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This condition causes low Cu content and modifications in the ripening-associated processes in tomato fruit. This research studies the transcriptomic changes that occur in red ripe tomato fruit grown under suboptimal Cu conditions to shed light on the molecular mechanisms underlying this stress. Comparative RNA-sequencing and functional analyses revealed that Cu deficiency during cultivation activates signals for metal ion transport, cellular redox homeostasis, pyridoxal phosphate binding, and amino acid metabolism while repressing the response to phosphate starvation in harvested fruit. Transcriptomic analyses highlighted a number of novel Cu stress-responsive genes of unknown function and indicated that Cu homeostasis regulation in tomato fruit may involve additional components than those described in model plants. It also studied the regulation of high-affinity Cu transporters and a number of well-known Cu stress-responsive genes during tomato fruit ripening depending on Cu availability, which allowed potential candidates to be targeted for biotechnological improvements in reproductive tissues. We provide the first study characterizing the molecular responses of fruit to Cu deficiency stress for any fruit crop.<\/jats:p>","DOI":"10.3390\/plants12102062","type":"journal-article","created":{"date-parts":[[2023,5,23]],"date-time":"2023-05-23T01:36:48Z","timestamp":1684805808000},"page":"2062","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":5,"title":["Molecular Responses of Red Ripe Tomato Fruit to Copper Deficiency Stress"],"prefix":"10.3390","volume":"12","author":[{"ORCID":"https:\/\/orcid.org\/0000-0002-7811-0897","authenticated-orcid":false,"given":"Paco","family":"Romero","sequence":"first","affiliation":[{"name":"Department of Food Biotechnology, Institute of Agrochemistry and Food Technology (IATA-CSIC), Avenida Catedr\u00e1tico Agust\u00edn Escardino 7, 46980 Paterna, Valencia, Spain"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-6987-1440","authenticated-orcid":false,"given":"Mar\u00eda Teresa","family":"Lafuente","sequence":"additional","affiliation":[{"name":"Department of Food Biotechnology, Institute of Agrochemistry and Food Technology (IATA-CSIC), Avenida Catedr\u00e1tico Agust\u00edn Escardino 7, 46980 Paterna, Valencia, Spain"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2023,5,22]]},"reference":[{"key":"ref_1","unstructured":"Marschner, P. (2012). Marschner\u2019s Mineral Nutrition of Higher Plants, Elsevier."},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"47","DOI":"10.1146\/annurev.arplant.58.032806.103750","article-title":"Nutrient Sensing and Signaling: NPKS","volume":"58","author":"Schachtman","year":"2007","journal-title":"Annu. Rev. Plant Biol."},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"282","DOI":"10.1016\/j.scitotenv.2018.04.268","article-title":"Copper Distribution in European Topsoils: An Assessment Based on LUCAS Soil Survey","volume":"636","author":"Ballabio","year":"2018","journal-title":"Sci. Total. Environ."},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"199","DOI":"10.1016\/0304-4238(78)90001-8","article-title":"Effects of Copper Deficiency and Liming on the Yield, Quality and Copper Status of Tomatoes, Lettuce and Cucumbers Grown in Peat","volume":"9","author":"Adams","year":"1978","journal-title":"Sci. Hortic."},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"371","DOI":"10.1104\/pp.14.2.371","article-title":"The Essentiality of Certain Elements in Minute Quantity for Plants with Special Reference to Copper","volume":"14","author":"Arnon","year":"1939","journal-title":"Plant Physiol."