{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,7,30]],"date-time":"2026-07-30T09:18:20Z","timestamp":1785403100200,"version":"3.56.0"},"reference-count":79,"publisher":"MDPI AG","issue":"12","license":[{"start":{"date-parts":[[2026,6,19]],"date-time":"2026-06-19T00:00:00Z","timestamp":1781827200000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/501100001809","name":"National Natural Science Foundation of China","doi-asserted-by":"publisher","award":["32172521"],"award-info":[{"award-number":["32172521"]}],"id":[{"id":"10.13039\/501100001809","id-type":"DOI","asserted-by":"publisher"}]},{"award":["32172521"],"award-info":[{"award-number":["32172521"]}],"id":[{"id":"https:\/\/ror.org\/01h0zpd94","id-type":"ROR","asserted-by":"publisher"}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["IJMS"],"abstract":"<jats:p>Identifying cold-resistance genes is essential for improving the ability of apples (Malus \u00d7 domestica) to tolerate low temperatures, as cold stress significantly limits their growth and productivity. The MdWRKY31 gene was cloned from apple, and its sequence characteristics, expression pattern, and biological function were systematically investigated. Bioinformatic analysis indicated that MdWRKY31 belongs to the group II WRKY transcription factors and is localized in the nucleus. Expression analysis revealed that MdWRKY31 transcript levels were markedly upregulated under low-temperature stress. To further explore its function, MdWRKY31 was heterologously overexpressed in tomato (Solanum lycopersicum). Following low-temperature treatment, transgenic tomato plants exhibited significantly reduced accumulation of reactive oxygen species, markedly enhanced activities of antioxidant enzymes (SOD, POD, and CAT), increased contents of proline and soluble protein, and a notable decrease in malondialdehyde levels. Additionally, transcript levels of SlCBF1, SlCBF2, SlCBF3, SlICE1, along with the ABA signaling-related genes SlNCED1 and SlABI5, were markedly elevated. Further molecular docking showed that the MdWRKY31 protein has strong binding affinity to the W-box elements in the promoters of SlCBF1 suggesting that it may regulate the expression of these genes through direct protein\u2013DNA interactions. These findings indicate that MdWRKY31 improves plant cold tolerance by CBF-dependent pathways to modulate antioxidant defenses and osmotic balance. These findings identify candidate genetic resources for breeding cold-resistant apple cultivation.<\/jats:p>","DOI":"10.3390\/ijms27125560","type":"journal-article","created":{"date-parts":[[2026,6,19]],"date-time":"2026-06-19T14:37:42Z","timestamp":1781879862000},"page":"5560","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":0,"title":["Functional Characterization and Potential Regulatory Role of MdWRKY31 in Cold Tolerance"],"prefix":"10.3390","volume":"27","author":[{"given":"Yonghui","family":"Liang","sequence":"first","affiliation":[{"name":"The Key Laboratory of Biology and Genetic Improvement of Horticultural Crops (Northeast Region), Ministry of Agriculture and Rural Affairs\/National-Local Joint Engineering Research Center for Development and Utilization of Small Fruits in Cold Regions, College of Horticulture, Northeast Agricultural University, Harbin 150030, China"},{"name":"State Key Laboratory of Crop Stress Biology for Arid Areas\/Shaanxi Key Laboratory of Apple, College of Horticulture, Northwest A&F University, Yangling 712100, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Guishuang","family":"Wang","sequence":"additional","affiliation":[{"name":"The Key Laboratory of Biology and Genetic Improvement of Horticultural Crops (Northeast Region), Ministry of Agriculture and Rural Affairs\/National-Local Joint Engineering Research Center for Development and Utilization of Small Fruits in Cold