"2023-09-06T10:01:56Z","timestamp":1693994516000},"update-policy":"https:\/\/doi.org\/10.1007\/springer_crossmark_policy","source":"Crossref","is-referenced-by-count":18,"title":["Unravelling molecular mechanisms involved in resistance priming against downy mildew (Plasmopara viticola) in grapevine (Vitis vinifera L.)"],"prefix":"10.1038","volume":"13","author":[{"given":"Nicolas","family":"Vigneron","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"J\u00e9r\u00f4me","family":"Grimplet","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Eric","family":"Remolif","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Markus","family":"Rienth","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"297","published-online":{"date-parts":[[2023,9,6]]},"reference":[{"key":"41981_CR1","unstructured":"International Organisation of Vine and Wine, O. State of the world vine and wine sector 2022 (2022)."},{"key":"41981_CR2","doi-asserted-by":"publisher","DOI":"10.4172\/2157-7625.S5-005","author":"U Asghar","year":"2016","unstructured":"Asghar, U. & Malik, M. F. Pesticide exposure and human health: A review. J. Ecosyst. Ecogr. https:\/\/doi.org\/10.4172\/2157-7625.S5-005 (2016).","journal-title":"J. Ecosyst. Ecogr."},{"key":"41981_CR3","doi-asserted-by":"publisher","DOI":"10.3389\/fpls.2021.717223","author":"M Rienth","year":"2021","unstructured":"Rienth, M. et al. Modifications of grapevine berry composition induced by main viral and fungal pathogens in a climate change scenario. Front. Plant Sci. https:\/\/doi.org\/10.3389\/fpls.2021.717223 (2021).","journal-title":"Front. Plant Sci."},{"key":"41981_CR4","doi-asserted-by":"publisher","DOI":"10.3389\/fmicb.2022.889472","author":"K Koledenkova","year":"2022","unstructured":"Koledenkova, K. et al. Plasmopara viticola the causal agent of downy mildew of grapevine: From its taxonomy to disease management. Front. Microbiol. https:\/\/doi.org\/10.3389\/fmicb.2022.889472 (2022).","journal-title":"Front. Microbiol."},{"key":"41981_CR5","doi-asserted-by":"publisher","first-page":"7327","DOI":"10.1021\/acs.est.0c02093","volume":"55","author":"B Droz","year":"2021","unstructured":"Droz, B. et al. Copper content and export in European vineyard soils influenced by climate and soil properties. Environ. Sci. Technol. 55, 7327\u20137334. https:\/\/doi.org\/10.1021\/acs.est.0c02093 (2021).","journal-title":"Environ. Sci. Technol."},{"key":"41981_CR6","doi-asserted-by":"publisher","first-page":"119","DOI":"10.3390\/microorganisms9010119","volume":"9","author":"F Massi","year":"2021","unstructured":"Massi, F., Torriani, S. F. F., Borghi, L. & Toffolatti, S. L. Fungicide resistance evolution and detection in plant pathogens: Plasmopara viticola as a case study. Microorganisms 9, 119 (2021).","journal-title":"Microorganisms"},{"key":"41981_CR7","doi-asserted-by":"publisher","first-page":"575","DOI":"10.1094\/PDIS-94-5-0575","volume":"94","author":"S Dagostin","year":"2010","unstructured":"Dagostin, S., Formolo, T., Giovannini, O., Pertot, I. & Schmitt, A. Salvia officinalis extract can protect grapevine against Plasmopara viticola. Plant Dis. 94, 575\u2013580. https:\/\/doi.org\/10.1094\/PDIS-94-5-0575 (2010).","journal-title":"Plant Dis."},{"key":"41981_CR8","doi-asserted-by":"publisher","first-page":"1369","DOI":"10.3390\/agriculture12091369","volume":"12","author":"RK Singh","year":"2022","unstructured":"Singh, R. K. et al. Viewpoint of chitosan application in grapevine for abiotic stress\/disease management towards more resilient viticulture practices. Agriculture 12, 1369 (2022).","journal-title":"Agriculture"},{"key":"41981_CR9","doi-asserted-by":"publisher","first-page":"776","DOI":"10.1016\/j.cropro.2011.02.031","volume":"30","author":"S Dagostin","year":"2011","unstructured":"Dagostin, S., Sch\u00e4rer, H.