},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"143","DOI":"10.1017\/S0021859600047870","article-title":"Investigations on Copper Deficiency in Plants","volume":"32","author":"Piper","year":"1942","journal-title":"J. Agric. Sci."},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"558","DOI":"10.1002\/j.1537-2197.1943.tb10299.x","article-title":"Copper Deficiency in Tomatoes","volume":"30","author":"Bailey","year":"1943","journal-title":"Am. J. Bot."},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"e03233","DOI":"10.7554\/eLife.03233","article-title":"Plant Quality Declines as CO2 Levels Rise","volume":"3","author":"Weigel","year":"2014","journal-title":"Elife"},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"e02245","DOI":"10.7554\/eLife.02245","article-title":"Hidden Shift of the Ionome of Plants Exposed to Elevated CO2 Depletes Minerals at the Base of Human Nutrition","volume":"3","author":"Loladze","year":"2014","journal-title":"Elife"},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"111537","DOI":"10.1016\/j.plantsci.2022.111537","article-title":"Deficient Copper Availability on Organoleptic and Nutritional Quality of Tomato Fruit","volume":"326","author":"Lafuente","year":"2023","journal-title":"Plant Sci."},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"271","DOI":"10.1111\/j.1365-3040.2007.01642.x","article-title":"Copper and Iron Homeostasis in Arabidopsis: Responses to Metal Deficiencies, Interactions and Biotechnological Applications","volume":"30","author":"Puig","year":"2007","journal-title":"Plant Cell Environ."},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"799","DOI":"10.1111\/j.1469-8137.2009.02846.x","article-title":"Copper Homeostasis","volume":"182","author":"Burkhead","year":"2009","journal-title":"New Phytol."},{"key":"ref_13","first-page":"255","article-title":"Temporal Aspects of Copper Homeostasis and Its Crosstalk with Hormones","volume":"6","author":"Romero","year":"2015","journal-title":"Front. Plant Sci."},{"key":"ref_14","unstructured":"Kamiya, T., Burritt, D.J., Tran, L.-S.P., and Fujiwara, T.B.T.-P.M.U.E. (2018). Plant Micronutrient Use Efficiency: Molecular and Genomic Perspectives in Crop Plants, Academic Press."},{"key":"ref_15","first-page":"216","article-title":"Functions and Homeostasis of Zinc, Copper, and Nickel in Plants","volume":"14","author":"Clemens","year":"2006","journal-title":"Top. Curr. Genet."},{"key":"ref_16","doi-asserted-by":"crossref","unstructured":"Schulten, A., and Kr\u00e4mer, U. (2017). Interactions between Copper Homeostasis and Metabolism in Plants, Springer.","DOI":"10.1007\/124_2017_7"},{"key":"ref_17","doi-asserted-by":"crossref","unstructured":"Sheng, H., Jiang, Y., Ishka, M.R., Chia, J.-C., Dokuchayeva, T., Kavulych, Y., Zavodna, T.-O., Mendoza, P., Huang, R., and Smieshka, L. (2019). YSL3-Mediated Copper Distribution Is Required for Fertility, Grain Yield, and Size in Brachypodium. bioRxiv, 13.","DOI":"10.1101\/2019.12.12.874396"},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"1446","DOI":"10.1104\/pp.106.082586","article-title":"Mutations in Arabidopsis Yellow Stripe-Like1 and Yellow Stripe-Like3 Reveal Their Roles in Metal Ion Homeostasis and Loading of Metal Ions in Seeds","volume":"141","author":"Waters","year":"2006","journal-title":"Plant Physiol."},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"738","DOI":"10.1105\/tpc.111.090431","article-title":"Transcriptome Sequencing Identifies SPL7-Regulated Copper Acquisition Genes FRO4 \/ FRO5 and the Copper Dependence of Iron Homeostasis in Arabidopsis","volume":"24","author":"Bernal","year":"2012","journal-title":"Plant Cell"},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"305","DOI":"10.1111\/j.1469-8137.2011.03869.x","article-title":"Moving Copper in Plants","volume":"192","author":"Pilon","year":"2011","journal-title":"New Phytol."