Regions, College of Horticulture, Northeast Agricultural University, Harbin 150030, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Xiaomeng","family":"Yang","sequence":"additional","affiliation":[{"name":"The Key Laboratory of Biology and Genetic Improvement of Horticultural Crops (Northeast Region), Ministry of Agriculture and Rural Affairs\/National-Local Joint Engineering Research Center for Development and Utilization of Small Fruits in Cold Regions, College of Horticulture, Northeast Agricultural University, Harbin 150030, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Bowen","family":"Zhang","sequence":"additional","affiliation":[{"name":"The Key Laboratory of Biology and Genetic Improvement of Horticultural Crops (Northeast Region), Ministry of Agriculture and Rural Affairs\/National-Local Joint Engineering Research Center for Development and Utilization of Small Fruits in Cold Regions, College of Horticulture, Northeast Agricultural University, Harbin 150030, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Yuting","family":"Ma","sequence":"additional","affiliation":[{"name":"The Key Laboratory of Biology and Genetic Improvement of Horticultural Crops (Northeast Region), Ministry of Agriculture and Rural Affairs\/National-Local Joint Engineering Research Center for Development and Utilization of Small Fruits in Cold Regions, College of Horticulture, Northeast Agricultural University, Harbin 150030, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Yujie","family":"Ji","sequence":"additional","affiliation":[{"name":"The Key Laboratory of Biology and Genetic Improvement of Horticultural Crops (Northeast Region), Ministry of Agriculture and Rural Affairs\/National-Local Joint Engineering Research Center for Development and Utilization of Small Fruits in Cold Regions, College of Horticulture, Northeast Agricultural University, Harbin 150030, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-0132-3018","authenticated-orcid":false,"given":"Deguo","family":"Han","sequence":"additional","affiliation":[{"name":"The Key Laboratory of Biology and Genetic Improvement of Horticultural Crops (Northeast Region), Ministry of Agriculture and Rural Affairs\/National-Local Joint Engineering Research Center for Development and Utilization of Small Fruits in Cold Regions, College of Horticulture, Northeast Agricultural University, Harbin 150030, China"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2026,6,19]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","unstructured":"Yan, T., Shu, X., Ning, C., Li, Y., Wang, Z., Wang, T., and Zhuang, W. (2024). Functions and regulatory mechanisms of bHLH transcription factors during the responses to biotic and abiotic stresses in woody plants. Plants, 13.","DOI":"10.3390\/plants13162315"},{"key":"ref_2","first-page":"100054","article-title":"Functional analysis of maize GRAS transcription factor gene ZmGRAS72 in response to drought and salt stresses","volume":"2","author":"She","year":"2024","journal-title":"Agric. Commun."},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"544","DOI":"10.1016\/j.molp.2020.02.004","article-title":"Molecular regulation of plant responses to environmental temperatures","volume":"13","author":"Ding","year":"2020","journal-title":"Mol. Plant."},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"uhae296","DOI":"10.1093\/hr\/uhae296","article-title":"The GRAS transcription factor PtrPAT1 of Poncirus trifoliata functions in cold tolerance and modulates glycine betaine content by regulating the BADH-like gene","volume":"12","author":"Ming","year":"2025","journal-title":"Hortic. Res."},{"key":"ref_5","doi-asserted-by":"crossref","unstructured":"Primo-Capella, A., Forner-Giner, M.\u00c1., Mart\u00ednez-Cuenca, M.