{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,7,31]],"date-time":"2026-07-31T21:46:57Z","timestamp":1785534417870,"version":"3.56.0"},"reference-count":61,"publisher":"Wiley","issue":"3","license":[{"start":{"date-parts":[[2025,10,13]],"date-time":"2025-10-13T00:00:00Z","timestamp":1760313600000},"content-version":"vor","delay-in-days":0,"URL":"http:\/\/creativecommons.org\/licenses\/by-nc\/4.0\/"},{"start":{"date-parts":[[2025,10,13]],"date-time":"2025-10-13T00:00:00Z","timestamp":1760313600000},"content-version":"tdm","delay-in-days":0,"URL":"http:\/\/doi.wiley.com\/10.1002\/tdm_license_1.1"}],"funder":[{"DOI":"10.13039\/501100001809","name":"National Natural Science Foundation of China","doi-asserted-by":"publisher","award":["31971766"],"award-info":[{"award-number":["31971766"]}],"id":[{"id":"10.13039\/501100001809","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100001809","name":"National Natural Science Foundation of China","doi-asserted-by":"publisher","award":["32030074"],"award-info":[{"award-number":["32030074"]}],"id":[{"id":"10.13039\/501100001809","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":["onlinelibrary.wiley.com"],"crossmark-restriction":true},"short-container-title":["Plant Biotechnology Journal"],"published-print":{"date-parts":[[2026,3]]},"abstract":"ABSTRACT<\/jats:title>\n \n Low temperature triggers Ca\n 2+<\/jats:sup>\n signalling and reprogramming of gene expression and metabolism in plants. However, how the Ca\n 2+<\/jats:sup>\n signal is transduced to the downstream metabolic pathways remains unknown. The involvement of a cold\u2010induced calmodulin\u2010like protein, MfCML50, from\n \n Medicago falcata<\/jats:italic>\n <\/jats:styled-content>\n in regulation of cold tolerance was examined in the present study. The interaction of MfCML50 with isopiperitenol\/carveol dehydrogenase (MfCDH) was identified, which was dependent upon Ca\n 2+<\/jats:sup>\n and led to activated activity of MfCDH. MfCDH catalysed the production of carvone from carveol, with\n K<\/jats:italic>\n m<\/jats:sub>\n value of 10.25\u2009\u03bcM. Overexpression of\n MfCML50<\/jats:italic>\n or\n MfCDH<\/jats:italic>\n in\n \n Medicago truncatula<\/jats:italic>\n <\/jats:styled-content>\n led to enhanced cold tolerance with increased accumulation of carvone under cold conditions. The knockout mutation of the ortholog MtCML50 and MtCDH in\n \n M. truncatula<\/jats:italic>\n <\/jats:styled-content>\n led to reduced cold tolerance with decreased accumulation of carvone in the\n mtcml50<\/jats:italic>\n ,\n mtcdh<\/jats:italic>\n , or\n mtcml50 mtcdh<\/jats:italic>\n mutants under cold conditions, which could be recovered by expressing\n MfCML50<\/jats:italic>\n or\n MfCDH<\/jats:italic>\n or exogenous application of carvone. The diphenyl\u20102\u2010picrylhydrazyl (DPPH) assay showed that carvone exhibited strong antioxidant activity. Less ROS were accumulated in\n MfCML50<\/jats:italic>\n and\n MfCDH<\/jats:italic>\n overexpressing lines, but more ROS were accumulated in\n mtcml50<\/jats:italic>\n and\n mtcdh<\/jats:italic>\n mutants under cold conditions. The results suggested that the Ca\n 2+<\/jats:sup>\n signal activated the MfCML50\u2010MfCDH module regulates cold tolerance through promoted production of carvone to maintain ROS homeostasis.\n <\/jats:p>","DOI":"10.1111\/pbi.70372","type":"journal-article","created":{"date-parts":[[2025,10,14]],"date-time":"2025-10-14T01:17:56Z","timestamp":1760404676000},"page":"1152-1165","update-policy":"https:\/\/doi.org\/10.1002\/crossmark_policy","source":"Crossref","is-referenced-by-count":2,"title":["Calmodulin\u2010Like Protein MfCML50 Interacts With Carveol Dehydrogenase in\n Medicago falcata<\/i>\n to Regulate Cold Tolerance Through Mediating ROS Homeostasis"],"prefix":"10.1111","volume":"24","author":[{"given":"Bohao","family":"Geng","sequence":"first","affiliation":[{"name":"College of Grassland Science Nanjing Agricultural University Nanjing China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Shuhan","family":"Yu","sequence":"additional","affiliation":[{"name":"College