},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"577","DOI":"10.1023\/A:1022345507112","article-title":"Identification of a Copper Transporter Family in Arabidopsis Thaliana","volume":"51","author":"Puig","year":"2003","journal-title":"Plant Mol. Biol."},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1155\/2014\/476917","article-title":"Function and Regulation of the Plant COPT Family of High-Affinity Copper Transport Proteins","volume":"2014","author":"Puig","year":"2014","journal-title":"Adv. Bot."},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"26021","DOI":"10.1074\/jbc.M202547200","article-title":"Biochemical and Genetic Analyses of Yeast and Human High Affinity Copper Transporters Suggest a Conserved Mechanism for Copper Uptake","volume":"277","author":"Puig","year":"2002","journal-title":"J. Biol. Chem."},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"97","DOI":"10.1016\/B978-0-12-394390-3.00004-5","article-title":"Structure and Function of Copper Uptake Transporters","volume":"69","author":"Pope","year":"2012","journal-title":"Curr. Top. Membr."},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"537","DOI":"10.1146\/annurev-biochem-030409-143539","article-title":"Copper Metallochaperones","volume":"79","author":"Robinson","year":"2010","journal-title":"Annu. Rev. Biochem."},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"919","DOI":"10.1089\/ars.2012.5084","article-title":"Copper and Iron Homeostasis in Plants: The Challenges of Oxidative Stress","volume":"19","author":"Ravet","year":"2013","journal-title":"Antioxid Redox Signal."},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"2307","DOI":"10.1016\/j.febslet.2005.03.025","article-title":"AtCCS Is a Functional Homolog of the Yeast Copper Chaperone Ccs1\/Lys7","volume":"579","author":"Burkhead","year":"2005","journal-title":"FEBS Lett."},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"28129","DOI":"10.1074\/jbc.R114.592618","article-title":"Lysosome-Related Organelles as Mediators of Metal Homeostasis","volume":"289","author":"Merchant","year":"2014","journal-title":"J. Biol. Chem."},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"521","DOI":"10.1046\/j.1365-313x.2001.00985.x","article-title":"Evidence for the Plant-Specific Intercellular Transport of the Arabidopsis Copper Chaperone CCH","volume":"25","author":"Mira","year":"2001","journal-title":"Plant J."},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"269","DOI":"10.1016\/j.mito.2014.02.011","article-title":"Mitochondria and Copper Homeostasis in Plants","volume":"19","author":"Garcia","year":"2014","journal-title":"Mitochondrion"},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"1852","DOI":"10.1104\/pp.010963","article-title":"AtCOX17, an Arabidopsis Homolog of the Yeast Copper Chaperone COX17","volume":"129","author":"Balandin","year":"2002","journal-title":"Plant Physiol."},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"343","DOI":"10.1007\/s11103-007-9224-1","article-title":"Characterization of Arabidopsis Thaliana Genes Encoding Functional Homologues of the Yeast Metal Chaperone Cox19p, Involved in Cytochrome c Oxidase Biogenesis","volume":"65","author":"Attallah","year":"2007","journal-title":"Plant Mol. Biol."},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"825","DOI":"10.1016\/S0006-291X(03)00680-6","article-title":"Identification of a Copper Chaperone from Tomato Fruits Infected with Botrytis Cinerea by Differential Display","volume":"304","author":"Company","year":"2003","journal-title":"Biochem. Biophys. Res. Commun."