{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,7,27]],"date-time":"2026-07-27T17:54:13Z","timestamp":1785174853479,"version":"3.55.0"},"reference-count":45,"publisher":"MDPI AG","issue":"10","license":[{"start":{"date-parts":[[2025,5,13]],"date-time":"2025-05-13T00:00:00Z","timestamp":1747094400000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"name":"National Natural Science Foundation Regional Fund","award":["32360721"],"award-info":[{"award-number":["32360721"]}]},{"name":"National Natural Science Foundation Regional Fund","award":["2024DA010"],"award-info":[{"award-number":["2024DA010"]}]},{"name":"Xinjiang Production and Construction Corps science and technology development project","award":["32360721"],"award-info":[{"award-number":["32360721"]}]},{"name":"Xinjiang Production and Construction Corps science and technology development project","award":["2024DA010"],"award-info":[{"award-number":["2024DA010"]}]},{"name":"Tianchi Talent Young Doctoral Program of Xinjiang Uygur Autonomous Region","award":["32360721"],"award-info":[{"award-number":["32360721"]}]},{"name":"Tianchi Talent Young Doctoral Program of Xinjiang Uygur Autonomous Region","award":["2024DA010"],"award-info":[{"award-number":["2024DA010"]}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["IJMS"],"abstract":"<jats:p>Sunburn in apple peel significantly affects fruit appearance and reduces its commercial value. Previous research has shown that apple peel reduces sunburn by increasing the accumulation of proanthocyanidins (PAs) and other protective compounds. However, the precise molecular regulatory mechanism remains unclear. In this study, we systematically investigated MdANR, a key gene involved in PAs biosynthesis. We found that MdANR expression in apple peel is responsive to temperature and light fluctuations, with higher expression levels observed under increased temperature and light exposure. Functional analysis revealed that MdANR overexpression in apple peel and callus enhanced resistance to high-temperature and -light-intensity stress, accompanied by a corresponding increase in PAs and chlorogenic acid contents. In addition, we demonstrated that MdMYBR9 can activate MdANR promoter activity and promote its expression through yeast one-hybrid, dual-luciferase, and electrophoretic mobility transfer experiments. The results indicated that MdMYBR9 was an upstream regulator of MdANR. Based on these findings, this study proposes the MdMYBR9-MdANR-PAs regulatory model for apple sunburn resistance, providing a molecular framework for enhancing sunburn tolerance in apple breeding programs.<\/jats:p>","DOI":"10.3390\/ijms26104656","type":"journal-article","created":{"date-parts":[[2025,5,13]],"date-time":"2025-05-13T09:26:48Z","timestamp":1747128408000},"page":"4656","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":2,"title":["Regulation of MdANR in Anti-Burning Process of Apple Peel"],"prefix":"10.3390","volume":"26","author":[{"given":"Yifeng","family":"Feng","sequence":"first","affiliation":[{"name":"College of Horticulture and Forestry, Tarim University, Alar 843300, China"},{"name":"College of Horticulture, Northwest A&F University, Yangling 712100, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Wenya","family":"Tian","sequence":"additional","affiliation":[{"name":"College of Horticulture and Forestry, Tarim University, Alar 843300, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Junjiao","family":"Guo","sequence":"additional","affiliation":[{"name":"College of Horticulture and Forestry, Tarim University, Alar 843300, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jianghong","family":"Fu","sequence":"additional","affiliation":[{"name":"College of Horticulture, Northwest A&F University, Yangling 712100, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-5315-3658","authenticated-orcid":false,"given":"Jiangbo","family":"Wang","sequence":"additional","affiliation":[{"name":"College of Horticulture and Forestry, Tarim University, Alar 843300, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Yan","family":"Wang","sequence":"additional","affiliation":[{"name":"College of Horticulture and Forestry, Tarim University, Alar 843300, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Zhengyang","family":"Zhao","sequence":"additional","affiliation":[{"name":"College of Horticulture, Northwest A&F University, Yangling 712100, China"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2025,5,13]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"455","DOI":"10.1080\/07352689.2012.696453","article-title":"Sunburn of Apple Fruit: Historical Background, Recent Advances and Future Perspectives","volume":"31","author":"Racsko","year":"2012","journal-title":"Crit. Rev. Plant Sci."