{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,7,14]],"date-time":"2026-07-14T15:38:21Z","timestamp":1784043501307,"version":"3.55.0"},"reference-count":98,"publisher":"MDPI AG","issue":"22","license":[{"start":{"date-parts":[[2025,11,13]],"date-time":"2025-11-13T00:00:00Z","timestamp":1762992000000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"name":"Polish Ministry of Agriculture and Rural Development"}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["IJMS"],"abstract":"<jats:p>Transcriptomic analysis of fruit flesh of the cultivars \u2018Trinity\u2019 (red-fleshed) and \u2018Free Redstar\u2019 (white-fleshed) uncovered a set of ten genes involved in different metabolic pathways. Three\u2014N3Dioxy, LAR1 and F3Mo\u2014were mapped via phenylpropanoid and flavonoid biosynthesis (mdm00940, mdm00941); four\u2014AlcFARed, CER1, Cyp86A4 and PalmTransf\u2014were mapped on the cutin, suberine and wax biosynthesis pathways (mdm00073); and three\u2014TropRed, CyP865B1 and CytP450\u2014were mapped via the tropane\/piperidine\/pyridine alkaloid biosynthesis pathway and the peroxisome pathway (KEGG:mdm00960, KEGG:mdm04146). Our study highlighted the higher activity of AlcFARed, CER1, PalmTransf and CYP86A4 in red-fleshed apple fruits and allowed us to discover a specific relationship between significant reductions in fruit wax coating and anthocyanin enrichment in fruit flesh. In addition, the uncovered inhibition of the TropRed gene and the activation of both Cyp865B1 and CYP86A4 suggests that both compounds generate primary alcohols and alkanes, ultimately bound to wax formation. Our results postulate that the fatty acid degradation process is initiated in the flesh of apple fruits and depends on the relationship between anthocyanin content and lipid and wax metabolism. These findings further our understanding of the molecular mechanism linking anthocyanin and wax, making it significantly important in the context of apple fruit storage stability.<\/jats:p>","DOI":"10.3390\/ijms262210987","type":"journal-article","created":{"date-parts":[[2025,11,13]],"date-time":"2025-11-13T09:59:09Z","timestamp":1763027949000},"page":"10987","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":1,"title":["Molecular Interaction of Genes Related to Anthocyanin, Lipid and Wax Biosynthesis in Apple Red-Fleshed Fruits"],"prefix":"10.3390","volume":"26","author":[{"ORCID":"https:\/\/orcid.org\/0000-0002-3473-9706","authenticated-orcid":false,"given":"Sylwia El\u017cbieta","family":"Keller-Przyby\u0142kowicz","sequence":"first","affiliation":[{"name":"Department of Horticultural Crop Breeding, The National Institute of Horticultural Research, Konstytucji 3 Maja 1\/3, 96-100 Skierniewice, Poland"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-0696-3505","authenticated-orcid":false,"given":"Micha\u0142","family":"Oskiera","sequence":"additional","affiliation":[{"name":"Department of Microbiology and Rhizosphere, The National Institute of Horticultural Research, Konstytucji 3-go Maja 1\/3, 96-100 Skierniewice, Poland"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0009-0001-1011-5616","authenticated-orcid":false,"given":"Agnieszka","family":"Walencik","sequence":"additional","affiliation":[{"name":"Department of Horticultural Crop Breeding, The National Institute of Horticultural Research, Konstytucji 3 Maja 1\/3, 96-100 Skierniewice, Poland"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-4852-5514","authenticated-orcid":false,"given":"Mariusz","family":"Lewandowski","sequence":"additional","affiliation":[{"name":"Department of Horticultural Crop Breeding, The National Institute of Horticultural Research, Konstytucji 3 Maja 1\/3, 96-100 Skierniewice, Poland"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2025,11,13]]},"reference":[{"key":"ref_1","unstructured":"(2025, November 03). Available online: https:\/\/www.fao.org\/faostat\/en\/#search\/apple%20fruits."