-J., Pertot, I. & Tamm, L. Are there alternatives to copper for controlling grapevine downy mildew in organic viticulture?. Crop Prot. 30, 776\u2013788. https:\/\/doi.org\/10.1016\/j.cropro.2011.02.031 (2011).","journal-title":"Crop Prot."},{"key":"41981_CR10","doi-asserted-by":"publisher","first-page":"200","DOI":"10.3390\/biom10020200","volume":"10","author":"L Nerva","year":"2020","unstructured":"Nerva, L., Sandrini, M., Gambino, G. & Chitarra, W. Double-stranded RNAs (dsRNAs) as a sustainable tool against gray mold (Botrytis cinerea) in grapevine: Effectiveness of different application methods in an open-air environment. Biomolecules 10, 200 (2020).","journal-title":"Biomolecules"},{"key":"41981_CR11","doi-asserted-by":"publisher","DOI":"10.1371\/journal.pone.0088145","volume":"9","author":"A Gauthier","year":"2014","unstructured":"Gauthier, A. et al. The sulfated laminarin triggers a stress transcriptome before priming the SA- and ROS-dependent defenses during grapevine\u2019s induced resistance against Plasmopara viticola. PLoS ONE 9, e88145. https:\/\/doi.org\/10.1371\/journal.pone.0088145 (2014).","journal-title":"PLoS ONE"},{"key":"41981_CR12","doi-asserted-by":"publisher","first-page":"134","DOI":"10.1016\/j.plaphy.2018.10.030","volume":"133","author":"M-C H\u00e9loir","year":"2018","unstructured":"H\u00e9loir, M.-C. et al. Assessment of the impact of PS3-induced resistance to downy mildew on grapevine physiology. Plant Physiol. Biochem. 133, 134\u2013141. https:\/\/doi.org\/10.1016\/j.plaphy.2018.10.030 (2018).","journal-title":"Plant Physiol. Biochem."},{"key":"41981_CR13","doi-asserted-by":"publisher","first-page":"1781","DOI":"10.1021\/acs.jafc.0c06103","volume":"69","author":"A Burdziej","year":"2021","unstructured":"Burdziej, A. et al. Three types of elicitors induce grapevine resistance against downy mildew via common and specific immune responses. J. Agric. Food Chem. 69, 1781\u20131795. https:\/\/doi.org\/10.1021\/acs.jafc.0c06103 (2021).","journal-title":"J. Agric. Food Chem."},{"key":"41981_CR14","doi-asserted-by":"publisher","first-page":"17574","DOI":"10.1038\/s41598-020-73027-x","volume":"10","author":"M Colombo","year":"2020","unstructured":"Colombo, M. et al. NoPv1: A synthetic antimicrobial peptide aptamer targeting the causal agents of grapevine downy mildew and potato late blight. Sci. Rep. 10, 17574. https:\/\/doi.org\/10.1038\/s41598-020-73027-x (2020).","journal-title":"Sci. Rep."},{"key":"41981_CR15","doi-asserted-by":"publisher","first-page":"819","DOI":"10.1094\/mpmi-18-0819","volume":"18","author":"MM Hamiduzzaman","year":"2005","unstructured":"Hamiduzzaman, M. M., Jakab, G., Barnavon, L., Neuhaus, J. M. & Mauch-Mani, B. beta-Aminobutyric acid-induced resistance against downy mildew in grapevine acts through the potentiation of callose formation and jasmonic acid signaling. Mol. Plant Microbe Interact. MPMI 18, 819\u2013829. https:\/\/doi.org\/10.1094\/mpmi-18-0819 (2005).","journal-title":"Mol. Plant Microbe Interact. MPMI"},{"key":"41981_CR16","doi-asserted-by":"publisher","first-page":"545","DOI":"10.1111\/ajgw.12558","volume":"28","author":"Y Wang","year":"2022","unstructured":"Wang, Y. et al. Kaolin particle film limits grapevine downy mildew epidemic under open-field conditions and stimulates the plant defence response. Aust. J. Grape Wine Res. 28, 545\u2013560. https:\/\/doi.org\/10.1111\/ajgw.12558 (2022).","journal-title":"Aust. J. Grape Wine Res."