{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,3,10]],"date-time":"2026-03-10T01:47:47Z","timestamp":1773107267503,"version":"3.50.1"},"reference-count":103,"publisher":"Oxford University Press (OUP)","issue":"18","license":[{"start":{"date-parts":[[2021,6,9]],"date-time":"2021-06-09T00:00:00Z","timestamp":1623196800000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/academic.oup.com\/journals\/pages\/open_access\/funder_policies\/chorus\/standard_publication_model"}],"funder":[{"name":"Funda\u00e7\u00e3o para a Ci\u00eancia e Tecnologia","award":["UIDB\/04046\/2020"],"award-info":[{"award-number":["UIDB\/04046\/2020"]}]},{"name":"Funda\u00e7\u00e3o para a Ci\u00eancia e Tecnologia","award":["UIDP\/04046\/2020"],"award-info":[{"award-number":["UIDP\/04046\/2020"]}]},{"name":"GrapInfectomics","award":["PTDC\/ASP-HOR\/28485\/2017"],"award-info":[{"award-number":["PTDC\/ASP-HOR\/28485\/2017"]}]},{"name":"Spanish Ministry of Economy","award":["BIO2017-86375-R"],"award-info":[{"award-number":["BIO2017-86375-R"]}]},{"DOI":"10.13039\/501100000921","name":"European Cooperation in Science and Technology","doi-asserted-by":"publisher","id":[{"id":"10.13039\/501100000921","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":[],"published-print":{"date-parts":[[2021,9,30]]},"abstract":"<jats:title>Abstract<\/jats:title><jats:p>Grapevine (Vitis vinifera) berries are extremely sensitive to infection by the biotrophic pathogen Erysiphe necator, causing powdery mildew disease with deleterious effects on grape and wine quality. The combined analysis of the transcriptome and metabolome associated with this common fungal infection has not been previously carried out in any fruit. In order to identify the molecular, hormonal, and metabolic mechanisms associated with infection, healthy and naturally infected V. vinifera cv. Carignan berries were collected at two developmental stages: late green (EL33) and early v\u00e9raison (EL35). RNA sequencing combined with GC\u2013electron impact ionization time-of-flight MS, GC\u2013electron impact ionization\/quadrupole MS, and LC\u2013tandem MS analyses revealed that powdery mildew-susceptible grape berries were able to activate defensive mechanisms with the involvement of salicylic acid and jasmonates and to accumulate defense-associated metabolites (e.g. phenylpropanoids, fatty acids). The defensive strategies also indicated organ-specific responses, namely the activation of fatty acid biosynthesis. However, defense responses were not enough to restrict fungal growth. The fungal metabolic program during infection involves secretion of effectors related to effector-triggered susceptibility, carbohydrate-active enzymes and activation of sugar, fatty acid, and nitrogen uptake, and could be under epigenetic regulation. This study also identified potential metabolic biomarkers such as gallic, eicosanoic, and docosanoic acids and resveratrol, which can be used to monitor early stages of infection.<\/jats:p>","DOI":"10.1093\/jxb\/erab258","type":"journal-article","created":{"date-parts":[[2021,6,8]],"date-time":"2021-06-08T19:55:02Z","timestamp":1623182102000},"page":"6544-6569","source":"Crossref","is-referenced-by-count":38,"title":["Transcriptional, hormonal, and metabolic changes in susceptible grape berries under powdery mildew infection"],"prefix":"10.1093","volume":"72","author":[{"given":"Diana","family":"Pimentel","sequence":"first","affiliation":[{"name":"BioISI \u2013 Biosystems and Integrative Sciences Institute, Faculty of Sciences, University of Lisbon, Campo Grande, 1749-016 Lisboa, Portugal"}]},{"given":"Rute","family":"Amaro","sequence":"additional","affiliation":[{"name":"BioISI \u2013 Biosystems and Integrative Sciences Institute, Faculty of Sciences, University of Lisbon, Campo Grande, 1749-016 Lisboa, Portugal"}]},{"given":"Alexander","family":"Erban","sequence":"additional","affiliation":[{"name":"Max-Planck-Institut f\u00fcr Molekulare Pflanzenphysiologie, 14476 Potsdam-Golm, Germany"}]},{"given":"Nuria","family":"Mauri","sequence":"additional","affiliation":[{"name":"Instituto de Ciencias de la Vid y del Vino, CSIC-UR-Gobierno de La Rioja, Ctra. de Burgos km 6, 26007 Logro\u00f1o, Spain"}]},{"given":"Fl\u00e1vio","family":"Soares","sequence":"additional","affiliation":[{"name":"BioISI \u2013 Biosystems and Integrative Sciences Institute, Faculty of Sciences, University of Lisbon, Campo Grande, 1749-016 Lisboa, Portugal"}]},{"given":"Cec\u00edlia","family":"Rego","sequence":"additional","affiliation":[{"name":"Instituto Superior de Agronomia, Universidade de Lisboa, Tapada da Ajuda, 1349-017 Lisboa, Portugal"}]},{"given":"Jos\u00e9 M","family":"Mart\u00ednez-Zapater","sequence":"additional","affiliation":[{"name":"Instituto de Ciencias de la Vid y del Vino, CSIC-UR-Gobierno de La Rioja, Ctra. de Burgos km 6, 26007 Logro\u00f1o, Spain"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-5229-6913","authenticated-orcid":false,"given":"Axel","family":"Mith\u00f6fer","sequence":"additional","affiliation":[{"name":"Research Group Plant Defense Physiology, Max-Planck-Institute for Chemical Ecology, 07745 