},{"key":"ref_2","doi-asserted-by":"crossref","unstructured":"Keller-Przybylkowicz, S., Oskiera, M., Liu, X., Song, L., Zhao, L., Du, X., Kruczynska, D., Walencik, A., Kowara, N., and Bartoszewski, G. (2024). Transcriptome Analysis of White- and Red-Fleshed Apple Fruits Uncovered Novel Genes Related to the Regulation of Anthocyanin Biosynthesis. Int. J. Mol. Sci., 25.","DOI":"10.3390\/ijms25031778"},{"key":"ref_3","doi-asserted-by":"crossref","unstructured":"Chagn\u00e9, D., Carlisle, C.M., Blond, C., Volz, R.K., Whitworth, C.J., Oraguzie, N.C., Crowhurst, R.N., Allan, A.C., Espley, R.V., and Hellens, R.P. (2007). Mapping a candidate gene (MdMYB10) for red flesh and foliage colour in apple. BMC Genom., 8.","DOI":"10.1186\/1471-2164-8-212"},{"key":"ref_4","doi-asserted-by":"crossref","unstructured":"Chagn\u00e9, D., Krieger, C., Rassam, M., Sullivan, M., Fraser, J., Andr\u00e9, C., Pindo, M., Troggio, M., Gardiner, S.E., and Henry, R.A. (2012). QTL and candidate gene mapping for polyphenolic composition in apple fruit. BMC Plant Biol., 12.","DOI":"10.1186\/1471-2229-12-12"},{"key":"ref_5","first-page":"304","article-title":"Red flesh breeding in apple: Progress and challenges","volume":"814","author":"Volz","year":"2009","journal-title":"Acta Hortic."},{"key":"ref_6","unstructured":"(2025, September 20). Available online: https:\/\/suttonelms.org.uk\/apple43.html."},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"276","DOI":"10.1111\/tpj.13487","article-title":"MYB12 and MYB22 play essential roles in proanthocyanidin and flavonol synthesis in red-fleshed apple (Malus sieversii f. niedzwetzkyana)","volume":"90","author":"Wang","year":"2017","journal-title":"Plant J."},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"305","DOI":"10.2503\/hortj.OKD-R01","article-title":"Anthocyanin Biosynthesis in Apple Fruit","volume":"87","author":"Honda","year":"2018","journal-title":"Hortic. J."},{"key":"ref_9","first-page":"2554","article-title":"Plant secondary metabolism and its response to environment","volume":"6","author":"Yan","year":"2007","journal-title":"Acta Ecol. Sin."},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"414","DOI":"10.1111\/j.1365-313X.2006.02964.x","article-title":"Red coloration in apple fruit is due to the activity of the MYB transcription factor, MdMYB10","volume":"49","author":"Espley","year":"2007","journal-title":"Plant J."},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"187","DOI":"10.1016\/j.molp.2020.01.008","article-title":"Crop Phenomics and High-Throughput Phenotyping: Past Decades, Current Challenges, and Future Perspectives","volume":"13","author":"Yang","year":"2020","journal-title":"Mol. Plant"},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"267","DOI":"10.1016\/j.plaphy.2021.02.033","article-title":"Research progress of fruit color development in apple (Malus domestica Borkh.)","volume":"162","author":"Chen","year":"2021","journal-title":"Plant Physiol. Biochem."},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"18440","DOI":"10.4238\/2015.December.23.32","article-title":"Selection of reference genes for expression analyses of red-fleshed sweet orange (Citrus sinensis)","volume":"14","author":"Pinheiro","year":"2015","journal-title":"Genet. Mol. Res."},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"141","DOI":"10.2503\/hortj.MI-077","article-title":"Effects of Developmental Stages, Light, and an Auxin Polar Transport Inhibitor on the Skin and Flesh Pigmentation of Red-fleshed Peach Fruit","volume":"85","author":"Rumainum","year":"2016","journal-title":"Hortic. J."},{"key":"ref_15","unstructured":"Brooks, R.M., and Olmo, H.P. (1997). The Brooks and Olmo Register of Fruit & Nut Varieties, ASHS Press. [3rd ed.]."},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"527","DOI":"10.1515\/znc-2006-7-810","article-title":"Anthocyanins, colour and antioxidant properties of eggplant (Solanum melongena L.) and violet pepper (Capsicum annuum L.) peel extracts","volume":"6","author":"Sadilova","year":"2006","journal-title":"Naturforsch. C J. Biosci."},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"534","DOI":"10.21273\/HORTSCI.45.4.534","article-title":"Efficient Breeding System for Red-fleshed Apple Based on Linkage with S3-RNase Allele in \u2018Pink Pearl\u2019","volume":"45","author":"Sekido","year":"2010","journal-title":"HortScience"},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"39","DOI":"10.1111\/tpj.14013","article-title":"The proanthocyanidin-specific transcription factor MdMYBPA1 initiates anthocyanin synthesis under low-temperature conditions in red-fleshed apples","volume":"96","author":"Wang","year":"2018","journal-title":"Plant J."