},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"844","DOI":"10.1111\/pce.12020","article-title":"Calcium- and Potassium-Permeable Plasma Membrane Transporters Are Activated by Copper in Arabidopsis Root Tips: Linking Copper Transport with Cytosolic Hydroxyl Radical Production","volume":"36","author":"Poschenrieder","year":"2013","journal-title":"Plant Cell Env."},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"623","DOI":"10.1016\/j.tplants.2014.06.013","article-title":"A Tidal Wave of Signals: Calcium and ROS at the Forefront of Rapid Systemic Signaling","volume":"19","author":"Gilroy","year":"2014","journal-title":"Trends Plant Sci"},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"347","DOI":"10.1105\/tpc.108.060137","article-title":"SQUAMOSA Promoter Binding Protein-Like7 Is a Central Regulator for Copper Homeostasis in Arabidopsis","volume":"21","author":"Yamasaki","year":"2009","journal-title":"Plant Cell"},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"16369","DOI":"10.1074\/jbc.M700138200","article-title":"Regulation of Copper Homeostasis by Micro-RNA in Arabidopsis","volume":"282","author":"Yamasaki","year":"2007","journal-title":"J. Biol. Chem."},{"key":"ref_38","first-page":"1","article-title":"Functional Characterisation of Arabidopsis SPL7 Conserved Protein Domains Suggests Novel Regulatory Mechanisms in the Cu Deficiency Response","volume":"14","author":"Xing","year":"2014","journal-title":"BMC Plant Biol."},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"600","DOI":"10.1016\/j.ijbiomac.2021.10.032","article-title":"Identification and Molecular Characterization of the High-Affinity Copper Transporters Family in Solanum Lycopersicum","volume":"192","author":"Romero","year":"2021","journal-title":"Int. J. Biol. Macromol."},{"key":"ref_40","doi-asserted-by":"crossref","unstructured":"Yuan, M., Li, X., Xiao, J., and Wang, S. (2011). Molecular and Functional Analyses of COPT\/Ctr-Type Copper Transporter-like Gene Family in Rice. BMC Plant Biol., 11.","DOI":"10.1186\/1471-2229-11-69"},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"644","DOI":"10.1016\/j.ijbiomac.2021.03.173","article-title":"Molecular Characterization of the COPT\/Ctr-Type Copper Transporter Family under Heavy Metal Stress in Alfalfa","volume":"181","author":"Wang","year":"2021","journal-title":"Int. J. Biol. Macromol."},{"key":"ref_42","doi-asserted-by":"crossref","unstructured":"Wang, H., Du, H., Li, H., Huang, Y., Ding, J., Liu, C., Wang, N., Lan, H., and Zhang, S. (2018). Identification and Functional Characterization of the ZmCOPT Copper Transporter Family in Maize. PLoS ONE, 13.","DOI":"10.1371\/journal.pone.0199081"},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"91","DOI":"10.1007\/s00425-014-2067-5","article-title":"Copper Homeostasis in Grapevine: Functional Characterization of the Vitis Vinifera Copper Transporter 1","volume":"240","author":"Martins","year":"2014","journal-title":"Planta"},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"236","DOI":"10.3389\/fpls.2014.00236","article-title":"Brachypodium Distachyon as a Model System for Studies of Copper Transport in Cereal Crops","volume":"5","author":"Jung","year":"2014","journal-title":"Front. Plant Sci."