Jena, Germany"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-9675-4883","authenticated-orcid":false,"given":"Joachim","family":"Kopka","sequence":"additional","affiliation":[{"name":"Max-Planck-Institut f\u00fcr Molekulare Pflanzenphysiologie, 14476 Potsdam-Golm, Germany"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-7552-0164","authenticated-orcid":false,"given":"Ana Margarida","family":"Fortes","sequence":"additional","affiliation":[{"name":"BioISI \u2013 Biosystems and Integrative Sciences Institute, Faculty of Sciences, University of Lisbon, Campo Grande, 1749-016 Lisboa, Portugal"}]}],"member":"286","published-online":{"date-parts":[[2021,6,9]]},"reference":[{"key":"2021093021155303400_CIT0001","doi-asserted-by":"crossref","first-page":"1769","DOI":"10.1093\/jxb\/eru517","article-title":"Transcriptome and metabolome reprogramming in Vitis vinifera cv. Trincadeira berries upon infection with Botrytis cinerea","volume":"66","author":"Agudelo-Romero","year":"2015","journal-title":"Journal of Experimental Botany"},{"key":"2021093021155303400_CIT0002","doi-asserted-by":"crossref","first-page":"e60422","DOI":"10.1371\/journal.pone.0060422","article-title":"Search for transcriptional and metabolic markers of grape pre-ripening and ripening and insights into specific aroma development in three Portuguese cultivars","volume":"8","author":"Agudelo-Romero","year":"2013","journal-title":"PLoS One"},{"key":"2021093021155303400_CIT0003","doi-asserted-by":"crossref","first-page":"W91","DOI":"10.1093\/nar\/gkm260","article-title":"FatiGO +: a functional profiling tool for genomic data. Integration of functional annotation, regulatory motifs and interaction data with microarray experiments","volume":"35","author":"Al-Shahrour","year":"2007","journal-title":"Nucleic Acids Research"},{"key":"2021093021155303400_CIT0004","doi-asserted-by":"crossref","first-page":"15037","DOI":"10.1038\/hortres.2015.37","article-title":"Comparative transcriptomics of central Asian Vitis vinifera accessions reveals distinct defense strategies against powdery mildew","volume":"2","author":"Amrine","year":"2015","journal-title":"Horticulture Research"},{"key":"2021093021155303400_CIT0005","doi-asserted-by":"crossref","first-page":"166","DOI":"10.1093\/bioinformatics\/btu638","article-title":"HTSeq\u2014a Python framework to work with high-throughput sequencing data","volume":"31","author":"Anders","year":"2015","journal-title":"Bioinformatics"},{"key":"2021093021155303400_CIT0006","doi-asserted-by":"crossref","first-page":"73","DOI":"10.1007\/s00122-013-2202-x","article-title":"Grapevine powdery mildew resistance and susceptibility loci identified on a high-resolution SNP map","volume":"127","author":"Barba","year":"2014","journal-title":"Theoretical and Applied Genetics"},{"key":"2021093021155303400_CIT0007","doi-asserted-by":"crossref","first-page":"9119","DOI":"10.1021\/jf0618022","article-title":"Methyl jasmonate induces defense responses in grapevine and triggers protection against Erysiphe necator","volume":"54","author":"Belhadj","year":"2006","journal-title":"Journal of Agricultural and Food Chemistry"},{"key":"2021093021155303400_CIT0008","doi-asserted-by":"crossref","first-page":"5781","DOI":"10.1021\/jf800578c","article-title":"Ethephon elicits protection against Erysiphe necator in grapevine","volume":"56","author":"Belhadj","year":"2008","journal-title":"Journal of Agricultural and Food Chemistry"},{"key":"2021093021155303400_CIT0009","doi-asserted-by":"crossref","first-page":"8","DOI":"10.1093\/pcp\/pcx181","article-title":"Salicylic acid and jasmonic acid pathways are activated in spatially different domains around the infection site during effector-triggered immunity in Arabidopsis thaliana","volume":"59","author":"Betsuyaku","year":"2018","journal-title":"Plant & Cell Physiology"},{"key":"2021093021155303400_CIT0010","doi-asserted-by":"crossref","first-page":"248","DOI":"10.1016\/0003-2697(76)90527-3","article-title":"A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding","volume":"72","author":"Bradford","year":"1976","journal-title":"Analytical Biochemistry"},{"key":"2021093021155303400_CIT0011","doi-asserted-by":"crossref","first-page":"7973","DOI":"10.1039\/D0AN01753A","article-title":"Microfluidic device for multiplexed detection of fungal infection biomarkers in grape cultivars","volume":"145","author":"Br\u00e1s","year":"2021","journal-title":"The Analyst"},{"key":"2021093021155303400_CIT0012","doi-asserted-by":"crossref","first-page":"812","DOI":"10.1111\/pbi.13017","article-title":"The grapevine (Vitis vinifera) LysM receptor kinases VvLYK1-1 and VvLYK1-2 mediate chitooligosaccharide-triggered immunity","volume":"17","author":"Brul\u00e9","year":"2019","journal-title":"Plant Biotechnology Journal"},{"key":"2021093021155303400_CIT0013","doi-asserted-by":"crossref","first-page":"434","DOI":"10.1111\/j.0032-0862.2004.01016.x","article-title":"Effects of Uncinula necator on the yield and quality of grapes (Vitis vinifera) and wine","volume":"53","author":"Calonnec","year":"2004","journal-title":"Plant Pathology"},{"key":"2021093021155303400_CIT0014","doi-asserted-by":"crossref","first-page":"1808","DOI":"10.3389\/fpls.2018.01808","article-title":"Pathogenicity