},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"7076","DOI":"10.1021\/acs.jafc.8b01273","article-title":"Transcriptomic Analysis of Red-Fleshed Apples Reveals the Novel Role of MdWRKY11 in Flavonoid and Anthocyanin Biosynthesis","volume":"66","author":"Wang","year":"2018","journal-title":"J. Agric. Food Chem."},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"70","DOI":"10.1038\/s41438-018-0084-4","article-title":"Malus sieversii: The origin, flavonoid synthesis mechanism, and breeding of red-skinned and red-fleshed apples","volume":"5","author":"Wang","year":"2018","journal-title":"Hortic. Res."},{"key":"ref_21","doi-asserted-by":"crossref","unstructured":"Korban, S.S. (2021). Genetics and genomics of fruit color development in apple. The Apple Genome, Springer International Publishing.","DOI":"10.1007\/978-3-030-74682-7"},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"uhaf135","DOI":"10.1093\/hr\/uhaf135","article-title":"Recent advances in biosynthesis and regulation of strawberry anthocyanins","volume":"12","author":"Duan","year":"2025","journal-title":"Hortic. Res."},{"key":"ref_23","doi-asserted-by":"crossref","unstructured":"Sun, P., Yang, C., Zhu, W., Wu, J., Lin, X., Wang, Y., Zhu, J., Chen, C., Zhou, K., and Qian, M. (2023). Metabolome, Plant Hormone, and Transcriptome Analyses Reveal the Mechanism of Spatial Accumulation Pattern of Anthocyanins in Peach Flesh. Foods, 12.","DOI":"10.3390\/foods12122297"},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"1718","DOI":"10.1093\/plphys\/kiad160","article-title":"Colorful hues: Insight into the mechanisms of anthocyanin pigmentation in fruit","volume":"192","author":"Zhao","year":"2023","journal-title":"Plant Physiol."},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"1019979","DOI":"10.1080\/15592324.2015.1019979","article-title":"CHS silencing suggests a negative cross-talk between wax and flavonoid pathways in tomato fruit cuticle","volume":"10","year":"2015","journal-title":"Plant Signal. Behav."},{"key":"ref_26","doi-asserted-by":"crossref","unstructured":"Hu, Y., \u0160marda, P., Liu, G., Wang, B., Gao, X., and Guo, Q. (2022). High-Depth Transcriptome Reveals Differences in Natural Haploid Ginkgo biloba L. Due to the Effect of Reduced Gene Dosage. Int. J. Mol. Sci., 23.","DOI":"10.3390\/ijms23168958"},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"955","DOI":"10.1016\/S0981-9428(02)01454-7","article-title":"Anthocyanin biosynthetic genes are coordinately expressed during red coloration in apple skin","volume":"40","author":"Honda","year":"2002","journal-title":"Plant Physiol. Biochem."},{"key":"ref_28","doi-asserted-by":"crossref","unstructured":"Bouillon, P., Belin, E., Fanciullino, A.L., Balzergue, S., Hanteville, S., Letekoma, Y., Cournol, M., Faris, F., Bouanich, A., and Br\u00e9ard, D. (2025). Fade into you: Genetic control of pigmentation patterns in red-flesh apple (Malus domestica). Front. Plant Sci., 15.","DOI":"10.3389\/fpls.2024.1462545"},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"11263","DOI":"10.1007\/s11033-012-2036-7","article-title":"Flower color diversity revealed by differential expression of flavonoid biosynthetic genes and flavonoid accumulation in herbaceous peony (Paeonia lactiflora Pall.)","volume":"39","author":"Zhao","year":"2012","journal-title":"Mol. Biol. Rep."},{"key":"ref_30","doi-asserted-by":"crossref","unstructured":"Zhang, T., Li, B., Wang, Z., Hu, D., Zhang, X., Zhao, B., and Wang, J. (2023). Green biosynthesis of rare DHA-phospholipids by lipase-catalyzed transesterification with edible algal oil in solvent-free system and catalytic mechanism study. Front. Bioeng. Biotechnol., 11.","DOI":"10.3389\/fbioe.2023.1158348"},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"408","DOI":"10.1111\/pbi.12017","article-title":"Analysis of genetically modified red-fleshed apples reveals effects on growth and consumer attributes","volume":"11","author":"Espley","year":"2013","journal-title":"Plant Biotechnol. J."