of Grassland Science Nanjing Agricultural University Nanjing China"},{"name":"College of Landscape and Architecture Zhejiang A&F University Hangzhou China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Qiguo","family":"Sun","sequence":"additional","affiliation":[{"name":"College of Grassland Science Nanjing Agricultural University Nanjing China"},{"name":"Department of Agronomy and Horticulture Jiangsu Vocational College of Agriculture and Forestry Jurong China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Lei","family":"Yang","sequence":"additional","affiliation":[{"name":"College of Grassland Science Nanjing Agricultural University Nanjing China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Qian","family":"Yang","sequence":"additional","affiliation":[{"name":"College of Grassland Science Nanjing Agricultural University Nanjing China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Hailong","family":"Yang","sequence":"additional","affiliation":[{"name":"College of Grassland Science Nanjing Agricultural University Nanjing China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-6840-1589","authenticated-orcid":false,"given":"Zhenfei","family":"Guo","sequence":"additional","affiliation":[{"name":"College of Grassland Science Nanjing Agricultural University Nanjing China"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"311","published-online":{"date-parts":[[2025,10,13]]},"reference":[{"key":"e_1_2_8_2_1","doi-asserted-by":"publisher","DOI":"10.1074\/jbc.M117.787796"},{"key":"e_1_2_8_3_1","doi-asserted-by":"publisher","DOI":"10.3390\/biom11121803"},{"key":"e_1_2_8_4_1","doi-asserted-by":"publisher","DOI":"10.1111\/nph.13612"},{"key":"e_1_2_8_5_1","doi-asserted-by":"publisher","DOI":"10.1104\/pp.108.119461"},{"key":"e_1_2_8_6_1","doi-asserted-by":"publisher","DOI":"10.1111\/pce.15342"},{"key":"e_1_2_8_7_1","doi-asserted-by":"publisher","DOI":"10.1111\/jipb.13228"},{"key":"e_1_2_8_8_1","doi-asserted-by":"publisher","DOI":"10.1007\/s00299-021-02757-7"},{"key":"e_1_2_8_9_1","doi-asserted-by":"publisher","DOI":"10.1111\/tpj.15535"},{"key":"e_1_2_8_10_1","doi-asserted-by":"publisher","DOI":"10.1105\/tpc.002477"},{"key":"e_1_2_8_11_1","doi-asserted-by":"publisher","DOI":"10.1111\/pbi.12166"},{"key":"e_1_2_8_12_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.postharvbio.2023.112417"},{"key":"e_1_2_8_13_1","doi-asserted-by":"publisher","DOI":"10.1093\/plphys\/kiad527"},{"key":"e_1_2_8_14_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.plaphy.2011.10.013"},{"key":"e_1_2_8_15_1","doi-asserted-by":"publisher","DOI":"10.1007\/s00018-008-8588-y"},{"key":"e_1_2_8_16_1","doi-asserted-by":"publisher","DOI":"10.1111\/tpj.13249"},{"key":"e_1_2_8_17_1","doi-asserted-by":"publisher","DOI":"10.1093\/hr\/uhae366"},{"key":"e_1_2_8_18_1","doi-asserted-by":"publisher","DOI":"10.1093\/plphys\/kiae130"},{"key":"e_1_2_8_19_1","doi-asserted-by":"publisher","DOI":"10.3390\/ijms25147635"},{"key":"e_1_2_8_20_1","doi-asserted-by":"publisher","DOI":"10.1038\/s41598-019-44681-7"},{"key":"e_1_2_8_21_1","doi-asserted-by":"publisher","DOI":"10.1111\/j.1365-313X.2008.03622.x"},{"key":"e_1_2_8_22_1","doi-asserted-by":"publisher","DOI":"10.1038\/s41477-018-0224-8"},{"key":"e_1_2_8_23_1","doi-asserted-by":"publisher","DOI":"10.1007\/s11103-018-0703-3"},{"key":"e_1_2_8_24_1","doi-asserted-by":"publisher","DOI":"10.1186\/1471-2229-12-219"},{"key":"e_1_2_8_25_1","doi-asserted-by":"publisher","DOI":"10.1038\/srep31772"},{"key":"e_1_2_8_26_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.foodres.2022.111107"},{"key":"e_1_2_8_27_1","doi-asserted-by":"publisher","DOI":"10.1104\/pp.107.108779"},{"key":"e_1_2_8_28_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.cbi.2012.11.009"},{"key":"e_1_2_8_29_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.phytochem.2021.113080"},{"key":"e_1_2_8_30_1","doi-asserted-by":"publisher","DOI":"10.1177\/1934578X1701200502"},{"key":"e_1_2_8_31_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.envexpbot.2015.12.012"},{"key":"e_1_2_8_32_1","doi-asserted-by":"publisher","DOI":"10.2135\/cropsci2002.1081