traits correlate with the susceptible Vitis vinifera leaf physiology transition in the biotroph fungus Erysiphe necator: an adaptation to plant ontogenic resistance","volume":"9","author":"Calonnec","year":"2018","journal-title":"Frontiers in Plant Science"},{"key":"2021093021155303400_CIT0015","doi-asserted-by":"crossref","first-page":"D233","DOI":"10.1093\/nar\/gkn663","article-title":"The Carbohydrate-Active EnZymes database (CAZy): an expert resource for glycogenomics","volume":"37","author":"Cantarel","year":"2009","journal-title":"Nucleic Acids Research"},{"key":"2021093021155303400_CIT0016","doi-asserted-by":"crossref","first-page":"266","DOI":"10.1016\/j.plantsci.2019.01.024","article-title":"The study of hormonal metabolism of Trincadeira and Syrah cultivars indicates new roles of salicylic acid, jasmonates, ABA and IAA during grape ripening and upon infection with Botrytis cinerea","volume":"283","author":"Coelho","year":"2019","journal-title":"Plant Science"},{"key":"2021093021155303400_CIT0017","doi-asserted-by":"crossref","first-page":"1599","DOI":"10.1093\/jxb\/48.8.1599","article-title":"The development of the grape berry cuticle in relation to susceptibility to bunch rot disease","volume":"48","author":"Commenil","year":"1997","journal-title":"Journal of Experimental Botany"},{"key":"2021093021155303400_CIT0018","doi-asserted-by":"crossref","first-page":"1150","DOI":"10.3389\/fpls.2016.01150","article-title":"Kaolin foliar application has a stimulatory effect on phenylpropanoid and flavonoid pathways in grape berries","volume":"7","author":"Conde","year":"2016","journal-title":"Frontiers in Plant Science"},{"key":"2021093021155303400_CIT0019","first-page":"1","article-title":"Biochemical changes throughout grape berry development and fruit and wine quality","volume":"1","author":"Conde","year":"2007","journal-title":"Food"},{"key":"2021093021155303400_CIT0020","doi-asserted-by":"crossref","first-page":"100","DOI":"10.1111\/j.1755-0238.1995.tb00086.x","article-title":"Growth stages of the grapevine: Adoption of a system for identifying grapevine growth stages","volume":"1","author":"Coombe","year":"1995","journal-title":"Australian Journal of Grape and Wine Research"},{"key":"2021093021155303400_CIT0021","doi-asserted-by":"crossref","first-page":"171","DOI":"10.1007\/978-1-4939-0844-8_14","article-title":"Profiling methods to identify cold-regulated primary metabolites using gas chromatography coupled to mass spectrometry","volume":"1166","author":"Dethloff","year":"2014","journal-title":"Methods in Molecular Biology"},{"key":"2021093021155303400_CIT0022","doi-asserted-by":"crossref","first-page":"3126","DOI":"10.1093\/jxb\/eraa046","article-title":"Drought stress modulates cuticular wax composition of the grape berry","volume":"71","author":"Dimopoulos","year":"2020","journal-title":"Journal of Experimental Botany"},{"key":"2021093021155303400_CIT0023","doi-asserted-by":"crossref","first-page":"366","DOI":"10.1016\/j.pbi.2007.04.020","article-title":"Networks of WRKY transcription factors in defense signaling","volume":"10","author":"Eulgem","year":"2007","journal-title":"Current Opinion in Plant Biology"},{"key":"2021093021155303400_CIT0024","doi-asserted-by":"crossref","first-page":"1255","DOI":"10.1071\/FP08173","article-title":"Identification of grapevine MLO gene candidates involved in susceptibility to powdery mildew","volume":"35","author":"Feechan","year":"2008","journal-title":"Functional Plant Biology"},{"key":"2021093021155303400_CIT0025","doi-asserted-by":"crossref","first-page":"732","DOI":"10.1016\/j.plaphy.2009.03.006","article-title":"Up-regulated transcripts in a compatible powdery mildew\u2013grapevine interaction","volume":"47","author":"Fekete","year":"2009","journal-title":"Plant Physiology and Biochemistry"},{"key":"2021093021155303400_CIT0026","doi-asserted-by":"crossref","first-page":"2601","DOI":"10.1105\/tpc.105.033910","article-title":"Arabidopsis SENESCENCE-ASSOCIATED GENE101 stabilizes and signals within an ENHANCED DISEASE SUSCEPTIBILITY1 complex in plant innate immunity","volume":"17","author":"Feys","year":"2005","journal-title":"The Plant Cell"},{"key":"2021093021155303400_CIT0027","doi-asserted-by":"crossref","first-page":"556","DOI":"10.1094\/PHYTO.2003.93.5.556","article-title":"Effects of ontogenic resistance upon establishment and growth of Uncinula necator on grape berries","volume":"93","author":"Ficke","year":"2003","journal-title":"Phytopathology"},{"key":"2021093021155303400_CIT0028","doi-asserted-by":"crossref","first-page":"149","DOI":"10.1186\/1471-2229-11-149","article-title":"Transcript and metabolite analysis in Trincadeira cultivar reveals novel information regarding the dynamics of grape ripening","volume":"11","author":"Fortes","year":"2011","journal-title":"BMC Plant Biology"},{"key":"2021093021155303400_CIT0029","doi-asserted-by":"crossref","first-page":"9326","DOI":"10.3390\/molecules20059326","article-title":"Complex interplay of hormonal signals during grape berry