},{"key":"41981_CR17","doi-asserted-by":"publisher","first-page":"498","DOI":"10.3390\/agronomy12020498","volume":"12","author":"N Mijailovic","year":"2022","unstructured":"Mijailovic, N., Nesler, A., Perazzolli, M., Aziz, A. & Essa\u00efd, A. B. Foliar application of a tagatose-based product reduces downy mildew symptoms through induction of grapevine resistance and anti-oomycete action. Agronomy 12, 498 (2022).","journal-title":"Agronomy"},{"key":"41981_CR18","doi-asserted-by":"publisher","first-page":"660","DOI":"10.1186\/1471-2164-13-660","volume":"13","author":"M Perazzolli","year":"2012","unstructured":"Perazzolli, M. et al. Downy mildew resistance induced by Trichoderma harzianum T39 in susceptible grapevines partially mimics transcriptional changes of resistant genotypes. BMC Genom. 13, 660. https:\/\/doi.org\/10.1186\/1471-2164-13-660 (2012).","journal-title":"BMC Genom."},{"key":"41981_CR19","doi-asserted-by":"publisher","first-page":"2020","DOI":"10.1002\/ps.5317","volume":"75","author":"RM De Miccolis Angelini","year":"2019","unstructured":"De Miccolis Angelini, R. M. et al. Global transcriptome analysis and differentially expressed genes in grapevine after application of the yeast-derived defense inducer cerevisane. Pest Manag. Sci. 75, 2020\u20132033. https:\/\/doi.org\/10.1002\/ps.5317 (2019).","journal-title":"Pest Manag. Sci."},{"key":"41981_CR20","doi-asserted-by":"publisher","DOI":"10.1590\/0100-29452017015","author":"R Fialho","year":"2017","unstructured":"Fialho, R., Papa, M., Panosso, A. & Cassiolato, A. Fungitoxicity of essential oils on plasmapora viticola, causal agent of grapevine downy mildew. Rev. Bras. Frutic. https:\/\/doi.org\/10.1590\/0100-29452017015 (2017).","journal-title":"Rev. Bras. Frutic."},{"key":"41981_CR21","doi-asserted-by":"publisher","first-page":"1982","DOI":"10.3390\/life12121982","volume":"12","author":"E Kakouri","year":"2022","unstructured":"Kakouri, E. et al. Origanum majorana essential oil; A review of its chemical profile and pesticide activity. Life 12, 1982 (2022).","journal-title":"Life"},{"key":"41981_CR22","doi-asserted-by":"publisher","first-page":"873","DOI":"10.1007\/s11101-018-9566-0","volume":"17","author":"M Marrelli","year":"2018","unstructured":"Marrelli, M., Statti, G. A. & Conforti, F. Origanum spp.: An update of their chemical and biological profiles. Phytochem. Rev. 17, 873\u2013888. https:\/\/doi.org\/10.1007\/s11101-018-9566-0 (2018).","journal-title":"Phytochem. Rev."},{"key":"41981_CR23","doi-asserted-by":"publisher","DOI":"10.1371\/journal.pone.0222854","author":"M Rienth","year":"2019","unstructured":"Rienth, M., Crovadore, M., Ghaffari, S. & Lefort, F. Oregano essential oil vapour prevents Plasmopora viticola infection in grapevine (Vitis vinifera) by triggering autoimmune metabolic pathway. PLoS ONE https:\/\/doi.org\/10.1371\/journal.pone.0222854 (2019).","journal-title":"PLoS ONE"},{"key":"41981_CR24","doi-asserted-by":"publisher","DOI":"10.14601\/Phyto-11605","author":"A Burggraf","year":"2020","unstructured":"Burggraf, A. & Rienth, M. Origanum vulgare essential oil vapour impedes Botrytis cinerea development on grapevine (Vitis vinifera) fruit. Phytopathol. Mediterr. https:\/\/doi.org\/10.14601\/Phyto-11605 (2020).","journal-title":"Phytopathol. Mediterr."},{"key":"41981_CR25","doi-asserted-by":"publisher","first-page":"485","DOI":"10.1146\/annurev-arplant-042916-041132","volume":"68","author":"B Mauch-Mani","year":"2017","unstructured":"Mauch-Mani, B., Baccelli, I., Luna, E. & Flors, V. Defense priming: An adaptive part of induced resistance. Annu. Rev. Plant Biol. 68, 485\u2013512. https:\/\/doi.org\/10.1146\/annurev-arplant-042916-041132 (2017).","journal-title":"Annu. Rev. Plant Biol."