},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"354","DOI":"10.1111\/ppl.12043","article-title":"The role of anthocyanin in photoprotection and its relationship with the xanthophyll cycle and the antioxidant system in apple peel depends on the light conditions","volume":"149","author":"Chen","year":"2013","journal-title":"Physiol. Plant."},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"48205","DOI":"10.1074\/jbc.M407845200","article-title":"Different mechanisms participate in the R-dependent activity of the R2R3 MYB transcription factor C1","volume":"279","author":"Hernandez","year":"2004","journal-title":"J. Biol. Chem."},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"366","DOI":"10.1111\/j.1365-313X.2004.02138.x","article-title":"TT2, TT8, and TTG1 synergistically specify the expression of BANYULS and proanthocyanidin biosynthesis in Arabidopsis thaliana","volume":"39","author":"Baudry","year":"2004","journal-title":"Plant J."},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"63","DOI":"10.1016\/j.tplants.2004.12.011","article-title":"MYB-bHLH-WD40 protein complex and the evolution of cellular diversity","volume":"10","author":"Ramsay","year":"2005","journal-title":"Trends Plant Sci."},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"259","DOI":"10.1023\/A:1024018729349","article-title":"Enhancing anthocyanin production by altering competition for substrate between flavonol synthase and dihydroflavonol 4-reductase","volume":"131","author":"Davies","year":"2003","journal-title":"Euphytica"},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"218","DOI":"10.1016\/S1369-5266(02)00256-X","article-title":"Biosynthesis of flavonoids and effects of stress","volume":"5","year":"2002","journal-title":"Curr. Opin. Plant Biol."},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"1216","DOI":"10.1104\/pp.106.088104","article-title":"Light-induced expression of a MYB gene regulates anthocyanin biosynthesis in red apples","volume":"142","author":"Takos","year":"2006","journal-title":"Plant Physiol."},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"49","DOI":"10.1146\/annurev.arplant.51.1.49","article-title":"Sugar-induced signal transduction in plants","volume":"51","author":"Smeekens","year":"2000","journal-title":"Annu. Rev. Plant Physiol. Plant Mol. Biol."},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"154471","DOI":"10.1016\/j.jplph.2025.154471","article-title":"Sugar sensors in plants: Orchestrators of growth, stress tolerance, and hormonal crosstalk","volume":"307","author":"Supriya","year":"2025","journal-title":"J. Plant Physiol."},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"173","DOI":"10.1146\/annurev.ge.25.120191.001133","article-title":"Genetic and developmental control of anthocyanin biosynthesis","volume":"25","author":"Dooner","year":"1991","journal-title":"Annu. Rev. Genet."},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"1071","DOI":"10.2307\/3870058","article-title":"Genetics and Biochemistry of Anthocyanin Biosynthesis","volume":"7","author":"Holton","year":"1995","journal-title":"Plant Cell"},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"380","DOI":"10.1016\/S1360-1385(00)01720-9","article-title":"Glycosyltransferases in plant natural product synthesis: Characterization of a supergene family","volume":"5","author":"Vogt","year":"2000","journal-title":"Trends Plant Sci."},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"1221","DOI":"10.1093\/jxb\/erh143","article-title":"Responses of primary and secondary metabolism to sugar accumulation revealed by microarray expression analysis of the Arabidopsis mutant, pho3","volume":"55","author":"Lloyd","year":"2004","journal-title":"J. Exp. Bot."},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"1840","DOI":"10.1104\/pp.105.066688","article-title":"Sucrose-specific induction of anthocyanin biosynthesis in Arabidopsis requires the MYB75\/PAP1 gene","volume":"139","author":"Teng","year":"2005","journal-title":"Plant Physiol."