{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,8,3]],"date-time":"2026-08-03T05:46:13Z","timestamp":1785735973435,"version":"3.56.0"},"reference-count":48,"publisher":"Frontiers Media SA","license":[{"start":{"date-parts":[[2026,8,3]],"date-time":"2026-08-03T00:00:00Z","timestamp":1785715200000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/501100004837","name":"Ministerio de Ciencia e Innovaci\u00f3n","doi-asserted-by":"publisher","award":["PID2024-160692OB-I00"],"award-info":[{"award-number":["PID2024-160692OB-I00"]}],"id":[{"id":"10.13039\/501100004837","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100011011","name":"Junta de Andaluc\u00eda","doi-asserted-by":"publisher","id":[{"id":"10.13039\/501100011011","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":["frontiersin.org"],"crossmark-restriction":true},"short-container-title":["Front. Plant Sci."],"abstract":"<jats:p>\n                    The plant cuticle plays several roles with agronomic relevance such as controlling water loss or protecting against ultraviolet (UV) radiation and mechanical damage. In tomato fruit cuticle, phenolics are chiefly the flavonoid chalconaringenin and a small portion of phenolic acids. They confer the cuticle mechanical resistance as well as thermal properties and UV photoprotection. Nine QTLs related to the accumulation of cuticle phenolics in tomato fruit were previously detected in a\n                    <jats:italic>Solanum lycopersicum<\/jats:italic>\n                    \u00d7\n                    <jats:italic>S. pimpinellifolium<\/jats:italic>\n                    recombinant inbred population. Confocal Raman microscopy has been employed to separate the effect of these cuticle QTLs on the two phenolic fractions, showing that most QTL lines preferentially affected chalconaringenin accumulation, with only two QTL lines (\n                    <jats:italic>ph8.1<\/jats:italic>\n                    and\n                    <jats:italic>ph12.1<\/jats:italic>\n                    ) having an equal effect on both chalconaringenin and phenolic acids. A QTL pyramiding strategy has been employed to study the combined effect of different\n                    <jats:italic>loci<\/jats:italic>\n                    and has revealed a complex array of interactions. Approximately 80% of the double and triple QTL lines displayed significant epistatic interaction. Notably, a QTL combination between chromosomes 5 and 12 that increases the percentage of cuticle phenolics beyond single QTL lines was identified.\n                    <jats:italic>CHALCONE SYNTHASE<\/jats:italic>\n                    (\n                    <jats:italic>CHS1<\/jats:italic>\n                    and\n                    <jats:italic>CHS2<\/jats:italic>\n                    ) expression analyses have shown that\n                    <jats:italic>CHS1<\/jats:italic>\n                    seems to be the main enzyme responsible for the synthesis of chalconaringenin that is accumulated within the cuticle. Additionally, an\n                    <jats:italic>S. pimpinellifolium<\/jats:italic>\n                    genomic region in chromosome 5 that favors\n                    <jats:italic>CHALCONE ISOMERASE1<\/jats:italic>\n                    expression in the peel of ripening tomatoes without affecting chalconaringenin accumulation in the cuticle was identified, raising the possibility of an increase in fruit of downstream flavonols without compromising cuticle phenolics.