},{"key":"41981_CR26","doi-asserted-by":"publisher","first-page":"67","DOI":"10.1007\/s11306-019-1530-5","volume":"15","author":"A Burdziej","year":"2019","unstructured":"Burdziej, A. et al. Impact of different elicitors on grapevine leaf metabolism monitored by 1H NMR spectroscopy. Metabolomics 15, 67. https:\/\/doi.org\/10.1007\/s11306-019-1530-5 (2019).","journal-title":"Metabolomics"},{"key":"41981_CR27","doi-asserted-by":"publisher","first-page":"948","DOI":"10.1111\/nph.13325","volume":"206","author":"A Piasecka","year":"2015","unstructured":"Piasecka, A., Jedrzejczak-Rey, N. & Bednarek, P. Secondary metabolites in plant innate immunity: Conserved function of divergent chemicals. New Phytol 206, 948\u2013964. https:\/\/doi.org\/10.1111\/nph.13325 (2015).","journal-title":"New Phytol"},{"key":"41981_CR28","doi-asserted-by":"publisher","first-page":"117","DOI":"10.1186\/1471-2164-11-117","volume":"11","author":"M Polesani","year":"2010","unstructured":"Polesani, M. et al. General and species-specific transcriptional responses to downy mildew infection in a susceptible (Vitis vinifera) and a resistant (V. riparia) grapevine species. BMC Genom. 11, 117. https:\/\/doi.org\/10.1186\/1471-2164-11-117 (2010).","journal-title":"BMC Genom."},{"key":"41981_CR29","doi-asserted-by":"publisher","first-page":"28","DOI":"10.1007\/s10681-019-2355-z","volume":"215","author":"S Fr\u00f6bel","year":"2019","unstructured":"Fr\u00f6bel, S., Dudenh\u00f6ffer, J., T\u00f6pfer, R. & Zyprian, E. Transcriptome analysis of early downy mildew (Plasmopara viticola) defense in grapevines carrying the Asian resistance locus Rpv10. Euphytica 215, 28. https:\/\/doi.org\/10.1007\/s10681-019-2355-z (2019).","journal-title":"Euphytica"},{"key":"41981_CR30","doi-asserted-by":"publisher","first-page":"12523","DOI":"10.1038\/s41598-018-30413-w","volume":"8","author":"SL Toffolatti","year":"2018","unstructured":"Toffolatti, S. L. et al. Unique resistance traits against downy mildew from the center of origin of grapevine (Vitis vinifera). Sci. Rep. 8, 12523\u201312523. https:\/\/doi.org\/10.1038\/s41598-018-30413-w (2018).","journal-title":"Sci. Rep."},{"key":"41981_CR31","doi-asserted-by":"publisher","first-page":"261","DOI":"10.3390\/genes11030261","volume":"11","author":"SL Toffolatti","year":"2020","unstructured":"Toffolatti, S. L. et al. Novel aspects on the interaction between grapevine and Plasmopara viticola: Dual-RNA-Seq analysis highlights gene expression dynamics in the pathogen and the plant during the battle for infection. Genes 11, 261 (2020).","journal-title":"Genes"},{"key":"41981_CR32","doi-asserted-by":"publisher","first-page":"343","DOI":"10.1186\/s12870-019-1935-3","volume":"19","author":"B Eisenmann","year":"2019","unstructured":"Eisenmann, B. et al. Rpv3-1 mediated resistance to grapevine downy mildew is associated with specific host transcriptional responses and the accumulation of stilbenes. BMC Plant Biol. 19, 343. https:\/\/doi.org\/10.1186\/s12870-019-1935-3 (2019).","journal-title":"BMC Plant Biol."},{"key":"41981_CR33","doi-asserted-by":"publisher","first-page":"757","DOI":"10.1038\/s41598-018-19158-8","volume":"8","author":"M Brilli","year":"2018","unstructured":"Brilli, M. et al. A multi-omics study of the grapevine-downy mildew (Plasmopara viticola) pathosystem unveils a complex protein coding- and noncoding-based arms race during infection. Sci. Rep. 8, 757. https:\/\/doi.org\/10.1038\/s41598-018-19158-8 (2018).","journal-title":"Sci. Rep."},{"key":"41981_CR34","unstructured":"OIV. Descriptor List for Grape Varieties and Vitis Species (Office International de la Vigne et du Vin, 2009)."