},{"key":"ref_46","doi-asserted-by":"crossref","first-page":"637","DOI":"10.1104\/pp.105.072579","article-title":"Sucrose-specific induction of the anthocyanin biosynthetic pathway in Arabidopsis","volume":"140","author":"Solfanelli","year":"2006","journal-title":"Plant Physiol."},{"key":"ref_47","doi-asserted-by":"crossref","first-page":"638","DOI":"10.1111\/tpj.12153","article-title":"Light and the E3 ubiquitin ligase COP1\/SPA control the protein stability of the MYB transcription factors PAP1 and PAP2 involved in anthocyanin accumulation in Arabidopsis","volume":"74","author":"Maier","year":"2013","journal-title":"Plant J."},{"key":"ref_48","doi-asserted-by":"crossref","first-page":"92","DOI":"10.1104\/pp.108.118992","article-title":"Arabidopsis sucrose transporter AtSUC1 is important for pollen germination and sucrose-induced anthocyanin accumulation","volume":"147","author":"Sivitz","year":"2008","journal-title":"Plant Physiol."},{"key":"ref_49","doi-asserted-by":"crossref","unstructured":"Hu, D.G., Sun, C.H., Zhang, Q.Y., An, J.P., You, C.X., and Hao, Y.J. (2016). Glucose Sensor MdHXK1 Phosphorylates and Stabilizes MdbHLH3 to Promote Anthocyanin Biosynthesis in Apple. PLoS Genet., 12.","DOI":"10.1371\/journal.pgen.1006273"},{"key":"ref_50","first-page":"59","article-title":"Cloudy red-fleshed apple juice production and quality","volume":"30","author":"Buczek","year":"2015","journal-title":"Pol. J. Nat. Sci."},{"key":"ref_51","doi-asserted-by":"crossref","first-page":"431","DOI":"10.3389\/fpls.2019.00431","article-title":"Developmental and Environmental Regulation of Cuticular Wax Biosynthesis in Fleshy","volume":"10","author":"Trivedi","year":"2019","journal-title":"Fruits Front. Plant Sci."},{"key":"ref_52","doi-asserted-by":"crossref","unstructured":"Arrieta-Baez, D., Perea-Flores, M.J., M\u00e9ndez-M\u00e9ndez, J., Mendoza, H., and G\u00f3mez-Pati\u00f1o, M. (2020). Structural Studies of the Cutin from Two Apple Varieties: Golden Delicious and Red Delicious (Malus domestica). Molecules, 25.","DOI":"10.3390\/molecules25245955"},{"key":"ref_53","doi-asserted-by":"crossref","first-page":"182","DOI":"10.1105\/tpc.104.026211","article-title":"Reverse Genetic Characterization of Cytosolic Acetyl-CoA Generation by ATP-Citrate Lyase in Arabidopsis","volume":"17","author":"Fatland","year":"2005","journal-title":"Plant Cell"},{"key":"ref_54","doi-asserted-by":"crossref","first-page":"34040","DOI":"10.1074\/jbc.M606266200","article-title":"Mitochondrial metabolism in developing embryos of Brassica napus","volume":"281","author":"Schwender","year":"2006","journal-title":"J. Biol. Chem."},{"key":"ref_55","doi-asserted-by":"crossref","first-page":"462","DOI":"10.1016\/j.tplants.2010.05.006","article-title":"Not just a circle: Flux modes in the plant TCA cycle","volume":"15","author":"Sweetlove","year":"2010","journal-title":"Trends Plant Sci."},{"key":"ref_56","doi-asserted-by":"crossref","first-page":"475","DOI":"10.1007\/s12013-013-9750-1","article-title":"Citric Acid Cycle and Role of its Intermediates in Metabolism","volume":"68","author":"Akram","year":"2014","journal-title":"Cell Biochem. Biophys."},{"key":"ref_57","doi-asserted-by":"crossref","first-page":"1199","DOI":"10.1111\/jipb.12690","article-title":"On the role of the tricarboxylic acid cycle in plant productivity","volume":"60","author":"Zhang","year":"2018","journal-title":"J. Integr. Plant Biol."},{"key":"ref_58","doi-asserted-by":"crossref","unstructured":"Liu, Y., Xu, R., Gu, H., Zhang, E., Qu, J., Cao, W., Huang, X., Yan, H., He, J., and Cai, Z. (2021). Metabolic reprogramming in macrophage responses. Biomark. Res., 9.","DOI":"10.1186\/s40364-020-00251-y"},{"key":"ref_59","doi-asserted-by":"crossref","first-page":"858","DOI":"10.1111\/mpp.12139","article-title":"Cell-wall invertases, key enzymes in the modulation of plant metabolism during defence responses","volume":"15","author":"Proels","year":"2014","journal-title":"Mol. Plant Pathol."