-R., and Terol, J. (2022). Comparative transcriptomic analyses of citrus cold-resistant vs. sensitive rootstocks might suggest a relevant role of ABA signaling in triggering cold scion adaption. BMC Plant Biol., 22.","DOI":"10.1186\/s12870-022-03578-w"},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"444","DOI":"10.1016\/j.tplants.2007.07.002","article-title":"Cold stress regulation of gene expression in plants","volume":"12","author":"Chinnusamy","year":"2007","journal-title":"Trends Plant Sci."},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"571","DOI":"10.1146\/annurev.arplant.50.1.571","article-title":"Plant cold acclimation: Freezing tolerance genes and regulatory mechanisms","volume":"50","author":"Thomashow","year":"1999","journal-title":"Annu. Rev. Plant Biol."},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"50","DOI":"10.1007\/s10535-012-0015-4","article-title":"Isolation and functional characterization of MxCS1: A gene encoding a citrate synthase in Malus xiaojinensis","volume":"56","author":"Han","year":"2012","journal-title":"Biol. Plant."},{"key":"ref_9","doi-asserted-by":"crossref","unstructured":"Zhang, H., Dong, J., Zhao, X., Zhang, Y., Ren, J., Xing, L., Jiang, C., Wang, X., Wang, J., and Zhao, S. (2019). Research progress in membrane lipid metabolism and molecular mechanism in peanut cold tolerance. Front. Plant Sci., 10.","DOI":"10.3389\/fpls.2019.00838"},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"kiaf420","DOI":"10.1093\/plphys\/kiaf420","article-title":"Glycosylated sterols enhance cold tolerance in tomato via membrane stabilization and jasmonate signaling","volume":"199","author":"Deng","year":"2025","journal-title":"Plant Physiol."},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"283","DOI":"10.1078\/0176-1617-00833","article-title":"Electrolyte leakage and lipid degradation account for cold sensitivity in leaves of Coffea sp. plants","volume":"160","author":"Campos","year":"2003","journal-title":"J. Plant Physiol."},{"key":"ref_12","first-page":"100071","article-title":"CAD1 enhances antioxidant activity to facilitate cold storage by regulating flavonoid synthesis in cucumber","volume":"3","author":"Xia","year":"2025","journal-title":"Agric. Commun."},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"287","DOI":"10.1111\/j.1399-3054.1985.tb04267.x","article-title":"Hardening, abscisic acid, proline and freezing resistance in two winter wheat varieties","volume":"63","author":"Lalk","year":"1985","journal-title":"Physiol. Plant."},{"key":"ref_14","doi-asserted-by":"crossref","unstructured":"Alam, P., Faizan, M., Arif, Y., Azzam, M.M., Hayat, S., Afzal, S., and Albalawi, T. (2025). Reactive oxygen species: Balancing agents in plants. Front. Plant Sci., 16.","DOI":"10.3389\/fpls.2025.1713590"},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"109455","DOI":"10.1016\/j.plaphy.2024.109455","article-title":"OsNCED5 confers cold stress tolerance through regulating ROS homeostasis in rice","volume":"220","author":"Xiang","year":"2025","journal-title":"Plant Physiol. Biochem."},{"key":"ref_16","doi-asserted-by":"crossref","unstructured":"Zhou, L., Ullah, F., Zou, J., and Zeng, X. (2025). Molecular and physiological responses of plants that enhance cold tolerance. Int. J. Mol. Sci., 26.","DOI":"10.3390\/ijms26031157"},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"1770","DOI":"10.1111\/pbi.13099","article-title":"A WRKY transcription factor PbrWRKY53 from Pyrus betulaefolia is involved in drought tolerance and AsA accumulation","volume":"17","author":"Liu","year":"2019","journal-title":"Plant Biotechnol. J."