ripening","volume":"20","author":"Fortes","year":"2015","journal-title":"Molecules"},{"key":"2021093021155303400_CIT0030","doi-asserted-by":"crossref","first-page":"821","DOI":"10.1104\/pp.103.021428","article-title":"The monosaccharide transporter gene, AtSTP4, and the cell-wall invertase, Atbetafruct1, are induced in Arabidopsis during infection with the fungal biotroph Erysiphe cichoracearum","volume":"132","author":"Fotopoulos","year":"2003","journal-title":"Plant Physiology"},{"key":"2021093021155303400_CIT0031","doi-asserted-by":"crossref","first-page":"236","DOI":"10.1104\/pp.107.108712","article-title":"Powdery mildew induces defense-oriented reprogramming of the transcriptome in a susceptible but not in a resistant grapevine","volume":"146","author":"Fung","year":"2008","journal-title":"Plant Physiology"},{"key":"2021093021155303400_CIT0032","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1111\/j.1364-3703.2011.00728.x","article-title":"Grapevine powdery mildew (Erysiphe necator): a fascinating system for the study of the biology, ecology and epidemiology of an obligate biotroph","volume":"13","author":"Gadoury","year":"2012","journal-title":"Molecular Plant Pathology"},{"key":"2021093021155303400_CIT0033","doi-asserted-by":"crossref","first-page":"547","DOI":"10.1094\/PHYTO.2003.93.5.547","article-title":"Ontogenic resistance to powdery mildew in grape berries","volume":"93","author":"Gadoury","year":"2003","journal-title":"Phytopathology"},{"key":"2021093021155303400_CIT0034","doi-asserted-by":"crossref","first-page":"137","DOI":"10.1094\/PDIS.2001.85.2.137","article-title":"Effects of powdery mildew on vine growth, yield, and quality of Concord grapes","volume":"85","author":"Gadoury","year":"2001","journal-title":"Plant Disease"},{"key":"2021093021155303400_CIT0035","doi-asserted-by":"crossref","first-page":"1356","DOI":"10.1094\/PHYTO-97-10-1356","article-title":"Effects of diffuse colonization of grape berries by Uncinula necator on bunch rots, berry microflora, and juice and wine quality","volume":"97","author":"Gadoury","year":"2007","journal-title":"Phytopathology"},{"key":"2021093021155303400_CIT0036","doi-asserted-by":"crossref","first-page":"381","DOI":"10.1007\/s11103-014-0235-4","article-title":"Functions of EDS1-like and PAD4 genes in grapevine defenses against powdery mildew","volume":"86","author":"Gao","year":"2014","journal-title":"Plant Molecular Biology"},{"key":"2021093021155303400_CIT0037","doi-asserted-by":"crossref","first-page":"1037","DOI":"10.1007\/s00425-010-1107-z","article-title":"A functional EDS1 ortholog is differentially regulated in powdery mildew resistant and susceptible grapevines and complements an Arabidopsis eds1 mutant","volume":"231","author":"Gao","year":"2010","journal-title":"Planta"},{"key":"2021093021155303400_CIT0038","doi-asserted-by":"crossref","first-page":"205","DOI":"10.1146\/annurev.phyto.43.040204.135923","article-title":"Contrasting mechanisms of defense against biotrophic and necrotrophic pathogens","volume":"43","author":"Glazebrook","year":"2005","journal-title":"Annual Review of Phytopathology"},{"key":"2021093021155303400_CIT0039","doi-asserted-by":"crossref","first-page":"e1003007","DOI":"10.1371\/journal.ppat.1003007","article-title":"Epigenetics of host-pathogen interactions: the road ahead and the road behind","volume":"8","author":"G\u00f3mez-D\u00edaz","year":"2012","journal-title":"PLoS Pathogens"},{"key":"2021093021155303400_CIT0040","doi-asserted-by":"crossref","first-page":"312","DOI":"10.1016\/j.ygeno.2019.02.011","article-title":"Genome-wide characterization revealed role of NBS-LRR genes during powdery mildew infection in Vitis vinifera","volume":"112","author":"Goyal","year":"2020","journal-title":"Genomics"},{"key":"2021093021155303400_CIT0041","doi-asserted-by":"crossref","first-page":"254","DOI":"10.1111\/j.1365-313X.2010.04235.x","article-title":"A role for \u03b2-sitosterol to stigmasterol conversion in plant-pathogen interactions","volume":"63","author":"Griebel","year":"2010","journal-title":"The Plant Journal"},{"key":"2021093021155303400_CIT0042","doi-asserted-by":"crossref","first-page":"15968","DOI":"10.1038\/s41598-017-16240-5","article-title":"The lateral organ boundaries domain gene family in grapevine: genome-wide characterization and expression analyses during developmental processes and stress responses","volume":"7","author":"Grimplet","year":"2017","journal-title":"Scientific Reports"},{"key":"2021093021155303400_CIT0043","doi-asserted-by":"crossref","first-page":"213","DOI":"10.1186\/1756-0500-5-213","article-title":"Comparative analysis of grapevine whole-genome gene predictions, functional annotation, categorization and integration of the predicted gene sequences","volume":"5","author":"Grimplet","year":"2012","journal-title":"BMC Research Notes"},{"key":"2021093021155303400_CIT0044","doi-asserted-by":"crossref","first-page":"2847","DOI":"10.1093\/bioinformatics\/btw313","article-title":"Complex heatmaps reveal patterns and correlations in multidimensional genomic data","volume":"32","author":"Gu","year":"2016","journal-title":"Bioinformatics"},{"key":"2021093021155303400_CIT0045","doi-asserted-by":"crossref","first-page":"211","DOI":"10.1104\/pp.110.154765","article-title":"Involvement