},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"781","DOI":"10.1007\/s00572-020-00987-3","article-title":"MtCOPT2 Is a Cu+ Transporter Specifically Expressed in Medicago Truncatula Mycorrhizal Roots","volume":"30","author":"Senovilla","year":"2020","journal-title":"Mycorrhiza"},{"key":"ref_46","doi-asserted-by":"crossref","unstructured":"Escaray, F.J., Antonelli, C.J., Copello, G.J., Puig, S., Pe\u00f1arrubia, L., Ruiz, O.A., and Perea-Garc\u00eda, A. (2019). Characterization of the Copper Transporters from Lotus Spp. and Their Involvement under Flooding Conditions. Int. J. Mol. Sci., 20.","DOI":"10.3390\/ijms20133136"},{"key":"ref_47","doi-asserted-by":"crossref","first-page":"e2208331119","DOI":"10.1073\/pnas.2208331119","article-title":"Plant Movement and LAC of It: How Copper Facilitates Explosive Seed Dispersal","volume":"119","author":"Vatamaniuk","year":"2022","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_48","doi-asserted-by":"crossref","first-page":"e00288","DOI":"10.1002\/pld3.288","article-title":"Copper Deficiency Alters Shoot Architecture and Reduces Fertility of Both Gynoecium and Androecium in Arabidopsis Thaliana","volume":"4","author":"Vatamaniuk","year":"2020","journal-title":"Plant Direct"},{"key":"ref_49","doi-asserted-by":"crossref","first-page":"3012","DOI":"10.1105\/tpc.17.00363","article-title":"Arabidopsis Pollen Fertility Requires the Transcription Factors CITF1 and SPL7 That Regulate Copper Delivery to Anthers and Jasmonic Acid Synthesis","volume":"29","author":"Yan","year":"2017","journal-title":"Plant Cell"},{"key":"ref_50","doi-asserted-by":"crossref","first-page":"170","DOI":"10.1104\/pp.110.153676","article-title":"Deregulated Copper Transport Affects Arabidopsis Development Especially in the Absence of Environmental Cycles","volume":"153","author":"Puig","year":"2010","journal-title":"Plant Physiol."},{"key":"ref_51","doi-asserted-by":"crossref","first-page":"15348","DOI":"10.1074\/jbc.M313321200","article-title":"The Arabidopsis Copper Transporter COPT1 Functions in Root Elongation and Pollen Development","volume":"279","author":"Puig","year":"2004","journal-title":"J. Biol. Chem."},{"key":"ref_52","doi-asserted-by":"crossref","first-page":"29","DOI":"10.1007\/s00775-009-0591-8","article-title":"Regulation of Copper Transport in Arabidopsis Thaliana: A Biochemical Oscillator?","volume":"15","author":"Moreno","year":"2010","journal-title":"J. Biol. Inorg. Chem."},{"key":"ref_53","doi-asserted-by":"crossref","unstructured":"Ishka, M.R., Chia, J.C., and Vatamaniuk, O.K. (2022). Advances in Understanding of Copper Function and Transport in Plants. Cation Transp. Plants, 205\u2013226.","DOI":"10.1016\/B978-0-323-85790-1.00021-X"},{"key":"ref_54","unstructured":"Kamiya, T., Burritt, D.J., Tran, L.-S.P., and Fujiwara, T.B.T.-P.M.U.E. (2018). Chapter 1-Regulation of Micronutrient Homeostasis and Deficiency Response in Plants A2-Hossain, Mohammad Anwar, Academic Press."},{"key":"ref_55","doi-asserted-by":"crossref","first-page":"180","DOI":"10.1104\/pp.112.212407","article-title":"Arabidopsis Copper Transport Protein COPT2 Participates in the Cross Talk between Iron Deficiency Responses and Low-Phosphate Signaling","volume":"162","author":"Puig","year":"2013","journal-title":"Plant Physiol."},{"key":"ref_56","doi-asserted-by":"crossref","first-page":"409","DOI":"10.1071\/FP08288","article-title":"Copper in Plants: Acquisition, Transport and Interactions","volume":"36","author":"Yruela","year":"2009","journal-title":"Funct. Plant Biol."},{"key":"ref_57","doi-asserted-by":"crossref","first-page":"114501","DOI":"10.1016\/j.ecoenv.2023.114501","article-title":"Effect of Potassium Intake on Cadmium Transporters and Root Cell Wall Biosynthesis in Sweet Potato","volume":"250","author":"Huang","year":"2023","journal-title":"Ecotoxicol. Environ. Saf."