},{"key":"ref_18","doi-asserted-by":"crossref","unstructured":"Ma, Q., Xia, Z., Cai, Z., Li, L., Cheng, Y., Liu, J., and Nian, H. (2019). GmWRKY16 enhances drought and salt tolerance through an ABA-mediated pathway in Arabidopsis thaliana. Front. Plant Sci., 9.","DOI":"10.3389\/fpls.2018.01979"},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"3631","DOI":"10.1093\/plcell\/koae171","article-title":"The MdHSC70\u2013MdWRKY75 module mediates basal apple thermotolerance by regulating the expression of heat shock factor genes","volume":"36","author":"Zhang","year":"2024","journal-title":"Plant Cell"},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"930","DOI":"10.1111\/pbi.14550","article-title":"The transcription factor OsNAC25 regulates potassium homeostasis in rice","volume":"23","author":"Wang","year":"2025","journal-title":"Plant Biotechnol. J."},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"81","DOI":"10.1007\/s11103-008-9353-1","article-title":"Studies on DNA-binding selectivity of WRKY transcription factors lend structural clues into WRKY-domain function","volume":"68","author":"Ciolkowski","year":"2008","journal-title":"Plant Mol. Biol."},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"247","DOI":"10.1016\/j.tplants.2010.02.006","article-title":"WRKY transcription factors","volume":"15","author":"Rushton","year":"2010","journal-title":"Trends Plant Sci."},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"199","DOI":"10.1016\/S1360-1385(00)01600-9","article-title":"The WRKY superfamily of plant transcription factors","volume":"5","author":"Eulgem","year":"2000","journal-title":"Trends Plant Sci."},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"3901","DOI":"10.1093\/jxb\/erq204","article-title":"Male gametophyte-specific WRKY34 transcription factor mediates cold sensitivity of mature pollen in Arabidopsis","volume":"61","author":"Zou","year":"2010","journal-title":"J. Exp. Bot."},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"383","DOI":"10.1111\/tpj.15950","article-title":"The OsWRKY63\u2013OsWRKY76\u2013OsDREB1B module regulates chilling tolerance in rice","volume":"112","author":"Zhang","year":"2022","journal-title":"Plant J."},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"110848","DOI":"10.1016\/j.scienta.2021.110848","article-title":"Overexpression of watermelon ClWRKY20 in transgenic Arabidopsis improves salt and low-temperature tolerance","volume":"295","author":"Zhu","year":"2022","journal-title":"Sci. Hortic."},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"988","DOI":"10.1111\/tpj.14378","article-title":"The ethylene response factor Va ERF 092 from Amur grape regulates the transcription factor Va WRKY 33, improving cold tolerance","volume":"99","author":"Sun","year":"2019","journal-title":"Plant J."},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"95","DOI":"10.1007\/s11103-019-00846-6","article-title":"Overexpression of VaWRKY12, a transcription factor from Vitis amurensis with increased nuclear localization under low temperature, enhances cold tolerance of plants","volume":"100","author":"Zhang","year":"2019","journal-title":"Plant Mol. Biol."},{"key":"ref_29","first-page":"6","article-title":"ALA up-regulated PpWRKY18 to enhance freezing tolerance of nectarine pistils","volume":"11","author":"Yuan","year":"2024","journal-title":"Hortic. Plant J."},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"65","DOI":"10.1016\/j.scienta.2012.10.004","article-title":"Overexpression of Malus xiaojinensis CS1 gene in tobacco affects plant development and increases iron stress tolerance","volume":"150","author":"Han","year":"2013","journal-title":"Sci. Hortic."},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"131020","DOI":"10.1016\/j.ijbiomac.2024.131020","article-title":"AmDHN4, a winter accumulated SKn-type dehydrin from Ammopiptanthus mongolicus, and regulated by AmWRKY45, enhances the tolerance of Arabidopsis to low temperature and osmotic stress","volume":"266","author":"Liu","year":"2024","journal-title":"Int. J. Biol. Macromol."