},{"key":"41981_CR35","doi-asserted-by":"publisher","first-page":"265","DOI":"10.1016\/j.mimet.2010.12.009","volume":"84","author":"E Peressotti","year":"2011","unstructured":"Peressotti, E., Duch\u00eane, E., Merdinoglu, D. & Mestre, P. A semi-automatic non-destructive method to quantify grapevine downy mildew sporulation. J. Microbiol. Methods 84, 265\u2013271. https:\/\/doi.org\/10.1016\/j.mimet.2010.12.009 (2011).","journal-title":"J. Microbiol. Methods"},{"key":"41981_CR36","doi-asserted-by":"publisher","first-page":"235","DOI":"10.1016\/j.mimet.2013.08.012","volume":"95","author":"IL Kim Khiook","year":"2013","unstructured":"Kim Khiook, I. L. et al. Image analysis methods for assessment of H2O2 production and Plasmopara viticola development in grapevine leaves: Application to the evaluation of resistance to downy mildew. J. Microbiol. Methods 95, 235\u2013244. https:\/\/doi.org\/10.1016\/j.mimet.2013.08.012 (2013).","journal-title":"J. Microbiol. Methods"},{"key":"41981_CR37","doi-asserted-by":"publisher","first-page":"172","DOI":"10.1186\/s13059-018-1536-8","volume":"19","author":"B Abu-Jamous","year":"2018","unstructured":"Abu-Jamous, B. & Kelly, S. Clust: Automatic extraction of optimal co-expressed gene clusters from gene expression data. Genome Biol. 19, 172. https:\/\/doi.org\/10.1186\/s13059-018-1536-8 (2018).","journal-title":"Genome Biol."},{"key":"41981_CR38","doi-asserted-by":"publisher","first-page":"6584693","DOI":"10.1155\/2021\/6584693","volume":"2021","author":"J Sharifi-Rad","year":"2021","unstructured":"Sharifi-Rad, J. et al. Phytochemical constituents, biological activities, and health-promoting effects of the Melissa officinalis. Oxid. Med. Cell. Longev. 2021, 6584693. https:\/\/doi.org\/10.1155\/2021\/6584693 (2021).","journal-title":"Oxid. Med. Cell. Longev."},{"key":"41981_CR39","doi-asserted-by":"publisher","first-page":"2539","DOI":"10.3390\/molecules24142539","volume":"24","author":"C Maes","year":"2019","unstructured":"Maes, C., Bouquillon, S. & Fauconnier, M.-L. Encapsulation of essential oils for the development of biosourced pesticides with controlled release: A review. Molecules (Basel Switzerland) 24, 2539. https:\/\/doi.org\/10.3390\/molecules24142539 (2019).","journal-title":"Molecules (Basel Switzerland)"},{"key":"41981_CR40","doi-asserted-by":"publisher","first-page":"559","DOI":"10.1186\/1471-2105-9-559","volume":"9","author":"P Langfelder","year":"2008","unstructured":"Langfelder, P. & Horvath, S. WGCNA: An R package for weighted correlation network analysis. BMC Bioinform. 9, 559. https:\/\/doi.org\/10.1186\/1471-2105-9-559 (2008).","journal-title":"BMC Bioinform."},{"key":"41981_CR41","doi-asserted-by":"publisher","first-page":"323","DOI":"10.1038\/nature05286","volume":"444","author":"JD Jones","year":"2006","unstructured":"Jones, J. D. & Dangl, J. L. The plant immune system. Nature 444, 323\u2013329. https:\/\/doi.org\/10.1038\/nature05286 (2006).","journal-title":"Nature"},{"key":"41981_CR42","doi-asserted-by":"publisher","DOI":"10.3389\/fpls.2020.596301","author":"Y Sun","year":"2020","unstructured":"Sun, Y., Qiao, Z., Muchero, W. & Chen, J.-G. Lectin receptor-like kinases: The sensor and mediator at the plant cell surface. Front. Plant Sci. https:\/\/doi.org\/10.3389\/fpls.2020.596301 (2020).","journal-title":"Front. Plant Sci."},{"key":"41981_CR43","doi-asserted-by":"publisher","first-page":"426","DOI":"10.1038\/ni.3124","volume":"16","author":"S Ranf","year":"2015","unstructured":"Ranf, S. et al. A lectin S-domain receptor kinase mediates lipopolysaccharide sensing in Arabidopsis thaliana. Nat. Immunol. 16, 426\u2013433. https:\/\/doi.org\/10.1038\/ni.3124 (2015).","journal-title":"Nat. Immunol."