},{"key":"ref_58","doi-asserted-by":"crossref","first-page":"148","DOI":"10.1104\/pp.105.076232","article-title":"Zinc-Dependent Global Transcriptional Control, Transcriptional Deregulation, and Higher Gene Copy Number for Genes in Metal Homeostasis of the Hyperaccumulator Arabidopsis Halleri","volume":"142","author":"Talke","year":"2006","journal-title":"Plant Physiol."},{"key":"ref_59","doi-asserted-by":"crossref","first-page":"589","DOI":"10.1016\/j.bbamcr.2007.10.017","article-title":"Glutaredoxins and Thioredoxins in Plants","volume":"1783","author":"Meyer","year":"2008","journal-title":"Biochim. Biophys. Acta (BBA)-Mol. Cell Res."},{"key":"ref_60","doi-asserted-by":"crossref","unstructured":"Chen, G., Li, J., Han, H., Du, R., and Wang, X. (2022). Physiological and Molecular Mechanisms of Plant Responses to Copper Stress. Int. J. Mol. Sci., 23.","DOI":"10.3390\/ijms232112950"},{"key":"ref_61","doi-asserted-by":"crossref","unstructured":"Srivastava, S., Srivastava, A.K., and Suprasanna, P. (2019). Plant-Metal Interactions, Springer.","DOI":"10.1007\/978-3-030-20732-8"},{"key":"ref_62","first-page":"407","article-title":"Interaction of Copper, Zinc, and Their Importance in Plant Physiology: Review, Acquisition and Transport","volume":"10","author":"Yassen","year":"2020","journal-title":"Middle East J. Appl. Sci."},{"key":"ref_63","doi-asserted-by":"crossref","first-page":"839","DOI":"10.1080\/01904160802043148","article-title":"Interaction of Iron with Copper, Zinc, and Manganese in Wheat as Affected by Iron and Manganese in a Calcareous Soil","volume":"31","author":"Ronaghi","year":"2008","journal-title":"J. Plant Nutr."},{"key":"ref_64","doi-asserted-by":"crossref","unstructured":"Gayomba, S.R., Zhai, Z., Jung, H.-I., and Vatamaniuk, O.K. (2015). Local and Systemic Signaling of Iron Status and Its Interactions with Homeostasis of Other Essential Elements. Front. Plant Sci., 6.","DOI":"10.3389\/fpls.2015.00716"},{"key":"ref_65","doi-asserted-by":"crossref","first-page":"285","DOI":"10.1093\/jxb\/erh009","article-title":"The Transcriptional Control of Plant Responses to Phosphate Limitation","volume":"55","author":"Bustos","year":"2004","journal-title":"J. Exp. Bot."},{"key":"ref_66","doi-asserted-by":"crossref","first-page":"965","DOI":"10.1111\/j.1365-313X.2008.03460.x","article-title":"Characterization of a Sub-Family of Arabidopsis Genes with the SPX Domain Reveals Their Diverse Functions in Plant Tolerance to Phosphorus Starvation","volume":"54","author":"Duan","year":"2008","journal-title":"Plant J."},{"key":"ref_67","doi-asserted-by":"crossref","first-page":"1714","DOI":"10.1093\/pcp\/pcy148","article-title":"Sensing and Signaling of Phosphate Starvation\u2013from Local to Long Distance","volume":"59","author":"Chien","year":"2018","journal-title":"Plant Cell Physiol."},{"key":"ref_68","doi-asserted-by":"crossref","first-page":"170231","DOI":"10.1098\/rsob.170231","article-title":"Evolution of the SPX Gene Family in Plants and Its Role in the Response Mechanism to Phosphorus Stress","volume":"8","author":"Liu","year":"2018","journal-title":"Open Biol."},{"key":"ref_69","doi-asserted-by":"crossref","first-page":"383","DOI":"10.1146\/annurev.biochem.73.011303.074021","article-title":"Pyridoxal Phosphate Enzymes: Mechanistic, Structural, and Evolutionary Considerations","volume":"73","author":"Eliot","year":"2004","journal-title":"Annu. Rev. Biochem."},{"key":"ref_70","doi-asserted-by":"crossref","first-page":"1617","DOI":"10.1104\/pp.112.4.1617","article-title":"Overexpression of L-Phenylalanine Ammonia-Lyase in Transgenic Tobacco Plants Reveals Control Points for Flux into Phenylpropanoid Biosynthesis","volume":"112","author":"Howles","year":"1996","journal-title":"Plant Physiol."