of abscisic acid in the coordinated regulation of a stress-inducible hexose transporter (VvHT5) and a cell wall invertase in grapevine in response to biotrophic fungal infection","volume":"153","author":"Hayes","year":"2010","journal-title":"Plant Physiology"},{"key":"2021093021155303400_CIT0046","doi-asserted-by":"crossref","first-page":"1569","DOI":"10.3389\/fpls.2018.01569","article-title":"A holistic approach to analyze systemic Jasmonate accumulation in individual leaves of Arabidopsis rosettes upon wounding","volume":"9","author":"Heyer","year":"2018","journal-title":"Frontiers in Plant Science"},{"key":"2021093021155303400_CIT0047","doi-asserted-by":"crossref","first-page":"427","DOI":"10.1007\/s00122-007-0680-4","article-title":"Resistance to Erysiphe necator in the grapevine \u2018Kishmish vatkana\u2019 is controlled by a single locus through restriction of hyphal growth","volume":"116","author":"Hoffmann","year":"2008","journal-title":"Theoretical and Applied Genetics"},{"key":"2021093021155303400_CIT0048","doi-asserted-by":"crossref","first-page":"322","DOI":"10.1007\/s11306-010-0198-7","article-title":"Decision tree supported substructure prediction of metabolites from GC-MS profiles","volume":"6","author":"Hummel","year":"2010","journal-title":"Metabolomics"},{"key":"2021093021155303400_CIT0049","doi-asserted-by":"crossref","first-page":"463","DOI":"10.1038\/nature06148","article-title":"The grapevine genome sequence suggests ancestral hexaploidization in major angiosperm phyla","volume":"449","author":"Jaillon","year":"2007","journal-title":"Nature"},{"key":"2021093021155303400_CIT0050","doi-asserted-by":"crossref","first-page":"158520","DOI":"10.1016\/j.bbalip.2019.158520","article-title":"Omega hydroxylated JA-Ile is an endogenous bioactive jasmonate that signals through the canonical jasmonate signaling pathway","volume":"1864","author":"Jimenez-Aleman","year":"2019","journal-title":"Biochimica et Biophysica Acta. Molecular and Cell Biology of Lipids"},{"key":"2021093021155303400_CIT0051","doi-asserted-by":"crossref","first-page":"323","DOI":"10.1038\/nature05286","article-title":"The plant immune system","volume":"444","author":"Jones","year":"2006","journal-title":"Nature"},{"key":"2021093021155303400_CIT0052","doi-asserted-by":"crossref","first-page":"1081","DOI":"10.1186\/1471-2164-15-1081","article-title":"Adaptive genomic structural variation in the grape powdery mildew pathogen, Erysiphe necator","volume":"15","author":"Jones","year":"2014","journal-title":"BMC Genomics"},{"key":"2021093021155303400_CIT0053","doi-asserted-by":"crossref","first-page":"357","DOI":"10.1038\/nmeth.3317","article-title":"HISAT: a fast spliced aligner with low memory requirements","volume":"12","author":"Kim","year":"2015","journal-title":"Nature Methods"},{"key":"2021093021155303400_CIT0054","doi-asserted-by":"crossref","first-page":"88","DOI":"10.3389\/fpls.2012.00088","article-title":"The cell wall-associated kinases, WAKs, as pectin receptors","volume":"3","author":"Kohorn","year":"2012","journal-title":"Frontiers in Plant Science"},{"key":"2021093021155303400_CIT0055","doi-asserted-by":"crossref","first-page":"9298","DOI":"10.1073\/pnas.1103542108","article-title":"Cytochrome P450 CYP94B3 mediates catabolism and inactivation of the plant hormone jasmonoyl-L-isoleucine","volume":"108","author":"Koo","year":"2011","journal-title":"Proceedings of the National Academy of Sciences, USA"},{"key":"2021093021155303400_CIT0056","doi-asserted-by":"crossref","first-page":"29728","DOI":"10.1074\/jbc.M114.603084","article-title":"Endoplasmic reticulum-associated inactivation of the hormone jasmonoyl-L-isoleucine by multiple members of the cytochrome P450 94 family in Arabidopsis","volume":"289","author":"Koo","year":"2014","journal-title":"The Journal of Biological Chemistry"},{"key":"2021093021155303400_CIT0057","doi-asserted-by":"crossref","first-page":"1635","DOI":"10.1093\/bioinformatics\/bti236","article-title":"GMD@CSB.DB: the Golm Metabolome Database","volume":"21","author":"Kopka","year":"2005","journal-title":"Bioinformatics"},{"key":"2021093021155303400_CIT0058","doi-asserted-by":"crossref","first-page":"179","DOI":"10.1094\/MPMI-12-16-0255-CR","article-title":"mlo-based resistance: an apparently universal \u201cweapon\u201d to defeat powdery mildew disease","volume":"30","author":"Kusch","year":"2017","journal-title":"Molecular Plant-Microbe Interactions"},{"key":"2021093021155303400_CIT0059","doi-asserted-by":"crossref","first-page":"4005","DOI":"10.1021\/acs.jafc.5b00013","article-title":"A focus on the biosynthesis and composition of cuticle in fruits","volume":"63","author":"Lara","year":"2015","journal-title":"Journal of Agricultural and Food Chemistry"},{"key":"2021093021155303400_CIT0060","doi-asserted-by":"crossref","first-page":"770","DOI":"10.3389\/fpls.2019.00770","article-title":"Shelf life potential and the fruit cuticle: the unexpected player","volume":"10","author":"Lara","year":"2019","journal-title":"Frontiers in Plant Science"},{"key":"2021093021155303400_CIT0061","first-page":"23","article-title":"Role of phenolics in the resistance mechanisms of plants