},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"110611","DOI":"10.1016\/j.plantsci.2020.110611","article-title":"MdWRKY30, a group IIa WRKY gene from apple, confers tolerance to salinity and osmotic stresses in transgenic apple callus and Arabidopsis seedlings","volume":"299","author":"Dong","year":"2020","journal-title":"Plant Sci."},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"629","DOI":"10.1016\/j.hpj.2023.05.005","article-title":"Overexpression of the transcription factor MdWRKY115 improves drought and osmotic stress tolerance by directly binding to the MdRD22 promoter in apple","volume":"10","author":"Dong","year":"2024","journal-title":"Hortic. Plant J."},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"105","DOI":"10.1038\/s41438-020-0326-0","article-title":"MdWRKY11 improves copper tolerance by directly promoting the expression of the copper transporter gene MdHMA5","volume":"7","author":"Shi","year":"2020","journal-title":"Hortic. Res."},{"key":"ref_35","doi-asserted-by":"crossref","unstructured":"Ge, M., Tang, Y., Guan, Y., Lv, M., Zhou, C., Ma, H., and Lv, J. (2024). TaWRKY31, a novel WRKY transcription factor in wheat, participates in regulation of plant drought stress tolerance. BMC Plant Biol., 24.","DOI":"10.1186\/s12870-023-04709-7"},{"key":"ref_36","doi-asserted-by":"crossref","unstructured":"Qu, J., Xiao, P., Zhao, Z.-Q., Wang, Y.-L., Zeng, Y.-K., Zeng, X., and Liu, J.-H. (2024). Genome-wide identification, expression analysis of WRKY transcription factors in Citrus ichangensis and functional validation of CiWRKY31 in response to cold stress. BMC Plant Biol., 24.","DOI":"10.1186\/s12870-024-05320-0"},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"1784","DOI":"10.1111\/nph.70546","article-title":"Phosphorylation of the transcription factor PoWRKY31 by PoKIN10 activates lignin biosynthesis to improve tree peony drought tolerance","volume":"248","author":"Luan","year":"2025","journal-title":"New Phytol."},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"1595","DOI":"10.1016\/j.hpj.2024.09.002","article-title":"A freezing responsive UDP-glycosyltransferase improves potato freezing tolerance via modifying flavonoid metabolism","volume":"11","author":"Bao","year":"2025","journal-title":"Hortic. Plant J."},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"244","DOI":"10.1111\/pce.15146","article-title":"Tree longevity: Multifaceted genetic strategies and beyond","volume":"48","author":"Liu","year":"2025","journal-title":"Plant Cell Environ."},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"735","DOI":"10.1111\/tpj.13289","article-title":"Apple (Malus domestica) Md ERF 2 negatively affects ethylene biosynthesis during fruit ripening by suppressing Md ACS 1 transcription","volume":"88","author":"Li","year":"2016","journal-title":"Plant J."},{"key":"ref_41","doi-asserted-by":"crossref","unstructured":"Zhang, L., Xing, L., Dai, J., Li, Z., Zhang, A., Wang, T., Liu, W., Li, X., and Han, D. (2024). Overexpression of a grape WRKY transcription factor VhWRKY44 improves the resistance to cold and salt of Arabidopsis thaliana. Int. J. Mol. Sci., 25.","DOI":"10.3390\/ijms25137437"},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"2021","DOI":"10.1111\/pbi.70439","article-title":"WRKY27-RAP2. 7 Regulatory Module Promotes Cold Tolerance via Modulation of Lignin Biosynthesis and Redox Homeostasis by Regulating Cinnamyl Alcohol Dehydrogenase 7 and Glutathione S-Transferase F6","volume":"24","author":"Qu","year":"2025","journal-title":"Plant Biotechnol. J."},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"57","DOI":"10.1111\/jipb.70076","article-title":"ABA signaling orchestrates SnRK1\u03b1-dependent phosphorylation of WRKY41 to regulate SPS4 and sugar accumulation in citrus fruit under drought conditions","volume":"68","author":"Zeng","year":"2026","journal-title":"J. Integr. Plant Biol."