},{"key":"41981_CR44","doi-asserted-by":"publisher","first-page":"794","DOI":"10.1111\/j.1365-313X.2006.02739.x","volume":"46","author":"X Chen","year":"2006","unstructured":"Chen, X. et al. A B-lectin receptor kinase gene conferring rice blast resistance. Plant J. 46, 794\u2013804. https:\/\/doi.org\/10.1111\/j.1365-313X.2006.02739.x (2006).","journal-title":"Plant J."},{"key":"41981_CR45","doi-asserted-by":"publisher","first-page":"123","DOI":"10.1016\/j.tplants.2013.10.003","volume":"19","author":"TWH Liebrand","year":"2014","unstructured":"Liebrand, T. W. H., van den Burg, H. A. & Joosten, M. H. A. J. Two for all: receptor-associated kinases SOBIR1 and BAK1. Trends Plant Sci. 19, 123\u2013132. https:\/\/doi.org\/10.1016\/j.tplants.2013.10.003 (2014).","journal-title":"Trends Plant Sci."},{"key":"41981_CR46","doi-asserted-by":"publisher","first-page":"4950","DOI":"10.1093\/plcell\/koac286","volume":"34","author":"M Yoon","year":"2022","unstructured":"Yoon, M., Middleditch, M. J. & Rikkerink, E. H. A. A conserved glutamate residue in RPM1-INTERACTING PROTEIN4 is ADP-ribosylated by the Pseudomonas effector AvrRpm2 to activate RPM1-mediated plant resistance. Plant Cell 34, 4950\u20134972. https:\/\/doi.org\/10.1093\/plcell\/koac286 (2022).","journal-title":"Plant Cell"},{"key":"41981_CR47","doi-asserted-by":"publisher","first-page":"15849","DOI":"10.1073\/pnas.95.26.15849","volume":"95","author":"DC Boyes","year":"1998","unstructured":"Boyes, D. C., Nam, J. & Dangl, J. L. The Arabidopsis thaliana RPM1 disease resistance gene product is a peripheral plasma membrane protein that is degraded coincident with the hypersensitive response. Proc. Natl. Acad. Sci. 95, 15849\u201315854. https:\/\/doi.org\/10.1073\/pnas.95.26.15849 (1998).","journal-title":"Proc. Natl. Acad. Sci."},{"key":"41981_CR48","doi-asserted-by":"publisher","first-page":"857","DOI":"10.1126\/science.abn0650","volume":"376","author":"H Kato","year":"2022","unstructured":"Kato, H. et al. Recognition of pathogen-derived sphingolipids in Arabidopsis. Science 376, 857\u2013860. https:\/\/doi.org\/10.1126\/science.abn0650 (2022).","journal-title":"Science"},{"key":"41981_CR49","doi-asserted-by":"publisher","DOI":"10.4161\/15592324.2014.976155","volume":"9","author":"Y Nitta","year":"2014","unstructured":"Nitta, Y., Ding, P. & Zhang, Y. Identification of additional MAP kinases activated upon PAMP treatment. Plant Signal Behav. 9, e976155. https:\/\/doi.org\/10.4161\/15592324.2014.976155 (2014).","journal-title":"Plant Signal Behav."},{"key":"41981_CR50","doi-asserted-by":"publisher","first-page":"14","DOI":"10.3390\/plants11010014","volume":"11","author":"MJ Marcec","year":"2022","unstructured":"Marcec, M. J. & Tanaka, K. Crosstalk between calcium and ROS signaling during Flg22-triggered immune response in Arabidopsis leaves. Plants 11, 14 (2022).","journal-title":"Plants"},{"key":"41981_CR51","doi-asserted-by":"publisher","first-page":"1711","DOI":"10.1111\/nph.18626","volume":"237","author":"Y Fichman","year":"2023","unstructured":"Fichman, Y. et al. Phytochrome B regulates reactive oxygen signaling during abiotic and biotic stress in plants. New Phytol. 237, 1711\u20131727. https:\/\/doi.org\/10.1111\/nph.18626 (2023).","journal-title":"New Phytol."},{"key":"41981_CR52","doi-asserted-by":"publisher","first-page":"205","DOI":"10.1023\/B:PLAN.0000028786.57439.b3","volume":"54","author":"PG Sappl","year":"2004","unstructured":"Sappl, P. G., O\u00f1ate-S\u00e1nchez, L., Singh, K. B. & Millar, A. H. Proteomic analysis of glutathione S-transferases of Arabidopsis thaliana reveals differential salicylic acid-induced expression of the plant-specific phi and tau classes. Plant Mol. Biol. 54, 205\u2013219. https:\/\/doi.org\/10.1023\/B:PLAN.0000028786.57439.b3 (2004).","journal-title":"Plant Mol. Biol."