},{"key":"ref_71","doi-asserted-by":"crossref","first-page":"300","DOI":"10.1016\/j.foodchem.2019.05.118","article-title":"A Relationship between Tomato Fruit Softening, Cuticle Properties and Water Availability","volume":"295","author":"Romero","year":"2019","journal-title":"Food Chem."},{"key":"ref_72","doi-asserted-by":"crossref","first-page":"130946","DOI":"10.1016\/j.foodchem.2021.130946","article-title":"Relative Humidity Regimes Modify Epicuticular Wax Metabolism and Fruit Properties during Navelate Orange Conservation in an ABA-Dependent Manner","volume":"369","author":"Romero","year":"2022","journal-title":"Food Chem."},{"key":"ref_73","doi-asserted-by":"crossref","first-page":"111295","DOI":"10.1016\/j.postharvbio.2020.111295","article-title":"Involvement of Phospholipases and Sucrose in Carbon Starvation-Induced Non-Chilling Peel Pitting in Citrus Fruit","volume":"169","author":"Romero","year":"2020","journal-title":"Postharvest Biol. Technol."},{"key":"ref_74","doi-asserted-by":"crossref","first-page":"1384","DOI":"10.1104\/pp.17.00387","article-title":"Cuticle Biosynthesis in Tomato Leaves Is Developmentally Regulated by Abscisic Acid","volume":"174","author":"Martin","year":"2017","journal-title":"Plant Physiol."},{"key":"ref_75","doi-asserted-by":"crossref","first-page":"1914","DOI":"10.3389\/fpls.2020.594184","article-title":"Abscisic Acid Deficiency Alters Epicuticular Wax Metabolism and Morphology That Leads to Increased Cuticle Permeability During Sweet Orange (Citrus sinensis) Fruit Ripening","volume":"11","author":"Romero","year":"2020","journal-title":"Front. Plant Sci."},{"key":"ref_76","doi-asserted-by":"crossref","first-page":"R36","DOI":"10.1186\/gb-2013-14-4-r36","article-title":"TopHat2: Accurate Alignment of Transcriptomes in the Presence of Insertions, Deletions and Gene Fusions","volume":"14","author":"Kim","year":"2013","journal-title":"Genome Biol."},{"key":"ref_77","doi-asserted-by":"crossref","first-page":"R80","DOI":"10.1186\/gb-2004-5-10-r80","article-title":"Bioconductor: Open Software Development for Computational Biology and Bioinformatics","volume":"5","author":"Gentleman","year":"2004","journal-title":"Genome Biol."},{"key":"ref_78","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":"ref_79","unstructured":"R Core Team, R. (2018). A Language and Environment for Statistical Computing, R Foundation for Statistical Computing. Available online: https:\/\/www.R-project.org."},{"key":"ref_80","doi-asserted-by":"crossref","first-page":"289","DOI":"10.1111\/j.2517-6161.1995.tb02031.x","article-title":"Controlling the False Discovery Rate: A Practical and Powerful Approach to Multiple Testing","volume":"57","author":"Benjamini","year":"1995","journal-title":"J. R. Stat. Soc. Ser. B (Methodol.)"},{"key":"ref_81","doi-asserted-by":"crossref","first-page":"1600","DOI":"10.1093\/bioinformatics\/btl140","article-title":"Improved Scoring of Functional Groups from Gene Expression Data by Decorrelating GO Graph Structure","volume":"22","author":"Alexa","year":"2006","journal-title":"Bioinformatics"}],"container-title":["Plants"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2223-7747\/12\/10\/2062\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,10]],"date-time":"2025-10-10T19:40:15Z","timestamp":1760125215000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2223-7747\/12\/10\/2062"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2023,5,22]]},"references-count":81,"journal-issue":{"issue":"10","published-online":{"date-parts":[[2023,5]]}},"alternative-id":["plants12102062"],"URL":"https:\/\/doi.org\/10.3390\/plants12102062","relation":{},"ISSN":["2223-7747"],"issn-type":[{"value":"2223-7747","type":"electronic"}],"subject":[],"published":{"date-parts":[[2023,5,22]]}}}