"},{"key":"e_1_2_8_33_1","doi-asserted-by":"publisher","DOI":"10.1104\/pp.104.053298"},{"key":"e_1_2_8_34_1","doi-asserted-by":"publisher","DOI":"10.1080\/15592324.2015.1011951"},{"key":"e_1_2_8_35_1","doi-asserted-by":"publisher","DOI":"10.3389\/fpls.2023.1165687"},{"key":"e_1_2_8_36_1","doi-asserted-by":"publisher","DOI":"10.3390\/pharmaceutics15010249"},{"key":"e_1_2_8_37_1","doi-asserted-by":"publisher","DOI":"10.1111\/tpj.15494"},{"key":"e_1_2_8_38_1","doi-asserted-by":"publisher","DOI":"10.3390\/ijms21197142"},{"key":"e_1_2_8_39_1","doi-asserted-by":"publisher","DOI":"10.1111\/j.1365-3040.2012.02573.x"},{"key":"e_1_2_8_40_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.jplph.2021.153373"},{"key":"e_1_2_8_41_1","doi-asserted-by":"publisher","DOI":"10.1038\/s41477-020-00831-8"},{"key":"e_1_2_8_42_1","doi-asserted-by":"publisher","DOI":"10.1104\/pp.112.198150"},{"key":"e_1_2_8_43_1","doi-asserted-by":"publisher","DOI":"10.1038\/s41586-024-07100-0"},{"key":"e_1_2_8_44_1","doi-asserted-by":"publisher","DOI":"10.1111\/pce.14020"},{"key":"e_1_2_8_45_1","doi-asserted-by":"publisher","DOI":"10.1111\/pce.12559"},{"key":"e_1_2_8_46_1","doi-asserted-by":"publisher","DOI":"10.3389\/fpls.2017.00824"},{"key":"e_1_2_8_47_1","doi-asserted-by":"publisher","DOI":"10.1186\/s12870-014-0327-y"},{"key":"e_1_2_8_48_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.hpj.2022.09.002"},{"key":"e_1_2_8_49_1","doi-asserted-by":"publisher","DOI":"10.1093\/plphys\/kiad313"},{"key":"e_1_2_8_50_1","doi-asserted-by":"publisher","DOI":"10.1093\/plphys\/kiad362"},{"key":"e_1_2_8_51_1","doi-asserted-by":"publisher","DOI":"10.1007\/s11103-014-0220-y"},{"key":"e_1_2_8_52_1","doi-asserted-by":"publisher","DOI":"10.3390\/ijms22179498"},{"key":"e_1_2_8_53_1","doi-asserted-by":"publisher","DOI":"10.1093\/plphys\/kiac311"},{"key":"e_1_2_8_54_1","doi-asserted-by":"publisher","DOI":"10.1093\/jxb\/erac073"},{"key":"e_1_2_8_55_1","doi-asserted-by":"publisher","DOI":"10.1111\/pce.14686"},{"key":"e_1_2_8_56_1","doi-asserted-by":"publisher","DOI":"10.1007\/s00425-011-1416-x"},{"key":"e_1_2_8_57_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.jprot.2019.04.017"},{"key":"e_1_2_8_58_1","doi-asserted-by":"publisher","DOI":"10.1111\/mpp.13144"},{"key":"e_1_2_8_59_1","doi-asserted-by":"publisher","DOI":"10.1111\/pbi.14297"},{"key":"e_1_2_8_60_1","doi-asserted-by":"publisher","DOI":"10.1111\/nph.17812"},{"key":"e_1_2_8_61_1","doi-asserted-by":"publisher","DOI":"10.1111\/pce.13114"},{"key":"e_1_2_8_62_1","doi-asserted-by":"publisher","DOI":"10.1111\/ppl.12019"}],"container-title":["Plant Biotechnology Journal"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/onlinelibrary.wiley.com\/doi\/pdf\/10.1111\/pbi.70372","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/onlinelibrary.wiley.com\/doi\/full-xml\/10.1111\/pbi.70372","content-type":"application\/xml","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/onlinelibrary.wiley.com\/doi\/pdf\/10.1111\/pbi.70372","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2026,3,8]],"date-time":"2026-03-08T20:50:23Z","timestamp":1773003023000},"score":1,"resource":{"primary":{"URL":"https:\/\/onlinelibrary.wiley.com\/doi\/10.1111\/pbi.70372"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2025,10,13]]},"references-count":61,"journal-issue":{"issue":"3","published-print":{"date-parts":[[2026,3]]}},"alternative-id":["10.1111\/pbi.70372"],"URL":"https:\/\/doi.org\/10.1111\/pbi.70372","archive":["Portico"],"relation":{},"ISSN":["1467-7644","1467-7652"],"issn-type":[{"value":"1467-7644","type":"print"},{"value":"1467-7652","type":"electronic"}],"subject":[],"published":{"date-parts":[[2025,10,13]]},"assertion":[{"value":"2025-05-04","order":0,"name":"received","label":"Received","group":{"name":"publication_history","label":"Publication History"}},{"value":"2025-08-15","order":2,"name":"accepted","label":"Accepted","group":{"name":"publication_history","label":"Publication History"}},{"value":"2025-10-13","order":3,"name":"published","label":"Published","group":{"name":"publication_history","label":"Publication History"}}]}}