},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"112950","DOI":"10.1016\/j.plantsci.2025.112950","article-title":"Heterologous overexpression of apple MdWAPL1 promotes fruit shape and alters fruit quality in tomato","volume":"364","author":"Shen","year":"2025","journal-title":"Plant Sci."},{"key":"ref_45","doi-asserted-by":"crossref","unstructured":"Nie, P., Wang, L., Li, M., Lyu, D., Qin, S., and Xue, X. (2023). MdSWEET23, a sucrose transporter from apple (Malus \u00d7 domestica Borkh.), influences sugar metabolism and enhances cold tolerance in tomato. Front. Plant Sci., 14.","DOI":"10.3389\/fpls.2023.1266194"},{"key":"ref_46","doi-asserted-by":"crossref","unstructured":"Fei, J., Wang, Y.-S., Cheng, H., Su, Y.-B., Zhong, Y.-J., and Zheng, L. (2022). The Kandelia obovata transcription factor KoWRKY40 enhances cold tolerance in transgenic Arabidopsis. BMC Plant Biol., 22.","DOI":"10.1186\/s12870-022-03661-2"},{"key":"ref_47","doi-asserted-by":"crossref","first-page":"909","DOI":"10.1016\/j.plaphy.2010.08.016","article-title":"Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants","volume":"48","author":"Gill","year":"2010","journal-title":"Plant Physiol. Biochem."},{"key":"ref_48","first-page":"709","article-title":"Reactive oxygen species in plants: Their generation, signal transduction, and scavenging mechanisms","volume":"5","author":"Karuppanapandian","year":"2011","journal-title":"Aust. J. Crop Sci."},{"key":"ref_49","doi-asserted-by":"crossref","first-page":"103831","DOI":"10.1016\/j.envexpbot.2019.103831","article-title":"Brassinosteroids enhance cold tolerance in Elymus nutans via mediating redox homeostasis and proline biosynthesis","volume":"167","author":"Fu","year":"2019","journal-title":"Environ. Exp. Bot."},{"key":"ref_50","doi-asserted-by":"crossref","unstructured":"Qian, Z., He, L., and Li, F. (2024). Understanding cold stress response mechanisms in plants: An overview. Front. Plant Sci., 15.","DOI":"10.3389\/fpls.2024.1443317"},{"key":"ref_51","doi-asserted-by":"crossref","first-page":"59","DOI":"10.1007\/s12355-014-0343-0","article-title":"Effects of exogenous abscisic acid on cell membrane and endogenous hormone contents in leaves of sugarcane seedlings under cold stress","volume":"17","author":"Huang","year":"2015","journal-title":"Sugar Tech."},{"key":"ref_52","doi-asserted-by":"crossref","first-page":"105190","DOI":"10.1016\/j.envexpbot.2022.105190","article-title":"Low temperature stress-induced perception and molecular signaling pathways in plants","volume":"207","author":"Guan","year":"2023","journal-title":"Environ. Exp. Bot."},{"key":"ref_53","doi-asserted-by":"crossref","first-page":"2907","DOI":"10.1105\/tpc.113.112631","article-title":"Jasmonate regulates the inducer of CBF expression\u2013c-repeat binding factor\/DRE binding factor1 cascade and freezing tolerance in Arabidopsis","volume":"25","author":"Hu","year":"2013","journal-title":"Plant Cell"},{"key":"ref_54","doi-asserted-by":"crossref","first-page":"2578","DOI":"10.1105\/tpc.112.098640","article-title":"Ethylene signaling negatively regulates freezing tolerance by repressing expression of CBF and type-A ARR genes in Arabidopsis","volume":"24","author":"Shi","year":"2012","journal-title":"Plant Cell"},{"key":"ref_55","doi-asserted-by":"crossref","first-page":"2712","DOI":"10.1111\/pce.13868","article-title":"The HY5 and MYB15 transcription factors positively regulate cold tolerance in tomato via the CBF pathway","volume":"43","author":"Zhang","year":"2020","journal-title":"Plant Cell Environ."},{"key":"ref_56","doi-asserted-by":"crossref","first-page":"113662","DOI":"10.1016\/j.scienta.2024.113662","article-title":"Overexpression of SlMYB1R1 improves chilling stress tolerance in tomato","volume":"338","author":"Nie","year":"2024","journal-title":"Sci. Hortic."