\n                  <\/jats:p>","DOI":"10.3389\/fpls.2026.1863369","type":"journal-article","created":{"date-parts":[[2026,8,3]],"date-time":"2026-08-03T05:31:29Z","timestamp":1785735089000},"update-policy":"https:\/\/doi.org\/10.3389\/crossmark-policy","source":"Crossref","is-referenced-by-count":0,"title":["QTL pyramiding uncovers epistatic interactions that modify cuticle phenolics in tomato"],"prefix":"10.3389","volume":"17","author":[{"given":"Rida","family":"Barraj Barraj","sequence":"first","affiliation":[{"name":"Instituto de Hortofruticultura Subtropical y Mediterr\u00e1nea \u201cLa Mayora\u201d, Universidad de M\u00e1laga-Consejo Superior de Investigaciones Cient\u00edficas, Departamento de Mejora Gen\u00e9tica y Biotecnolog\u00eda, Estaci\u00f3n Experimental La Mayora","place":["M\u00e1laga, Spain"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Mar\u00eda","family":"Urrutia","sequence":"additional","affiliation":[{"name":"Instituto de Hortofruticultura Subtropical y Mediterr\u00e1nea \u201cLa Mayora\u201d, Universidad de M\u00e1laga-Consejo Superior de Investigaciones Cient\u00edficas, Departamento de Mejora Gen\u00e9tica y Biotecnolog\u00eda, Estaci\u00f3n Experimental La Mayora","place":["M\u00e1laga, Spain"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Juan Carlos","family":"Mateos del Amo","sequence":"additional","affiliation":[{"name":"Instituto de Hortofruticultura Subtropical y Mediterr\u00e1nea \u201cLa Mayora\u201d, Universidad de M\u00e1laga-Consejo Superior de Investigaciones Cient\u00edficas, Departamento de Biolog\u00eda Molecular y Bioqu\u00edmica, Universidad de M\u00e1laga","place":["M\u00e1laga, Spain"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Ana","family":"Gonz\u00e1lez Moreno","sequence":"additional","affiliation":[{"name":"Instituto de Hortofruticultura Subtropical y Mediterr\u00e1nea \u201cLa Mayora\u201d, Universidad de M\u00e1laga-Consejo Superior de Investigaciones Cient\u00edficas, Departamento de Biolog\u00eda Molecular y Bioqu\u00edmica, Universidad de M\u00e1laga","place":["M\u00e1laga, Spain"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Antonio","family":"Heredia","sequence":"additional","affiliation":[{"name":"Instituto de Hortofruticultura Subtropical y Mediterr\u00e1nea \u201cLa Mayora\u201d, Universidad de M\u00e1laga-Consejo Superior de Investigaciones Cient\u00edficas, Departamento de Biolog\u00eda Molecular y Bioqu\u00edmica, Universidad de M\u00e1laga","place":["M\u00e1laga, Spain"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Rafael","family":"Fern\u00e1ndez-Mu\u00f1oz","sequence":"additional","affiliation":[{"name":"Instituto de Hortofruticultura Subtropical y Mediterr\u00e1nea \u201cLa Mayora\u201d, Universidad de M\u00e1laga-Consejo Superior de Investigaciones Cient\u00edficas, Departamento de Mejora Gen\u00e9tica y Biotecnolog\u00eda, Estaci\u00f3n Experimental La Mayora","place":["M\u00e1laga, Spain"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Eva","family":"Dom\u00ednguez","sequence":"additional","affiliation":[{"name":"Instituto de Hortofruticultura Subtropical y Mediterr\u00e1nea \u201cLa Mayora\u201d, Universidad de M\u00e1laga-Consejo Superior de Investigaciones Cient\u00edficas, Departamento de Mejora Gen\u00e9tica y Biotecnolog\u00eda, Estaci\u00f3n Experimental La Mayora","place":["M\u00e1laga, Spain"]}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1965","published-online":{"date-parts":[[2026,8,3]]},"reference":[{"key":"B1","doi-asserted-by":"publisher","DOI":"10.1371\/journal.pgen.1000777","article-title":"Fruit-surface flavonoid accumulation in tomato is controlled by a SlMYB12-regulated transcriptional network","volume":"5","author":"Adato","year":"2009","journal-title":"PloS Genet."