},{"key":"ref_60","doi-asserted-by":"crossref","first-page":"11","DOI":"10.1016\/j.phytochem.2017.06.007","article-title":"Postharvest changes in LIN5-down-regulated plants suggest a role for sugar deficiency in cuticle metabolism during ripening","volume":"142","author":"Vallarino","year":"2017","journal-title":"Phytochemistry"},{"key":"ref_61","doi-asserted-by":"crossref","first-page":"112891","DOI":"10.1016\/j.scienta.2024.112891","article-title":"Transcriptome reveals insights into the regulatory mechanism of cuticular wax synthesis in developing apple fruit","volume":"328","author":"Min","year":"2024","journal-title":"Sci. Hortic."},{"key":"ref_62","doi-asserted-by":"crossref","unstructured":"Zhao, Y.-W., Wang, C.-K., Huang, X.-Y., and Hu, D.-G. (2021). Genome-Wide Analysis of the Glutathione S-Transferase (GST) Genes and Functional Identification of MdGSTU12 Reveals the Involvement in the Regulation of Anthocyanin Accumulation in Apple. Genes, 12.","DOI":"10.3390\/genes12111733"},{"key":"ref_63","doi-asserted-by":"crossref","first-page":"1320","DOI":"10.1111\/tpj.15312","article-title":"Two loss-of-function alleles of the glutathione S-transferase (GST) gene cause anthocyanin deficiency in flower and fruit skin of peach (Prunus persica)","volume":"107","author":"Lu","year":"2021","journal-title":"Plant J."},{"key":"ref_64","doi-asserted-by":"crossref","first-page":"112502","DOI":"10.1016\/j.scienta.2023.112502","article-title":"Role of an ATP-binding cassette (ABC) transporter MdABCI17 in the anthocyanin accumulation of apple","volume":"323","author":"Xiang","year":"2024","journal-title":"Sci. Hortic."},{"key":"ref_65","doi-asserted-by":"crossref","unstructured":"Zhang, X., Liu, Y., Ayaz, A., Zhao, H., and L\u00fc, S. (2022). The Plant Fatty Acyl Reductases. Int. J. Mol. Sci., 23.","DOI":"10.3390\/ijms232416156"},{"key":"ref_66","doi-asserted-by":"crossref","unstructured":"Buhrman, K., Aravena-Calvo, J., Ross Zaulich, C., Hinz, K., and Laursen, T. (2022). Anthocyanic Vacuolar Inclusions: From Biosynthesis to Storage and Possible Applications. Front. Chem., 10.","DOI":"10.3389\/fchem.2022.913324"},{"key":"ref_67","doi-asserted-by":"crossref","first-page":"971","DOI":"10.21273\/JASHS.127.6.971","article-title":"Changes in the expression of anthocyanin biosynthetic genes during apple development","volume":"127","author":"Kondo","year":"2002","journal-title":"J. Am. Soc. Hortic. Sci."},{"key":"ref_68","doi-asserted-by":"crossref","first-page":"279","DOI":"10.1104\/pp.105.073262","article-title":"Identification of the flavonoid hydroxylases from grapevine and their regulation during fruit development","volume":"140","author":"Bogs","year":"2006","journal-title":"Plant Physiol."},{"key":"ref_69","doi-asserted-by":"crossref","first-page":"806","DOI":"10.1104\/pp.109.152801","article-title":"Ectopic expression of apple F3\u2032H genes contributes to anthocyanin accumulation in the Arabidopsis tt7 mutant grown under nitrogen stress","volume":"153","author":"Han","year":"2010","journal-title":"Plant Physiol."},{"key":"ref_70","doi-asserted-by":"crossref","unstructured":"Huo, W., Liu, S., Chen, X., Gu, T., Wang, Z., Xu, X., Liu, D., Zhang, Y., and Jiang, S. (2025). Combined analysis of lncRNAs and mRNAs associated with coloration and wax formation during \u2018Fumei\u2019 Apple development. BMC Plant Biol., 25.","DOI":"10.1186\/s12870-025-06545-3"},{"key":"ref_71","doi-asserted-by":"crossref","first-page":"624","DOI":"10.1046\/j.1365-313X.2003.01834.x","article-title":"The Arabidopsis TDS4 gene encodes leucoanthocyanidin dioxygenase (LDOX) and is essential for proanthocyanidin synthesis and vacuole development","volume":"35","author":"Abrahams","year":"2003","journal-title":"Plant J."},{"key":"ref_72","doi-asserted-by":"crossref","first-page":"31647","DOI":"10.1074\/jbc.M302783200","article-title":"Proanthocyanidin biosynthesis in plants. Purification of legume leucoanthocyanidin reductase and molecular cloning of its cDNA","volume":"278","author":"Tanner","year":"2003","journal-title":"J. Biol. Chem."