},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"9","DOI":"10.1016\/j.agrformet.2017.01.016","article-title":"Above and below-ground environmental changes associated with the use of photoselective protective netting to reduce sunburn in apple","volume":"237\u2013238","author":"Kalcsits","year":"2017","journal-title":"Agric. For. Meteorol."},{"key":"ref_3","first-page":"128","article-title":"Tools for climate resilience in tree fruit I: Large-dwarfing rootstocks can alleviate sunburn damage in \u201cBuckeye Gala\u201d apple","volume":"108","author":"Xu","year":"2022","journal-title":"Can. J. Plant Sci."},{"key":"ref_4","doi-asserted-by":"crossref","unstructured":"Yoo, J., Sepulveda, G., Rudell, D., and Torres, C.A. (2022). Comparative analysis of metabolic differences between sunburn and sunscald disorder on \u2019Packham\u2019s triumph\u2019 pear. Postharvest Biol. Technol., 195.","DOI":"10.1016\/j.postharvbio.2022.112153"},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"112153","DOI":"10.1016\/j.scienta.2024.112856","article-title":"Epicuticular waxes: A natural packaging to deal with sunburn browning in white grapes","volume":"328","author":"Domanda","year":"2024","journal-title":"Sci. Hortic."},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"27","DOI":"10.1016\/j.jfoodeng.2008.05.035","article-title":"Development of a machine for the automatic sorting of pomegranate (Punica granatum) arils based on computer vision","volume":"90","author":"Blasco","year":"2009","journal-title":"J. Food Eng."},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"388","DOI":"10.1016\/j.foodchem.2014.12.076","article-title":"Proteomics approach reveals mechanism underlying susceptibility of loquat fruit to sunburn during color changing period","volume":"176","author":"Jiang","year":"2015","journal-title":"Food Chem."},{"key":"ref_8","doi-asserted-by":"crossref","unstructured":"Morales-Quintana, L., Waite, J.M., Kalcsits, L., Torres, C.A., and Ramos, P. (2020). Sun injury on apple fruit: Physiological, biochemical and molecular advances, and future challenges. Sci. Hortic., 260.","DOI":"10.1016\/j.scienta.2019.108866"},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"160","DOI":"10.1080\/15538360802526472","article-title":"Photooxidative sunburn of apples: Characterization of a third type of apple sunburn","volume":"8","author":"Felicetti","year":"2008","journal-title":"Int. J. Fruit Sci."},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"57","DOI":"10.1016\/j.scienta.2009.12.003","article-title":"The effect of maturity, sunburn and the application of sunscreens on the internal and external qualities of pomegranate fruit grown in Australia","volume":"124","author":"Weerakkody","year":"2010","journal-title":"Sci. Hortic."},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"987","DOI":"10.1016\/j.foodchem.2015.11.004","article-title":"Evaluation of the antioxidant capacity of natural polyphenolic compounds using a macrocyclic Ni-(II) complex-catalysed Briggs\u2013Rauscher reaction","volume":"197","author":"Li","year":"2016","journal-title":"Food Chem."},{"key":"ref_12","doi-asserted-by":"crossref","unstructured":"Chai, W., Shao, T., Zeng, S., Guo, Y., Wu, Y., Wei, W., Pan, Q., and Xia, X.-L. (2024). Longan seed tannins as a quality tyrosinase inhibitor and browning resistance agent: Activity and mechanism. Ind. Crop. Prod., 222.","DOI":"10.1016\/j.indcrop.2024.119918"},{"key":"ref_13","doi-asserted-by":"crossref","unstructured":"Zhou, W., Yu, J., Zhao, L., Wang, K., Hu, Z., Wu, J.-Y., and Liu, X. (2024). Enhancement of chitosan-based film physicochemical and storage properties by interaction with proanthocyanidin and natural deep eutectic solvent. Int. J. Biol. Macromol., 278.","DOI":"10.1016\/j.ijbiomac.2024.134611"},{"key":"ref_14","doi-asserted-by":"crossref","unstructured":"Fu, J., Feng, Y., Zheng, Y., Zhong, Y., Li, X., Liu, L., and Zhao, Z. (2025). MdGATA15 regulates MdANR to promote the synthesis of procyanidin and enhance the sunburn resistance of apple fruit. Sci. Hortic., 339.","DOI":"10.1016\/j.scienta.2024.113854"},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"1557","DOI":"10.1016\/j.fshw.2023.02.003","article-title":"Transcriptome and weighted gene co-expression network analysis of jujube (Ziziphus jujub Mill.) fruit reveal putative genes involved in proanthocyanin biosynthesis and regulation","volume":"12","author":"Wang","year":"2023","journal-title":"Food Sci Hum Well."