against fungal pathogens and insects","volume":"661","author":"Lattanzio","year":"2006","journal-title":"Phytochemistry: Advances in Research"},{"key":"2021093021155303400_CIT0062","doi-asserted-by":"crossref","first-page":"1325","DOI":"10.1007\/s00425-010-1258-y","article-title":"Expression and functional analysis of two genes encoding transcription factors, VpWRKY1 and VpWRKY2, isolated from Chinese wild Vitis pseudoreticulata.","volume":"232","author":"Li","year":"2010","journal-title":"Planta"},{"key":"2021093021155303400_CIT0063","doi-asserted-by":"crossref","first-page":"969","DOI":"10.1016\/j.jplph.2006.07.006","article-title":"OsWRKY71, a rice transcription factor, is involved in rice defense response","volume":"164","author":"Liu","year":"2007","journal-title":"Journal of Plant Physiology"},{"key":"2021093021155303400_CIT0064","doi-asserted-by":"crossref","first-page":"6","DOI":"10.1007\/BF02668658","article-title":"A simple and efficient method for DNA extraction from grapevine cultivars and Vitis species","volume":"12","author":"Lodhi","year":"1994","journal-title":"Plant Molecular Biology Reporter"},{"key":"2021093021155303400_CIT0065","doi-asserted-by":"crossref","first-page":"732","DOI":"10.1093\/bioinformatics\/btn023","article-title":"TagFinder for the quantitative analysis of gas chromatography\u2013mass spectrometry (GC-MS)-based metabolite profiling experiments","volume":"24","author":"Luedemann","year":"2008","journal-title":"Bioinformatics"},{"key":"2021093021155303400_CIT0066","doi-asserted-by":"crossref","first-page":"412","DOI":"10.1016\/j.pbi.2008.05.001","article-title":"Evolution of prokaryotic and eukaryotic virulence effectors","volume":"11","author":"Ma","year":"2008","journal-title":"Current Opinion in Plant Biology"},{"key":"2021093021155303400_CIT0067","doi-asserted-by":"crossref","first-page":"365","DOI":"10.1111\/ppl.12251","article-title":"The transcription factor VvWRKY33 is involved in the regulation of grapevine (Vitis vinifera) defense against the oomycete pathogen Plasmopara viticola","volume":"153","author":"Merz","year":"2015","journal-title":"Physiologia Plantarum"},{"key":"2021093021155303400_CIT0068","doi-asserted-by":"crossref","first-page":"1226","DOI":"10.1104\/pp.110.168617","article-title":"12-Hydroxyjasmonic acid glucoside is a COI1-JAZ-independent activator of leaf-closing movement in Samanea saman","volume":"155","author":"Nakamura","year":"2011","journal-title":"Plant Physiology"},{"key":"2021093021155303400_CIT0069","doi-asserted-by":"crossref","first-page":"321","DOI":"10.5344\/ajev.1979.30.4.321","article-title":"Powdery mildew sensory effect on wine","volume":"30","author":"Ough","year":"1979","journal-title":"American Journal of Enology and Viticulture"},{"key":"2021093021155303400_CIT0070","doi-asserted-by":"crossref","first-page":"316","DOI":"10.1007\/s10327-017-0728-5","article-title":"Investigations on the role of cuticular wax in resistance to powdery mildew in grapevine","volume":"83","author":"\u00d6zer","year":"2017","journal-title":"Journal of General Plant Pathology"},{"key":"2021093021155303400_CIT0071","doi-asserted-by":"crossref","first-page":"170","DOI":"10.1186\/s12870-016-0855-8","article-title":"Identification of two novel powdery mildew resistance loci, Ren6 and Ren7, from the wild Chinese grape species Vitis piasezkii","volume":"16","author":"Pap","year":"2016","journal-title":"BMC Plant Biology"},{"key":"2021093021155303400_CIT0072","doi-asserted-by":"crossref","first-page":"16016","DOI":"10.1038\/hortres.2016.16","article-title":"Knockdown of MLO genes reduces susceptibility to powdery mildew in grapevine","volume":"3","author":"Pessina","year":"2016","journal-title":"Horticulture Research"},{"key":"2021093021155303400_CIT0073","doi-asserted-by":"crossref","first-page":"415","DOI":"10.1111\/ajgw.12291","article-title":"Feasibility of discriminating powdery mildew-affected grape berries at harvest using mid-infrared attenuated total reflection spectroscopy and fatty acid profiling","volume":"23","author":"Petrovic","year":"2017","journal-title":"Australian Journal of Grape and Wine Research"},{"key":"2021093021155303400_CIT0074","first-page":"85","article-title":"The phenolic composition of red grapes and wines as influenced by Oidium tuckeri development","volume":"38","author":"Piermattei","year":"1999","journal-title":"Vitis"},{"key":"2021093021155303400_CIT0075","doi-asserted-by":"crossref","first-page":"162","DOI":"10.1093\/pcp\/pct167","article-title":"Members of the NPF3 transporter subfamily encode pathogen-inducible nitrate\/nitrite transporters in grapevine and Arabidopsis","volume":"55","author":"Pike","year":"2014","journal-title":"Plant & Cell Physiology"},{"key":"2021093021155303400_CIT0076","doi-asserted-by":"crossref","first-page":"15020","DOI":"10.1038\/hortres.2015.20","article-title":"Current understanding of grapevine defense mechanisms against the biotrophic fungus (Erysiphe necator), the causal agent of powdery mildew disease","volume":"2","author":"Qiu","year":"2015","journal-title":"Horticulture Research"},{"key":"2021093021155303400_CIT0077","doi-asserted-by":"crossref","first-page":"1059","DOI":"10.1007\/s00122-010-1511-6","article-title":"Using