},{"key":"ref_57","first-page":"785","article-title":"Tomato inducer of CBF expression 1 (SlICE1) is involved in cold and salt stress signaling","volume":"4","author":"Yuasa","year":"2014","journal-title":"Am. J. Exp. Agric."},{"key":"ref_58","doi-asserted-by":"crossref","first-page":"162","DOI":"10.1016\/j.cj.2016.01.010","article-title":"Phytohormones and their metabolic engineering for abiotic stress tolerance in crop plants","volume":"4","author":"Wani","year":"2016","journal-title":"Crop J."},{"key":"ref_59","first-page":"251","article-title":"A novel cis-acting element in an Arabidopsis gene is involved in responsiveness to drought, low-temperature, or high-salt stress","volume":"6","author":"Shinozaki","year":"1994","journal-title":"Plant Cell"},{"key":"ref_60","doi-asserted-by":"crossref","unstructured":"Ren, C., Li, Z., Song, P., Wang, Y., Liu, W., Zhang, L., Li, X., Li, W., and Han, D. (2023). Overexpression of a grape MYB transcription factor gene VhMYB2 increases salinity and drought tolerance in Arabidopsis thaliana. Int. J. Mol. Sci., 24.","DOI":"10.3390\/ijms241310743"},{"key":"ref_61","doi-asserted-by":"crossref","first-page":"1075","DOI":"10.1093\/plphys\/kiad578","article-title":"Transcription factor SlWRKY50 enhances cold tolerance in tomato by activating the jasmonic acid signaling","volume":"194","author":"Wang","year":"2024","journal-title":"Plant Physiol."},{"key":"ref_62","doi-asserted-by":"crossref","unstructured":"Zhang, K., Chen, J., Liu, J., Li, H., and Jiang, M. (2025). Genome-wide identification of the WRKY transcription factors family and regulation of metabolites under cold stress in Astragalus membranaceus. BMC Plant Biol., 25.","DOI":"10.1186\/s12870-025-07685-2"},{"key":"ref_63","doi-asserted-by":"crossref","first-page":"802","DOI":"10.1007\/s11105-012-0551-2","article-title":"Overexpression of a Malus xiaojinensis Nas1 gene influences flower development and tolerance to iron stress in transgenic tobacco","volume":"31","author":"Han","year":"2013","journal-title":"Plant Mol. Biol. Rep."},{"key":"ref_64","doi-asserted-by":"crossref","first-page":"133","DOI":"10.1007\/s11105-014-0735-z","article-title":"Isolation and preliminary functional analysis of MxCS2: A gene encoding a citrate synthase in Malus xiaojinensis","volume":"33","author":"Han","year":"2015","journal-title":"Plant Mol. Biol. Rep."},{"key":"ref_65","doi-asserted-by":"crossref","first-page":"2057","DOI":"10.1111\/pbi.14112","article-title":"MdNAC104 positively regulates apple cold tolerance via CBF-dependent and CBF-independent pathways","volume":"21","author":"Mei","year":"2023","journal-title":"Plant Biotechnol. J."},{"key":"ref_66","doi-asserted-by":"crossref","first-page":"189","DOI":"10.1007\/s11627-022-10256-x","article-title":"Overexpression of MxFRO6, a FRO gene from Malus xiaojinensis, increases iron and salt tolerance in Arabidopsis thaliana","volume":"58","author":"Li","year":"2022","journal-title":"In Vitro Cell. Dev. Biol.-Plant"},{"key":"ref_67","doi-asserted-by":"crossref","first-page":"154526","DOI":"10.1016\/j.jplph.2025.154526","article-title":"MbWRKY50 confers cold and drought tolerance through upregulating antioxidant capacity associated with ROS scavenging","volume":"310","author":"Wang","year":"2025","journal-title":"J. Plant Physiol."},{"key":"ref_68","doi-asserted-by":"crossref","first-page":"2019","DOI":"10.1038\/nprot.2006.286","article-title":"Rapid, transient expression of fluorescent fusion proteins in tobacco plants and generation of stably transformed plants","volume":"1","author":"Sparkes","year":"2006","journal-title":"Nat. Protoc."},{"key":"ref_69","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_70","doi-asserted-by":"crossref","first-page":"209","DOI":"10.1007\/s10725-014-9945-5","article-title":"Isolation and functional analysis of MdCS1: A gene encoding a citrate synthase in Malus domestica (L.) Borkh","volume":"75","author":"Han","year":"2015","journal-title":"Plant Growth Regul."