},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"652","DOI":"10.1104\/pp.105.064238","article-title":"Proanthocyanidin synthesis and expression of genes encoding leucoanthocyanidin reductase and anthocyanidin reductase in developing grape berries and grapevine leaves","volume":"139","author":"Bogs","year":"2005","journal-title":"Plant Physiol."},{"key":"ref_17","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_18","doi-asserted-by":"crossref","unstructured":"Su, Z., Jiao, Y., Jiang, Z., Liu, P., Chen, Q., Qu, Y., and Deng, X. (2022). Gb_ANR-47 Enhances the Resistance of Gossypium barbadense to Fusarium oxysporum f. sp. vasinfectum (FOV) by Regulating the Content of Proanthocyanidins. Plants, 11.","DOI":"10.3390\/plants11151902"},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"892","DOI":"10.1111\/plb.13559","article-title":"Functional identification of ANR genes in apple (Malus halliana) that reduce saline\u2013alkali stress tolerance","volume":"25","author":"Wang","year":"2023","journal-title":"Plant Biol."},{"key":"ref_20","doi-asserted-by":"crossref","unstructured":"Feng, Y., Liu, L., Yu, J., Chen, R., Hu, C., Wang, H., Li, D., Wang, Z., and Zhao, Z. (2023). Combined transcriptomic and metabolomic analyses reveal the mechanism of debagged \u2018Fuji\u2019 apple sunburn. Food Sci. Technol., 181.","DOI":"10.1016\/j.lwt.2023.114680"},{"key":"ref_21","doi-asserted-by":"crossref","unstructured":"Yang, Y., Yao, G., Yue, W., Zhang, S., and Wu, J. (2015). Transcriptome profiling reveals differential gene expression in proanthocyanidin biosynthesis associated with red\/green skin color mutant of pear (Pyrus communis L.). Front. Plant Sci., 6.","DOI":"10.3389\/fpls.2015.00795"},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"91","DOI":"10.1016\/j.abb.2003.12.011","article-title":"Anthocyanidin reductases from Medicago truncatula and Arabidopsis thaliana","volume":"422","author":"Xie","year":"2004","journal-title":"Arch Biochem. Biophys."},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"562","DOI":"10.1111\/tpj.14050","article-title":"R2R3-MYB transcription factor MdMYB23 is involved in the cold tolerance and proanthocyanidin accumulation in apple","volume":"96","author":"An","year":"2018","journal-title":"Plant J."},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"2437","DOI":"10.1093\/jxb\/err415","article-title":"Introduction of apple ANR genes into tobacco inhibits expression of both CHI and DFR genes in flowers, leading to loss of anthocyanin","volume":"63","author":"Han","year":"2012","journal-title":"J. Exp. Bot."},{"key":"ref_25","doi-asserted-by":"crossref","unstructured":"Xin, Y., Meng, S., Ma, B., He, W., and He, N. (2020). Mulberry genes MnANR and MnLAR confer transgenic plants with resistance to Botrytis cinerea. Plant Sci., 296.","DOI":"10.1016\/j.plantsci.2020.110473"},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"36","DOI":"10.1016\/j.plantsci.2013.04.008","article-title":"Subcellular localization and vacuolar targeting of sorbitol dehydrogenase in apple seed","volume":"210","author":"Wang","year":"2013","journal-title":"Plant Sci."},{"key":"ref_27","doi-asserted-by":"crossref","unstructured":"Li, X., Liu, J., Chang, Q., Zhou, Z., Han, R., and Liang, Z. (2021). Antioxidant and Antidiabetic Activity of Proanthocyanidins from Fagopyrum dibotrys. Molecules, 26.","DOI":"10.3390\/molecules26092417"},{"key":"ref_28","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_29","doi-asserted-by":"crossref","first-page":"225","DOI":"10.1016\/j.jphotobiol.2018.07.024","article-title":"Characterization of anthocyanin and proanthocyanidin biosynthesis in two straw-berry genotypes during fruit development in response to different light qualities","volume":"186","author":"Zhang","year":"2018","journal-title":"J. Photochem. Photobiol. B"},{"key":"ref_30","doi-asserted-by":"crossref","unstructured":"Verma, P., Sen, R., Bamanna, A., Elhindawy, M., Nagpal, K., and Krishnan, V. (2024). Structural chemistry to therapeutic functionality: A comprehensive review on proanthocyanidins. Biocatal. Agric. Biotechnol., 55.","DOI":"10.1016\/j.bcab.2023.102963"},{"key":"ref_31","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_32","doi-asserted-by":"crossref","unstructured":"Junior, W.D.O.C., Guimar\u00e3es, M.L.R., Freitas, K.M., Pereira, R.S., de P\u00e1dua, R.M., Campana, P.R.V., and Braga, F.C. (2024). Structural characterization of a proanthocyanidin-rich fraction from Hancornia speciosa leaves and its effect on the release of pro-inflammatory cytokines and oxidative stress in THP-1 cells. J. Ethnopharmacol., 333.","DOI":"10.1016\/j.jep.2024.118471"},{"key":"ref_33","doi-asserted-by":"crossref","unstructured":"Simiyu, D.C., Bayaraa, U., Jang, J.H., and Lee, O.R. (2024). The R2R3-MYB transcription factor PgTT2 from Panax ginseng interacts with the WD40-repeat protein PgTTG1 during the regulation of proanthocyanidin biosynthesis and the response to salt stress. Plant Physiol. Biochem., 214.","DOI":"10.1016\/j.plaphy.2024.108877"},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"351","DOI":"10.1111\/nph.14569","article-title":"The transcription factor MYB115 contributes to the regulation ofproanthocya-nidin biosynthesis and enhances fungal resistance inpoplar","volume":"215","author":"Wang","year":"2017","journal-title":"New Phytol."