},{"key":"B2","doi-asserted-by":"publisher","DOI":"10.3389\/fpls.2015.00889","article-title":"Insights into molecular and metabolic events associated with fruit response to post-harvest fungal pathogens","volume":"6","author":"Alkan","year":"2015","journal-title":"Front. Plant Sci."},{"key":"B3","doi-asserted-by":"publisher","first-page":"71","DOI":"10.1104\/pp.109.147322","article-title":"Biochemical and molecular analysis of pink tomatoes: deregulated expression of the gene encoding transcription factor SlMYB12 leads to pink tomato fruit color","volume":"152","author":"Ballester","year":"2010","journal-title":"Plant Physiol."},{"key":"B4","doi-asserted-by":"publisher","first-page":"113","DOI":"10.1038\/s41438-021-00548-5","article-title":"Genome-wide QTL analysis of tomato fruit cuticle deposition and composition","volume":"8","author":"Barraj Barraj","year":"2021","journal-title":"Hortic. Res."},{"key":"B5","doi-asserted-by":"publisher","DOI":"10.3389\/fpls.2016.01172","article-title":"Exploring new alleles involved in tomato fruit quality in an introgression line library of Solanum pimpinellifolium","volume":"7","author":"Barrantes","year":"2016","journal-title":"Front. Plant Sci."},{"key":"B6","doi-asserted-by":"publisher","DOI":"10.3389\/fpls.2021.807723","article-title":"The response of tomato fruit cuticle membranes against heat and light","volume":"12","author":"Ben\u00edtez","year":"2022","journal-title":"Front. Plant Sci."},{"key":"B7","doi-asserted-by":"publisher","DOI":"10.1016\/j.postharvbio.2026.114178","article-title":"Cuticle changes during tomato fruit postharvest: implications of natural variability in biophysical properties","volume":"235","author":"Ben\u00edtez","year":"2026","journal-title":"Postharvest Biol. Technol."},{"key":"B8","doi-asserted-by":"publisher","first-page":"526","DOI":"10.1016\/j.bioteChadv.2014.01.005","article-title":"Transcriptional regulation of cuticle biosynthesis","volume":"32","author":"Borisjuk","year":"2014","journal-title":"Biotechnol. Adv."},{"key":"B9","doi-asserted-by":"publisher","first-page":"1301","DOI":"10.1038\/nbt.1506","article-title":"Enrichment of tomato fruit with health-promoting anthocyanins by expression of select transcription factors","volume":"26","author":"Butelli","year":"2008","journal-title":"Nat. Biotechnol."},{"key":"B10","doi-asserted-by":"publisher","first-page":"620","DOI":"10.1080\/10408390802603441","article-title":"Plant metabolism and the environment: implications for managing phenolics","volume":"50","author":"Cohen","year":"2010","journal-title":"Crit. Rev. Food Sci. Nutr."},{"key":"B11","doi-asserted-by":"publisher","first-page":"231","DOI":"10.1016\/j.pbi.2009.01.006","article-title":"Modeling QTL for complex traits: detection and context for plant breeding","volume":"12","author":"Cooper","year":"2009","journal-title":"Curr. Opin. Plant Biol."},{"key":"B12","doi-asserted-by":"publisher","first-page":"890","DOI":"10.1038\/nbt1108","article-title":"Fruit-specific RNAi-mediated suppression of DET1 enhances carotenoid and flavonoid content in tomatoes","volume":"23","author":"Davuluri","year":"2005","journal-title":"Nat. Biotechnol."},{"key":"B13","doi-asserted-by":"publisher","first-page":"613","DOI":"10.1071\/FP09039","article-title":"Biomechanics of isolated tomato fruit cuticles during ripening: the role of flavonoids","volume":"36","author":"Dom\u00ednguez","year":"2009","journal-title":"Funct. Plant Biol."},{"key":"B14","doi-asserted-by":"publisher","first-page":"2788","DOI":"10.1111\/pbi.14405","article-title":"Epistasis and pleiotropy-induced variation for plant breeding","volume":"22","author":"Dwivedi","year":"2024","journal-title":"Plant Biotechnol. J."