},{"key":"ref_71","doi-asserted-by":"crossref","first-page":"157","DOI":"10.1007\/s10725-006-9101-y","article-title":"Effect of salt and drought stress on antioxidant enzymes activities and SOD isoenzymes of liquorice (Glycyrrhiza uralensis Fisch)","volume":"49","author":"Pan","year":"2006","journal-title":"Plant Growth Regul."},{"key":"ref_72","doi-asserted-by":"crossref","first-page":"7057","DOI":"10.1021\/jf4051717","article-title":"Enzymatic changes in phenylalanine ammonia-lyase, cinnamic-4-hydroxylase, capsaicin synthase, and peroxidase activities in Capsicum under drought stress","volume":"62","author":"Phimchan","year":"2014","journal-title":"J. Agric. Food Chem."},{"key":"ref_73","doi-asserted-by":"crossref","first-page":"479","DOI":"10.1007\/s10725-017-0274-3","article-title":"Isolation and functional analysis of MxCS3: A gene encoding a citrate synthase in Malus xiaojinensis, with functions in tolerance to iron stress and abnormal flower in transgenic Arabidopsis thaliana","volume":"82","author":"Han","year":"2017","journal-title":"Plant Growth Regul."},{"key":"ref_74","doi-asserted-by":"crossref","first-page":"433","DOI":"10.1080\/17429145.2018.1499145","article-title":"Isolation and functional analysis of MxNAS3 involved in enhanced iron stress tolerance and abnormal flower in transgenic Arabidopsis","volume":"13","author":"Han","year":"2018","journal-title":"J. Plant Interact."},{"key":"ref_75","doi-asserted-by":"crossref","first-page":"143","DOI":"10.1016\/j.foodchem.2019.04.048","article-title":"Effect of eugenol fumigation treatment on chilling injury and CBF gene expression in eggplant fruit during cold storage","volume":"292","author":"Huang","year":"2019","journal-title":"Food Chem."},{"key":"ref_76","doi-asserted-by":"crossref","first-page":"154001","DOI":"10.1016\/j.jplph.2023.154001","article-title":"MxFRO4 confers iron and salt tolerance through up-regulating antioxidant capacity associated with the ROS scavenging","volume":"285","author":"Ren","year":"2023","journal-title":"J. Plant Physiol."},{"key":"ref_77","doi-asserted-by":"crossref","first-page":"9","DOI":"10.1016\/j.ecoenv.2019.04.006","article-title":"Enhanced drought tolerance of foxtail millet seedlings by sulfur dioxide fumigation","volume":"178","author":"Han","year":"2019","journal-title":"Ecotoxicol. Environ. Saf."},{"key":"ref_78","doi-asserted-by":"crossref","first-page":"3937","DOI":"10.1007\/s11033-019-04840-5","article-title":"ZmMYB31, a R2R3-MYB transcription factor in maize, positively regulates the expression of CBF genes and enhances resistance to chilling and oxidative stress","volume":"46","author":"Li","year":"2019","journal-title":"Mol. Biol. Rep."},{"key":"ref_79","doi-asserted-by":"crossref","first-page":"545","DOI":"10.1111\/pbi.12794","article-title":"Improvement of drought tolerance by overexpressing MdATG18a is mediated by modified antioxidant system and activated autophagy in transgenic apple","volume":"16","author":"Sun","year":"2018","journal-title":"Plant Biotechnol. J."}],"container-title":["International Journal of Molecular Sciences"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/1422-0067\/27\/12\/5560\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2026,6,27]],"date-time":"2026-06-27T05:03:22Z","timestamp":1782536602000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/1422-0067\/27\/12\/5560"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2026,6,19]]},"references-count":79,"journal-issue":{"issue":"12","published-online":{"date-parts":[[2026,6]]}},"alternative-id":["ijms27125560"],"URL":"https:\/\/doi.org\/10.3390\/ijms27125560","relation":{},"ISSN":["1422-0067"],"issn-type":[{"value":"1422-0067","type":"electronic"}],"subject":[],"published":{"date-parts":[[2026,6,19]]}}}