},{"key":"ref_35","doi-asserted-by":"crossref","unstructured":"Chen, L., Chen, Y., Shen, Y., Xing, W., Cui, Y., and Luo, P. (2023). RhMYB1 and RhMYB123 form a positive feedback loop to regulate the proanthocyanidin biosynthesis in rose. Ind. Crop. Prod., 196.","DOI":"10.1016\/j.indcrop.2023.116492"},{"key":"ref_36","doi-asserted-by":"crossref","unstructured":"Zhao, W., Wu, W., Liu, Y., Fan, L., Meng, H., Wang, L., and Wu, G. (2023). The TT2-type MYB transcription factor JrMYB12 positively regulates proanthocyanidin biosynthesis in red walnut. Sci. Hortic., 307.","DOI":"10.1016\/j.scienta.2022.111515"},{"key":"ref_37","doi-asserted-by":"crossref","unstructured":"Sun, Q., Jiang, S., Zhang, T., Xu, H., Fang, H., Zhang, J., Su, M., Wang, Y., Zhang, Z., and Wang, N. (2019). Apple NAC transcription factor MdNAC52 regulates biosynthesis of anthocyanin and proanthocyanidin through MdMYB9 and MdMYB11. Plant Sci., 289.","DOI":"10.1016\/j.plantsci.2019.110286"},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"650","DOI":"10.1093\/pcp\/pcu205","article-title":"MdMYB9 and MdMYB11 are Involved in the Regulation of the JA-Induced Biosynthesis of Anthocyanin and Proanthocyanidin in Apples","volume":"56","author":"An","year":"2015","journal-title":"Plant Cell Physiol."},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"305","DOI":"10.1016\/j.hpj.2022.10.013","article-title":"Resistance index and browning mechanism of apple peel under high temperature stress","volume":"10","author":"Wang","year":"2024","journal-title":"Hortic. Plant J."},{"key":"ref_40","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\u2212\u0394\u0394CT Method","volume":"25","author":"Livak","year":"2001","journal-title":"Methods"},{"key":"ref_41","doi-asserted-by":"crossref","unstructured":"Feng, Y., Li, S., Jia, R., Yang, J., Su, Q., and Zhao, Z. (2022). Physiological Characteristics of Sunburn Peel after Apple Debagged. Molecules, 27.","DOI":"10.3390\/molecules27123775"},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"200","DOI":"10.1016\/j.plaphy.2016.03.021","article-title":"Characterization and expression profiling of MYB transcription factors against stresses and during male organ development in Chinese cabbage (Brassica rapa ssp pekinensis)","volume":"104","author":"Saha","year":"2016","journal-title":"Plant Physiol. Biochem."},{"key":"ref_43","doi-asserted-by":"crossref","unstructured":"Liu, X., Liu, L., Yu, J., Li, S., Li, D., Feng, Y., and Zhao, Z. (2023). Role of the transcription factor MdABF2 in abscisic acid-induced volatile compound biosynthesis in \u2018Ruixue\u2019 (Malus \u00d7 domestica) apple during storage. Postharvest Biol. Technol., 205.","DOI":"10.1016\/j.postharvbio.2023.112524"},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"2102","DOI":"10.1093\/plphys\/kiad064","article-title":"Transcriptomic and metabolomic analysis reveals a protein module involved in preharvest apple peel browning","volume":"192","author":"Wang","year":"2023","journal-title":"Plant Physiol."},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"1683","DOI":"10.1111\/pbi.13839","article-title":"The MdBBX22-miR858-MdMYB9\/11\/12 module regulates proanthocyanidin biosynthesis in apple peel","volume":"20","author":"Zhang","year":"2022","journal-title":"Plant Biotechnol. J."}],"container-title":["International Journal of Molecular Sciences"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/1422-0067\/26\/10\/4656\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,9]],"date-time":"2025-10-09T17:31:53Z","timestamp":1760031113000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/1422-0067\/26\/10\/4656"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2025,5,13]]},"references-count":45,"journal-issue":{"issue":"10","published-online":{"date-parts":[[2025,5]]}},"alternative-id":["ijms26104656"],"URL":"https:\/\/doi.org\/10.3390\/ijms26104656","relation":{},"ISSN":["1422-0067"],"issn-type":[{"value":"1422-0067","type":"electronic"}],"subject":[],"published":{"date-parts":[[2025,5,13]]}}}