},{"key":"B15","doi-asserted-by":"publisher","first-page":"1371","DOI":"10.1104\/pp.114.246405","article-title":"Transient silencing of CHALCONE SYNTHASE during fruit ripening modifies tomato epidermal cells and cuticle","volume":"166","author":"Espa\u00f1a","year":"2014","journal-title":"Plant Physiol."},{"key":"B16","doi-asserted-by":"publisher","first-page":"790","DOI":"10.1111\/nph.12727","article-title":"Biomechanical properties of tomato fruit cuticle during development are modulated by changes in the relative amount of their components","volume":"202","author":"Espa\u00f1a","year":"2014","journal-title":"New Phytol."},{"key":"B17","doi-asserted-by":"publisher","DOI":"10.1186\/1471-2229-8-131","article-title":"Selection of internal control genes for quantitative real-time RT-PCR studies during tomato development process","volume":"8","author":"Exp\u00f3sito-Rodr\u00edguez","year":"2008","journal-title":"BMC Plant Biol."},{"key":"B18","doi-asserted-by":"publisher","first-page":"2703","DOI":"10.1093\/jxb\/erx134","article-title":"Uncovering tomato quantitative trait loci and candidate genes for fruit cuticular lipid composition using the Solanum pennellii introgression line population","volume":"68","author":"Fern\u00e1ndez-Moreno","year":"2017","journal-title":"J. Exp. Bot."},{"key":"B19","doi-asserted-by":"publisher","first-page":"681","DOI":"10.1038\/nrg1426","article-title":"Uncovering cryptic genetic variation","volume":"5","author":"Gibson","year":"2004","journal-title":"Nat. Rev. Genet."},{"key":"B20","doi-asserted-by":"publisher","first-page":"1036","DOI":"10.1104\/pp.15.00469","article-title":"Transcriptional activity of the MADS Box ARLEQUIN\/TOMATO AGAMOUS-LIKE1 gene is required for cuticle development of tomato fruit","volume":"68","author":"Gim\u00e9nez","year":"2015","journal-title":"Plant Physiol."},{"key":"B21","doi-asserted-by":"publisher","first-page":"219","DOI":"10.1093\/plphys\/kiac369","article-title":"3D (x-y-t) Raman imaging of tomato fruit cuticle: microchemistry during development","volume":"191","author":"Gonz\u00e1lez Moreno","year":"2023","journal-title":"Plant Physiol."},{"key":"B22","doi-asserted-by":"publisher","first-page":"1786","DOI":"10.1038\/s41467-022-29460-9","article-title":"Radiationless mechanism of UV deactivation by cuticle phenolics in plants","volume":"13","author":"Gonz\u00e1lez Moreno","year":"2022","journal-title":"Nat. Commun."},{"key":"B23","doi-asserted-by":"publisher","first-page":"202","DOI":"10.1111\/nph.13600","article-title":"Genetic control of cuticular wax compounds in Eucalyptus globulus","volume":"209","author":"Gosney","year":"2016","journal-title":"New Phytol."},{"key":"B24","doi-asserted-by":"publisher","first-page":"421","DOI":"10.1007\/BF02860832","article-title":"Environmental influences on cuticle development and resultant foliar penetration","volume":"41","author":"Hull","year":"1975","journal-title":"Bot. Rev."},{"key":"B25","doi-asserted-by":"publisher","first-page":"1415","DOI":"10.1016\/0031-9422(80)80185-3","article-title":"Phenolic constituents of tomato fruit cuticles","volume":"19","author":"Hunt","year":"1980","journal-title":"Phytochemistry"},{"key":"B26","doi-asserted-by":"publisher","DOI":"10.1016\/j.plaphy.2024.108991","article-title":"Metabolic and gene-expression analyses reveal developmental dynamics of cutin deposition in pomegranate fruit grown under different environmental conditions","volume":"215","author":"Kaplan","year":"2024","journal-title":"Plant Physiol. Biochem."