},{"key":"41981_CR53","doi-asserted-by":"publisher","first-page":"52","DOI":"10.1104\/pp.111.191841","volume":"159","author":"T Pick","year":"2012","unstructured":"Pick, T., Jaskiewicz, M., Peterh\u00e4nsel, C. & Conrath, U. Heat shock factor HsfB1 primes gene transcription and systemic acquired resistance in Arabidopsis. Plant Physiol. 159, 52\u201355. https:\/\/doi.org\/10.1104\/pp.111.191841 (2012).","journal-title":"Plant Physiol."},{"key":"41981_CR54","doi-asserted-by":"publisher","first-page":"491","DOI":"10.1038\/nature22372","volume":"545","author":"G Xu","year":"2017","unstructured":"Xu, G. et al. uORF-mediated translation allows engineered plant disease resistance without fitness costs. Nature 545, 491\u2013494. https:\/\/doi.org\/10.1038\/nature22372 (2017).","journal-title":"Nature"},{"key":"41981_CR55","doi-asserted-by":"publisher","first-page":"152","DOI":"10.1093\/mp\/ssn095","volume":"2","author":"M Kumar","year":"2009","unstructured":"Kumar, M. et al. Heat shock factors HsfB1 and HsfB2b are involved in the regulation of Pdf1.2 expression and pathogen resistance in Arabidopsis. Mol. Plant 2, 152\u2013165. https:\/\/doi.org\/10.1093\/mp\/ssn095 (2009).","journal-title":"Mol. Plant"},{"key":"41981_CR56","doi-asserted-by":"publisher","first-page":"12935","DOI":"10.1073\/pnas.0602316103","volume":"103","author":"J Schwachtje","year":"2006","unstructured":"Schwachtje, J. et al. SNF1-related kinases allow plants to tolerate herbivory by allocating carbon to roots. Proc. Natl. Acad. Sci. 103, 12935\u201312940. https:\/\/doi.org\/10.1073\/pnas.0602316103 (2006).","journal-title":"Proc. Natl. Acad. Sci."},{"key":"41981_CR57","unstructured":"Gindro, K. et al. In Plant Defence: Biological Control (eds. M\u00e9rillon, J. M. & Ramawat, K. G.) 25\u201354 (Springer Netherlands, 2012)."},{"key":"41981_CR58","doi-asserted-by":"publisher","first-page":"351","DOI":"10.1007\/s00425-012-1776-x","volume":"237","author":"G Latouche","year":"2013","unstructured":"Latouche, G., Bellow, S., Poutaraud, A., Meyer, S. & Cerovic, Z. G. Influence of constitutive phenolic compounds on the response of grapevine (Vitis vinifera L.) leaves to infection by Plasmopara viticola. Planta 237, 351\u2013361. https:\/\/doi.org\/10.1007\/s00425-012-1776-x (2013).","journal-title":"Planta"},{"key":"41981_CR59","doi-asserted-by":"publisher","first-page":"5488","DOI":"10.1021\/jf030227o","volume":"51","author":"R Pezet","year":"2003","unstructured":"Pezet, R. et al. delta-viniferin, a resveratrol dehydrodimer: One of the major stilbenes synthesized by grapevine leaves. J. Agric. Food Chem. 51, 5488\u20135492 (2003).","journal-title":"J. Agric. Food Chem."},{"key":"41981_CR60","doi-asserted-by":"publisher","first-page":"235","DOI":"10.20870\/oeno-one.2018.52.3.2033","volume":"52","author":"O Viret","year":"2018","unstructured":"Viret, O., Spring, J.-L. & Gindro, K. Stilbenes: Biomarkers of grapevine resistance to fungal diseases. OENO One 52, 235\u2013241. https:\/\/doi.org\/10.20870\/oeno-one.2018.52.3.2033 (2018).","journal-title":"OENO One"},{"key":"41981_CR61","doi-asserted-by":"publisher","first-page":"128","DOI":"10.1016\/j.pmpp.2008.07.002","volume":"72","author":"S Schnee","year":"2008","unstructured":"Schnee, S., Viret, O. & Gindro, K. Role of stilbenes in the resistance of grapevine to powdery mildew. Physiol. Mol. Plant Pathol. 72, 128\u2013133 (2008).","journal-title":"Physiol. Mol. Plant Pathol."},{"key":"41981_CR62","doi-asserted-by":"publisher","first-page":"1043","DOI":"10.1093\/pcp\/pcy045","volume":"59","author":"A Vannozzi","year":"2018","unstructured":"Vannozzi, A. et al. Combinatorial regulation of stilbene synthase genes by WRKY and MYB transcription factors in grapevine (Vitis vinifera L.). Plant Cell Physiol. 