},{"key":"ref_73","doi-asserted-by":"crossref","unstructured":"Liao, L., Vimolmangkang, S., Wei, G., Zhou, H., Korban, S.S., and Han, Y. (2015). Molecular characterization of genes encoding leucoanthocyanidin reductase involved in proanthocyanidin biosynthesis in apple. Front. Plant Sci., 6.","DOI":"10.3389\/fpls.2015.00243"},{"key":"ref_74","doi-asserted-by":"crossref","first-page":"141","DOI":"10.1016\/j.plaphy.2019.03.003","article-title":"Identification of leucoanthocyanidin reductase and anthocyanidin reductase genes involved in proanthocyanidin biosynthesis in Malus crabapple plants","volume":"139","author":"Li","year":"2019","journal-title":"Plant Physiol. Biochem."},{"key":"ref_75","doi-asserted-by":"crossref","first-page":"683","DOI":"10.1146\/annurev.arplant.59.103006.093219","article-title":"Sealing plant surfaces: Cuticular wax formation by epidermal cells","volume":"59","author":"Samuels","year":"2008","journal-title":"Annu. Rev. Plant Biol."},{"key":"ref_76","doi-asserted-by":"crossref","first-page":"118","DOI":"10.1016\/j.eng.2022.12.006","article-title":"Structures and Functions of Cuticular Wax in Postharvest Fruit and Its Regulation: A Comprehensive Review with Future Perspectives","volume":"23","author":"Wu","year":"2023","journal-title":"Engineering"},{"key":"ref_77","doi-asserted-by":"crossref","unstructured":"Zhang, X., Liu, T., Zhu, S., Wang, D., Sun, S., and Xin, L. (2022). Short-term hypobaric treatment alleviates chilling injury by regulating membrane fatty acids metabolism in peach fruit. J. Food Biochem., 46.","DOI":"10.1111\/jfbc.14113"},{"key":"ref_78","doi-asserted-by":"crossref","first-page":"2347","DOI":"10.1093\/jxb\/ern101","article-title":"The Arabidopsis cytochrome P450 CYP86A1 encodes a fatty acid omega-hydroxylase involved in suberin monomer biosynthesis","volume":"59","author":"Briesen","year":"2008","journal-title":"J. Exp. Bot."},{"key":"ref_79","doi-asserted-by":"crossref","first-page":"225","DOI":"10.1146\/annurev-arplant-050312-120229","article-title":"Triterpene biosynthesis in plants","volume":"65","author":"Thimmappa","year":"2014","journal-title":"Annu. Rev. Plant Biol."},{"key":"ref_80","doi-asserted-by":"crossref","first-page":"733","DOI":"10.1111\/tpj.12060","article-title":"The Arabidopsis cer26 mutant, like the cer2 mutant, is specifically affected in the very long chain fatty acid elongation process","volume":"73","author":"Pascal","year":"2013","journal-title":"Plant J."},{"key":"ref_81","doi-asserted-by":"crossref","first-page":"1667","DOI":"10.1104\/pp.107.099481","article-title":"The developmental pattern of tomato fruit wax accumulation and its impact on cuticular transpiration barrier properties: Effects of a deficiency in a beta-ketoacyl-coenzyme A synthase (LeCER6)","volume":"144","author":"Leide","year":"2007","journal-title":"Plant Physiol."},{"key":"ref_82","doi-asserted-by":"crossref","first-page":"101","DOI":"10.1093\/aob\/mcs087","article-title":"Identification of putative candidate genes involved in cuticle formation in Prunus avium (sweet cherry) fruit","volume":"110","author":"Alkio","year":"2012","journal-title":"Ann. Bot."},{"key":"ref_83","doi-asserted-by":"crossref","first-page":"177","DOI":"10.1016\/j.foodchem.2013.12.021","article-title":"Comparative analysis of surface wax in mature fruits between Satsuma mandarin (Citrus unshiu) and \u2018Newhall\u2019 navel orange (Citrus sinensis) from the perspective of crystal morphology, chemical composition and key gene expression","volume":"153","author":"Wang","year":"2014","journal-title":"Food Chem."},{"key":"ref_84","doi-asserted-by":"crossref","first-page":"28","DOI":"10.1016\/j.plantsci.2012.05.002","article-title":"Plant fatty acyl reductases: Enzymes generating fatty alcohols for protective layers with potential for industrial applications","volume":"193","author":"Rowland","year":"2012","journal-title":"Plant Sci."},{"key":"ref_85","doi-asserted-by":"crossref","unstructured":"Chai, G., Li, C., Xu, F., Li, Y., Shi, X., Wang, Y., and Wang, Z. (2017). Three endoplasmic reticulum-associated fatty acyl-coenzyme a reductases were involved in the production of primary alcohols in hexaploid wheat (Triticum aestivum L.). BMC Plant Biol., 18.","DOI":"10.1186\/s12870-018-1256-y"},{"key":"ref_86","doi-asserted-by":"crossref","unstructured":"Liu, H., Liu, Z., Wu, Y., Zheng, L., and Zhang, G. (2021). Regulatory Mechanisms of Anthocyanin Biosynthesis in Apple and Pear. Int. J. Mol. Sci., 22.","DOI":"10.3390\/ijms22168441"},{"key":"ref_87","doi-asserted-by":"crossref","first-page":"257","DOI":"10.1080\/07352689.2017.1402852","article-title":"Biosynthesis and Regulation of Phenylpropanoids in Plants","volume":"36","author":"Deng","year":"2017","journal-title":"Crit. Rev. Plant Sci."