},{"key":"B27","doi-asserted-by":"publisher","first-page":"1219","DOI":"10.1016\/0146-6380(94)90165-1","article-title":"A lignin-like polymer in the cuticle of spruce needles: implications for the humification of spruce litter","volume":"21","author":"K\u00f6gel-Knabner","year":"1994","journal-title":"Org. Geochem."},{"key":"B28","doi-asserted-by":"publisher","first-page":"1671","DOI":"10.1534\/g3.119.400884","article-title":"Genome-wide association study for maize leaf cuticular conductance identifies candidate genes involved in the regulation of cuticle development","volume":"10","author":"Lin","year":"2020","journal-title":"G3: Genes Genomes Genet."},{"key":"B29","doi-asserted-by":"publisher","DOI":"10.1016\/j.foodchem.2025.145837","article-title":"Postharvest storage affects the chemical composition of the avocado fruit cuticle in a cultivar-specific manner","volume":"493","author":"Manasherova","year":"2025","journal-title":"Food Chem."},{"key":"B30","doi-asserted-by":"publisher","first-page":"470","DOI":"10.1038\/88150","article-title":"Overexpression of petunia chalcone isomerase in tomato results in fruit containing increased levels of flavonols","volume":"19","author":"Muir","year":"2001","journal-title":"Nat. Biotechnol."},{"key":"B31","doi-asserted-by":"publisher","first-page":"151","DOI":"10.1111\/tpj.13194","article-title":"Solanum pennellii backcross inbred lines (BILs) link small genomic bins with tomato traits","volume":"87","author":"Ofner","year":"2016","journal-title":"Plant J."},{"key":"B32","doi-asserted-by":"publisher","first-page":"15","DOI":"10.1111\/j.1399-3054.2012.01592.x","article-title":"Fruit cuticle lipid composition and fruit post-harvest water loss in an advanced backcross generation of pepper (Capsicum sp.)","volume":"146","author":"Parsons","year":"2012","journal-title":"Physiol. Plant"},{"key":"B33","doi-asserted-by":"publisher","first-page":"888","DOI":"10.1104\/pp.113.232645","article-title":"Analyses of tomato fruit brightness mutants uncover both cutin-deficient and cutin-abundant mutants and a new hypomorphic allele of GDSL lipase","volume":"164","author":"Petit","year":"2013","journal-title":"Plant Physiol."},{"key":"B34","doi-asserted-by":"publisher","first-page":"445","DOI":"10.1007\/s00122-016-2825-9","article-title":"Genetic and biochemical analysis reveals linked QTLs determining natural variation for fruit post-harvest water loss in pepper (Capsicum)","volume":"130","author":"Popovsky-Sarid","year":"2017","journal-title":"Theor. Appl. Genet."},{"key":"B35","doi-asserted-by":"publisher","first-page":"654","DOI":"10.1104\/pp.111.187187","article-title":"Arabidopsis Deficient in Cutin Ferulate encodes a transferase required for feruloylation of omega-hydroxy fatty acids in cutin polyester","volume":"158","author":"Rautengarten","year":"2012","journal-title":"Plant Physiol."},{"key":"B36","doi-asserted-by":"publisher","DOI":"10.1038\/ncomms14713","article-title":"A phenol-enriched cuticle is ancestral to lignin evolution in land plants","volume":"8","author":"Renault","year":"2017","journal-title":"Nat. Commun."},{"key":"B37","doi-asserted-by":"publisher","DOI":"10.3389\/fpls.2019.01536","article-title":"QTL and transcriptomic analyses implicate cuticle transcription factor SHINE as a source of natural variation for epidermal traits in cucumber fruit","volume":"10","author":"Rett-Cadman","year":"2019","journal-title":"Front. Plant Sci."},{"key":"B38","doi-asserted-by":"publisher","first-page":"1821","DOI":"10.1093\/plphys\/kiac392","article-title":"The cutin polymer matrix undergoes a fine architectural tuning from early tomato fruit development to ripening","volume":"190","author":"Reynoud","year":"2022","journal-title":"Plant Physiol."