59, 1043\u20131059. https:\/\/doi.org\/10.1093\/pcp\/pcy045 (2018).","journal-title":"Plant Cell Physiol."},{"key":"41981_CR63","doi-asserted-by":"publisher","first-page":"4135","DOI":"10.1105\/tpc.113.117127","volume":"25","author":"J Holl","year":"2013","unstructured":"Holl, J. et al. The R2R3-MYB transcription factors MYB14 and MYB15 regulate stilbene biosynthesis in Vitis vinifera. Plant Cell 25, 4135\u20134149. https:\/\/doi.org\/10.1105\/tpc.113.117127 (2013).","journal-title":"Plant Cell"},{"key":"41981_CR64","doi-asserted-by":"publisher","first-page":"404","DOI":"10.1186\/s12870-019-2014-5","volume":"19","author":"M Ciaffi","year":"2019","unstructured":"Ciaffi, M. et al. Transcriptional regulation of stilbene synthases in grapevine germplasm differentially susceptible to downy mildew. BMC Plant Biol. 19, 404. https:\/\/doi.org\/10.1186\/s12870-019-2014-5 (2019).","journal-title":"BMC Plant Biol."},{"key":"41981_CR65","doi-asserted-by":"publisher","first-page":"12193","DOI":"10.1038\/s41598-020-69051-6","volume":"10","author":"G Chitarrini","year":"2020","unstructured":"Chitarrini, G. et al. Two-omics data revealed commonalities and differences between Rpv12- and Rpv3-mediated resistance in grapevine. Sci. Rep. 10, 12193. https:\/\/doi.org\/10.1038\/s41598-020-69051-6 (2020).","journal-title":"Sci. Rep."},{"key":"41981_CR66","doi-asserted-by":"publisher","first-page":"864","DOI":"10.1126\/science.abg0929","volume":"372","author":"MK Rich","year":"2021","unstructured":"Rich, M. K. et al. Lipid exchanges drove the evolution of mutualism during plant terrestrialization. Science 372, 864\u2013868. https:\/\/doi.org\/10.1126\/science.abg0929 (2021).","journal-title":"Science"},{"key":"41981_CR67","doi-asserted-by":"publisher","DOI":"10.1101\/2022.03.28.486070","author":"C Cathebras","year":"2022","unstructured":"Cathebras, C. et al. A novel cis element enabled bacterial uptake by plant cells. bioRxiv https:\/\/doi.org\/10.1101\/2022.03.28.486070 (2022).","journal-title":"bioRxiv"}],"container-title":["Scientific Reports"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.nature.com\/articles\/s41598-023-41981-x.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/www.nature.com\/articles\/s41598-023-41981-x","content-type":"text\/html","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/www.nature.com\/articles\/s41598-023-41981-x.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2023,11,21]],"date-time":"2023-11-21T02:03:59Z","timestamp":1700532239000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.nature.com\/articles\/s41598-023-41981-x"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2023,9,6]]},"references-count":67,"journal-issue":{"issue":"1","published-online":{"date-parts":[[2023,12]]}},"alternative-id":["41981"],"URL":"https:\/\/doi.org\/10.1038\/s41598-023-41981-x","relation":{},"ISSN":["2045-2322"],"issn-type":[{"value":"2045-2322","type":"electronic"}],"subject":[],"published":{"date-parts":[[2023,9,6]]},"assertion":[{"value":"19 March 2023","order":1,"name":"received","label":"Received","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"4 September 2023","order":2,"name":"accepted","label":"Accepted","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"6 September 2023","order":3,"name":"first_online","label":"First Online","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"The authors declare no competing interests.","order":1,"name":"Ethics","group":{"name":"EthicsHeading","label":"Competing interests"}}],"article-number":"14664"}}