a limited mapping strategy to identify major QTLs for resistance to grapevine powdery mildew (Erysiphe necator) and their use in marker-assisted breeding","volume":"122","author":"Riaz","year":"2011","journal-title":"Theoretical and Applied Genetics"},{"key":"2021093021155303400_CIT0078","doi-asserted-by":"crossref","first-page":"107","DOI":"10.1111\/j.1469-8137.2011.03675.x","article-title":"Different roles of Enhanced Disease Susceptibility1 (EDS1) bound to and dissociated from Phytoalexin Deficient4 (PAD4) in Arabidopsis immunity","volume":"191","author":"Rietz","year":"2011","journal-title":"New Phytologist"},{"key":"2021093021155303400_CIT0079","doi-asserted-by":"crossref","first-page":"317","DOI":"10.1146\/annurev-phyto-073009-114447","article-title":"Hormone crosstalk in plant disease and defense: more than just jasmonate-salicylate antagonism","volume":"49","author":"Robert-Seilaniantz","year":"2011","journal-title":"Annual Review of Phytopathology"},{"key":"2021093021155303400_CIT0080","doi-asserted-by":"crossref","first-page":"139","DOI":"10.1093\/bioinformatics\/btp616","article-title":"edgeR: a Bioconductor package for differential expression analysis of digital gene expression data","volume":"26","author":"Robinson","year":"2010","journal-title":"Bioinformatics"},{"key":"2021093021155303400_CIT0081","doi-asserted-by":"crossref","first-page":"R25","DOI":"10.1186\/gb-2010-11-3-r25","article-title":"A scaling normalization method for differential expression analysis of RNA-seq data","volume":"11","author":"Robinson","year":"2010","journal-title":"Genome Biology"},{"key":"2021093021155303400_CIT0082","doi-asserted-by":"crossref","first-page":"47","DOI":"10.1016\/j.fbr.2018.07.003","article-title":"Essential, deadly, enigmatic: Polyamine metabolism and roles in fungal cells","volume":"33","author":"Rocha","year":"2019","journal-title":"Fungal Biology Reviews"},{"key":"2021093021155303400_CIT0083","doi-asserted-by":"crossref","first-page":"2440","DOI":"10.1105\/tpc.111.084301","article-title":"The Arabidopsis leucine-rich repeat receptor-like kinases BAK1\/SERK3 and BKK1\/SERK4 are required for innate immunity to hemibiotrophic and biotrophic pathogens","volume":"23","author":"Roux","year":"2011","journal-title":"The Plant Cell"},{"key":"2021093021155303400_CIT0084","doi-asserted-by":"crossref","first-page":"295","DOI":"10.1105\/tpc.104.026013","article-title":"Functional analysis of Avr9\/Cf-9 rapidly elicited genes identifies a protein kinase, ACIK1, that is essential for full Cf-9-dependent disease resistance in tomato","volume":"17","author":"Rowland","year":"2005","journal-title":"The Plant Cell"},{"key":"2021093021155303400_CIT0085","doi-asserted-by":"crossref","first-page":"128","DOI":"10.1016\/j.pmpp.2008.07.002","article-title":"Role of stilbenes in the resistance of grapevine to powdery mildew","volume":"72","author":"Schnee","year":"2008","journal-title":"Physiological and Molecular Plant Pathology"},{"key":"2021093021155303400_CIT0086","doi-asserted-by":"crossref","first-page":"9444","DOI":"10.1074\/jbc.M109.096842","article-title":"Rapid heteromerization and phosphorylation of ligand-activated plant transmembrane receptors and their associated kinase BAK1","volume":"285","author":"Schulze","year":"2010","journal-title":"The Journal of Biological Chemistry"},{"key":"2021093021155303400_CIT0087","doi-asserted-by":"crossref","first-page":"144","DOI":"10.5344\/ajev.1965.16.3.144","article-title":"Colorimetry of total phenolics with phosphomolybdic-phosphotungstic acid reagents","volume":"16","author":"Singleton","year":"1965","journal-title":"American Journal of Enology and Viticulture"},{"key":"2021093021155303400_CIT0088","doi-asserted-by":"crossref","first-page":"51","DOI":"10.1016\/j.pbi.2015.05.025","article-title":"Chromatin-based control of effector gene expression in plant-associated fungi","volume":"26","author":"Soyer","year":"2015","journal-title":"Current Opinion in Plant Biology"},{"key":"2021093021155303400_CIT0089","doi-asserted-by":"crossref","first-page":"2117","DOI":"10.1105\/tpc.104.023549","article-title":"The oxylipin signal jasmonic acid is activated by an enzyme that conjugates it to isoleucine in Arabidopsis","volume":"16","author":"Staswick","year":"2004","journal-title":"The Plant Cell"},{"key":"2021093021155303400_CIT0090","doi-asserted-by":"crossref","first-page":"182","DOI":"10.1016\/j.jchromb.2008.04.042","article-title":"Retention index thresholds for compound matching in GC-MS metabolite profiling","volume":"871","author":"Strehmel","year":"2008","journal-title":"Journal of Chromatography. B, Analytical Technologies in the Biomedical and Life Sciences"},{"key":"2021093021155303400_CIT0091","doi-asserted-by":"crossref","first-page":"30825","DOI":"10.1038\/srep30825","article-title":"Expression of a grapevine NAC transcription factor gene is induced in response to powdery mildew colonization in salicylic acid-independent manner","volume":"6","author":"Toth","year":"2016","journal-title":"Scientific Reports"},{"key":"2021093021155303400_CIT0092","doi-asserted-by":"crossref","first-page":"e1004015","DOI":"10.1371\/journal.pgen.1004015","article-title":"Dual