},{"key":"B39","doi-asserted-by":"publisher","first-page":"21","DOI":"10.1002\/col.20070","article-title":"The CIEDE2000 color-difference formula: implementation notes, supplementary test data, and mathematical observations","volume":"30","author":"Sharma","year":"2005","journal-title":"Color Res. Appl."},{"key":"B40","doi-asserted-by":"publisher","first-page":"11","DOI":"10.1016\/j.plantsci.2013.10.004","article-title":"Dominance and epistasis are the main contributors to heterosis for plant height in rice","author":"Shen","year":"2014","journal-title":"Plant Sci."},{"key":"B41","doi-asserted-by":"publisher","first-page":"1142","DOI":"10.1016\/j.cell.2017.04.032","article-title":"Bypassing negative epistasis on yield in tomato imposed by a domestication gene","volume":"169","author":"Soyk","year":"2017","journal-title":"Cell."},{"key":"B42","doi-asserted-by":"publisher","DOI":"10.1186\/gb-2002-3-7-research0034","article-title":"Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes","volume":"3","author":"Vandesompele","year":"2002","journal-title":"Genome Biol."},{"key":"B43","doi-asserted-by":"publisher","first-page":"1231","DOI":"10.1021\/jf049355i","article-title":"Utilization of the genetic resources of wild species to create a nontransgenic high flavonoid tomato","volume":"53","author":"Willits","year":"2005","journal-title":"J. Agric. Food. Chem."},{"key":"B44","doi-asserted-by":"publisher","DOI":"10.1016\/j.postharvbio.2023.112564","article-title":"1-Methylcyclopropene reduces postharvest water loss by modulating cuticle formation in tomato fruit","volume":"206","author":"Wu","year":"2023","journal-title":"Postharvest Biol. Technol."},{"key":"B45","doi-asserted-by":"publisher","DOI":"10.1016\/j.postharvbio.2021.111771","article-title":"QTL analysis reveals the effect of CER1-1 and CER1-3 to reduce fruit water loss by increasing cuticular wax alkanes in citrus fruit","volume":"185","author":"Yang","year":"2022","journal-title":"Postharvest Biol. Technol."},{"key":"B46","doi-asserted-by":"publisher","first-page":"5","DOI":"10.1104\/pp.113.222737","article-title":"The formation and function of plant cuticles","volume":"163","author":"Yeats","year":"2013","journal-title":"Plant Physiol."},{"key":"B47","doi-asserted-by":"publisher","first-page":"984","DOI":"10.1038\/s41586-025-09243-0","article-title":"Cryptic variation fuels plant phenotypic change through hierarchical epistasis","volume":"64","author":"Zebell","year":"2025","journal-title":"Nature"},{"key":"B48","doi-asserted-by":"publisher","first-page":"97","DOI":"10.1111\/pbr.13224","article-title":"Genetic evidence of recessive epistasis among sex determining silkless1 (sk1) tasselseed1 (ts1) and tasselseed2 (ts2) genes and its utility in maize (Zea mays L.) breeding","volume":"144","author":"Zunjare","year":"2025","journal-title":"Plant Breed."}],"container-title":["Frontiers in Plant Science"],"original-title":[],"link":[{"URL":"https:\/\/www.frontiersin.org\/articles\/10.3389\/fpls.2026.1863369\/full","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2026,8,3]],"date-time":"2026-08-03T05:31:31Z","timestamp":1785735091000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.frontiersin.org\/articles\/10.3389\/fpls.2026.1863369\/full"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2026,8,3]]},"references-count":48,"alternative-id":["10.3389\/fpls.2026.1863369"],"URL":"https:\/\/doi.org\/10.3389\/fpls.2026.1863369","relation":{},"ISSN":["1664-462X"],"issn-type":[{"value":"1664-462X","type":"electronic"}],"subject":[],"published":{"date-parts":[[2026,8,3]]},"article-number":"1863369"}}