},{"key":"ref_88","doi-asserted-by":"crossref","first-page":"16073","DOI":"10.1038\/nplants.2016.73","article-title":"The rubber tree genome reveals new insights into rubber production and species adaptation","volume":"2","author":"Tang","year":"2016","journal-title":"Nat. Plants"},{"key":"ref_89","doi-asserted-by":"crossref","first-page":"629","DOI":"10.1146\/annurev.arplant.54.031902.134840","article-title":"Functional genomics of P450s","volume":"54","author":"Schuler","year":"2003","journal-title":"Annu. Rev. Plant Biol."},{"key":"ref_90","doi-asserted-by":"crossref","first-page":"402","DOI":"10.3390\/jox13030026","article-title":"Cytochrome P450 Gene Families: Role in Plant Secondary Metabolites Production and Plant Defense","volume":"13","author":"Chakraborty","year":"2023","journal-title":"J. Xenobiot."},{"key":"ref_91","doi-asserted-by":"crossref","first-page":"271","DOI":"10.1007\/s11101-006-9007-3","article-title":"Cytochrome P450s in flavonoid metabolism","volume":"5","author":"Ayabe","year":"2006","journal-title":"Phytochem. Rev."},{"key":"ref_92","doi-asserted-by":"crossref","unstructured":"Hu, X., Liu, W., Yan, Y., Deng, H., and Cai, Y. (2023). Tropinone reductase: A comprehensive review on its role as the key enzyme in tropane alkaloids biosynthesis. Int. J. Biol. Macromol., 253.","DOI":"10.1016\/j.ijbiomac.2023.127377"},{"key":"ref_93","doi-asserted-by":"crossref","first-page":"5281","DOI":"10.1038\/s41467-018-07671-3","article-title":"Tropinone synthesis via an atypical polyketide synthase and P450-mediated cyclization","volume":"9","author":"Bedewitz","year":"2018","journal-title":"Nat. Commun."},{"key":"ref_94","doi-asserted-by":"crossref","first-page":"327","DOI":"10.1016\/j.phytochem.2005.12.001","article-title":"Tropinone reductases, enzymes at the branch point of tropane alkaloid metabolism","volume":"67","year":"2006","journal-title":"Phytochemistry"},{"key":"ref_95","doi-asserted-by":"crossref","first-page":"149","DOI":"10.1007\/s11103-017-0601-0","article-title":"The molecular mechanism underlying anthocyanin metabolism in apple using the MdMYB16 and MdbHLH33 genes","volume":"94","author":"Xu","year":"2017","journal-title":"Plant Mol. Biol."},{"key":"ref_96","doi-asserted-by":"crossref","first-page":"402","DOI":"10.1006\/meth.2001.1262","article-title":"Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta DeltaC(T))","volume":"25","author":"Livak","year":"2001","journal-title":"Method. Methods"},{"key":"ref_97","doi-asserted-by":"crossref","first-page":"1269","DOI":"10.1093\/jaoac\/88.5.1269","article-title":"Determination of total monomeric anthocyanin pigment content of fruit juices, beverages, natural colorants, and wines by the pH differential method: Collaborative study","volume":"88","author":"Lee","year":"2005","journal-title":"J. AOAC Int."},{"key":"ref_98","doi-asserted-by":"crossref","first-page":"2123","DOI":"10.1002\/fsn3.2065","article-title":"Comparing pH differential and methanol-based methods for anthocyanin assessments of strawberries","volume":"10","author":"Taghavi","year":"2021","journal-title":"Food Sci. Nutr."}],"container-title":["International Journal of Molecular Sciences"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/1422-0067\/26\/22\/10987\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,11,13]],"date-time":"2025-11-13T10:02:25Z","timestamp":1763028145000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/1422-0067\/26\/22\/10987"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2025,11,13]]},"references-count":98,"journal-issue":{"issue":"22","published-online":{"date-parts":[[2025,11]]}},"alternative-id":["ijms262210987"],"URL":"https:\/\/doi.org\/10.3390\/ijms262210987","relation":{},"ISSN":["1422-0067"],"issn-type":[{"value":"1422-0067","type":"electronic"}],"subject":[],"published":{"date-parts":[[2025,11,13]]}}}