regulation of gene expression mediated by extended MAPK activation and salicylic acid contributes to robust innate immunity in Arabidopsis thaliana","volume":"9","author":"Tsuda","year":"2013","journal-title":"PLoS Genetics"},{"key":"2021093021155303400_CIT0093","doi-asserted-by":"crossref","first-page":"225","DOI":"10.1007\/978-1-4939-7819-9_16","article-title":"Acquisition of volatile compounds by gas chromatography-mass spectrometry (GC-MS)","volume":"1778","author":"Vallarino","year":"2018","journal-title":"Methods in Molecular Biology"},{"key":"2021093021155303400_CIT0094","doi-asserted-by":"crossref","first-page":"619","DOI":"10.1016\/j.chom.2013.11.006","article-title":"Structural basis for signaling by exclusive EDS1 heteromeric complexes with SAG101 or PAD4 in plant innate immunity","volume":"14","author":"Wagner","year":"2013","journal-title":"Cell Host & Microbe"},{"key":"2021093021155303400_CIT0095","doi-asserted-by":"crossref","first-page":"471","DOI":"10.1105\/tpc.107.056754","article-title":"A LysM receptor-like kinase plays a critical role in chitin signaling and fungal resistance in Arabidopsis","volume":"20","author":"Wan","year":"2008","journal-title":"The Plant Cell"},{"key":"2021093021155303400_CIT0096","doi-asserted-by":"crossref","first-page":"1784","DOI":"10.1016\/j.cub.2007.09.025","article-title":"Salicylic acid inhibits pathogen growth in plants through repression of the auxin signaling pathway","volume":"17","author":"Wang","year":"2007","journal-title":"Current Biology"},{"key":"2021093021155303400_CIT0097","first-page":"74","article-title":"Insights into auxin signaling in plant\u2013pathogen interactions","volume":"2","author":"Wang","year":"2011","journal-title":"Frontiers in Plant Science"},{"key":"2021093021155303400_CIT0098","first-page":"97","article-title":"Ectopic expression of the wild grape WRKY transcription factor VqWRKY52 in Arabidopsis thaliana enhances resistance to the biotrophic pathogen powdery mildew but not to the necrotrophic pathogen Botrytis cinerea","volume":"8","author":"Wang","year":"2017","journal-title":"Frontiers in Plant Science"},{"key":"2021093021155303400_CIT0099","first-page":"159","article-title":"Evaluation of foliar resistance to Uncinula necator in Chinese wild Vitis species","volume":"34","author":"Wang","year":"1995","journal-title":"Vitis"},{"key":"2021093021155303400_CIT0100","doi-asserted-by":"crossref","first-page":"14049","DOI":"10.1038\/hortres.2014.49","article-title":"Transcriptome of Erysiphe necator-infected Vitis pseudoreticulata leaves provides insight into grapevine resistance to powdery mildew","volume":"1","author":"Weng","year":"2014","journal-title":"Horticulture Research"},{"key":"2021093021155303400_CIT0101","doi-asserted-by":"crossref","first-page":"592","DOI":"10.1111\/j.1365-313X.2006.02901.x","article-title":"Arabidopsis WRKY33 transcription factor is required for resistance to necrotrophic fungal pathogens","volume":"48","author":"Zheng","year":"2006","journal-title":"The Plant Journal"},{"key":"2021093021155303400_CIT0102","doi-asserted-by":"crossref","first-page":"2109","DOI":"10.1007\/s00299-012-1321-1","article-title":"VpWRKY3, a biotic and abiotic stress-related transcription factor from the Chinese wild Vitis pseudoreticulata","volume":"31","author":"Zhu","year":"2012","journal-title":"Plant Cell Reports"},{"key":"2021093021155303400_CIT0103","doi-asserted-by":"crossref","first-page":"1088","DOI":"10.3389\/fpls.2018.01088","article-title":"Multifunctional roles of plant cuticle during plant-pathogen interactions","volume":"9","author":"Ziv","year":"2018","journal-title":"Frontiers in Plant Science"}],"container-title":["Journal of Experimental Botany"],"original-title":[],"language":"en","link":[{"URL":"http:\/\/academic.oup.com\/jxb\/advance-article-pdf\/doi\/10.1093\/jxb\/erab258\/39503125\/erab258.pdf","content-type":"application\/pdf","content-version":"am","intended-application":"syndication"},{"URL":"http:\/\/academic.oup.com\/jxb\/article-pdf\/72\/18\/6544\/40489909\/erab258.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"syndication"},{"URL":"http:\/\/academic.oup.com\/jxb\/article-pdf\/72\/18\/6544\/40489909\/erab258.pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2023,11,4]],"date-time":"2023-11-04T17:39:15Z","timestamp":1699119555000},"score":1,"resource":{"primary":{"URL":"https:\/\/academic.oup.com\/jxb\/article\/72\/18\/6544\/6295384"}},"subtitle":[],"editor":[{"given":"Ariel","family":"Vicente","sequence":"additional","affiliation":[{"name":"CONICET \u2013 National University of La Plata, Argentina"}]}],"short-title":[],"issued":{"date-parts":[[2021,6,9]]},"references-count":103,"journal-issue":{"issue":"18","published-online":{"date-parts":[[2021,6,9]]},"published-print":{"date-parts":[[2021,9,30]]}},"URL":"https:\/\/doi.org\/10.1093\/jxb\/erab258","relation":{},"ISSN":["0022-0957","1460-2431"],"issn-type":[{"value":"0022-0957","type":"print"},{"value":"1460-2431","type":"electronic"}],"subject":[],"published-other":{"date-parts":[[2021,9,30]]},"published":{"date-parts":[[2021,6,9]]}}}