{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,23]],"date-time":"2026-10-23T19:44:22Z","timestamp":1792784662245,"version":"4.5.0"},"reference-count":89,"publisher":"American Chemical Society (ACS)","issue":"37","license":[{"start":{"date-parts":[[2026,7,29]],"date-time":"2026-07-29T00:00:00Z","timestamp":1785283200000},"content-version":"stm-asf","delay-in-days":0,"URL":"https:\/\/doi.org\/10.15223\/policy-029"},{"start":{"date-parts":[[2026,7,29]],"date-time":"2026-07-29T00:00:00Z","timestamp":1785283200000},"content-version":"stm-asf","delay-in-days":0,"URL":"https:\/\/doi.org\/10.15223\/policy-037"},{"start":{"date-parts":[[2026,7,29]],"date-time":"2026-07-29T00:00:00Z","timestamp":1785283200000},"content-version":"stm-asf","delay-in-days":0,"URL":"https:\/\/doi.org\/10.15223\/policy-045"}],"funder":[{"DOI":"10.13039\/501100003787","name":"Natural Science Foundation of Hebei Province","doi-asserted-by":"publisher","award":["C2026209034"],"award-info":[{"award-number":["C2026209034"]}],"id":[{"id":"10.13039\/501100003787","id-type":"DOI","asserted-by":"publisher"}]},{"name":"Tangshan Science and Technology Plan Project","award":["25150203E"],"award-info":[{"award-number":["25150203E"]}]},{"name":"North China University of Science and Technology","award":["QNTJ202308"],"award-info":[{"award-number":["QNTJ202308"]}],"id":[{"id":"https:\/\/ror.org\/04z4wmb81","id-type":"ROR","asserted-by":"crossref"}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":[],"published-print":{"date-parts":[[2026,9,23]]},"abstract":"<jats:title>Abstract<\/jats:title>\n                  <jats:p>MATH domain-containing proteins are important for plant growth, development, and stress adaptation, but their evolution and cold resistance in Brassica napus remain unexplored. Here, we characterized MATH genes in B. napus, Brassica rapa, Brassica oleracea, and Arabidopsis thaliana. We identified 461 MATH genes. Microcollinearity and pan-genomic analyses revealed stable syntenic gene numbers, purifying selection, and conserved evolution. The MATH family experienced ancient duplications, showing weak codon bias and reduced functional redundancy. Type A and D MATH genes exhibited low expression in root and leaf tissues, whereas type B and C genes showed high expression. RT-qPCR confirmed their roles in the cold stress response. Duplicated genes underwent defunctionalization or subfunctionalization. Subcellular localization showed that BnaA04g13830D and BnaC09g03690D were localized to the plasma membrane. Overexpression of BnaA04g13830D and BnaC09g03690D in Arabidopsis enhanced cold tolerance, potentially by influencing C-repeat binding factor signaling genes. This study provides insights into the evolutionary patterns and functions of the MATH gene families.<\/jats:p>","DOI":"10.1021\/acs.jafc.5c17599","type":"journal-article","created":{"date-parts":[[2026,8,4]],"date-time":"2026-08-04T13:17:18Z","timestamp":1785849438000},"page":"29624-29645","source":"Crossref","is-referenced-by-count":0,"title":["Evolutionary Patterns\nand Functional Analysis of MATH\nGenes: Insights into Cold Tolerance Mechanisms in Oilseed Rape (\n                    <i>Brassica napus<\/i>\n                    )"],"prefix":"10.1021","volume":"74","author":[{"given":"Yingchao","family":"Zhang","sequence":"first","affiliation":[{"name":"North China University of Science and Technology , , , ,","place":["Tangshan, Hebei, China, 063210"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jianbin","family":"Quan","sequence":"additional","affiliation":[{"name":"North China University of Science and Technology , , , ,","place":["Tangshan, Hebei, China, 063210"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Bingyu","family":"Han","sequence":"additional","affiliation":[{"name":"North China University of Science and Technology , , , ,","place":["Tangshan, Hebei, China, 063210"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Shuyan","family":"Feng","sequence":"additional","affiliation":[{"name":"North China University of Science and Technology , , , ,","place":["Tangshan, Hebei, China, 063210"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Yihan","family":"Dong","sequence":"additional","affiliation":[{"name":"North China University of Science and Technology , , , ,","place":["Tangshan, Hebei, China, 063210"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Yahui","family":"Zhao","sequence":"additional","affiliation":[{"name":"North China University of Science and Technology , , , ,","place":["Tangshan, Hebei, China, 063210"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Xiaoming","family":"Song","sequence":"additional","affiliation":[{"name":"North China University of Science and Technology , , , ,","place":["Tangshan, Hebei, China, 063210"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-2186-3334","authenticated-orcid":true,"given":"Huilong","family":"Chen","sequence":"additional","affiliation":[{"name":"China Agricultural University , , ,","place":["Beijing, China, 100193"]}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"316","published-online":{"date-parts":[[2026,7,29]]},"reference":[{"key":"2026092310082534300_cit1","doi-asserted-by":"crossref","unstructured":"Zapata, J. M.; Marti\u0301nez-Garci\u0301a, V.; Lefebvre, S.\n          Phylogeny\nof the TRAF\/MATH Domain, TNF Receptor Associated Factors\n(TRAFs), 2007; pp 1\u201324.","DOI":"10.1007\/978-0-387-70630-6_1"},{"issue":"16","key":"2026092310082534300_cit2","doi-asserted-by":"publisher","first-page":"13248","DOI":"10.1074\/jbc.M011414200","article-title":"Marked differences\nbetween metalloproteases meprin A and B in substrate and peptide bond\nspecificity","volume":"276","author":"Bertenshaw","year":"2001","journal-title":"J. Biol. Chem."},{"issue":"1","key":"2026092310082534300_cit3","doi-asserted-by":"publisher","first-page":"222","DOI":"10.1104\/pp.110.155754","article-title":"RTM3, which controls\nlong-distance movement of potyviruses, is a member of a new plant\ngene family encoding a meprin and TRAF homology domain-containing\nprotein","volume":"154","author":"Cosson","year":"2010","journal-title":"Plant Physiol."},{"issue":"7","key":"2026092310082534300_cit4","doi-asserted-by":"publisher","first-page":"1247","DOI":"10.1002\/pro.5560040701","article-title":"The astacin family of metalloendopeptidases","volume":"4","author":"Bond","year":"1995","journal-title":"Protein Sci."},{"issue":"4","key":"2026092310082534300_cit5","doi-asserted-by":"publisher","first-page":"679","DOI":"10.1242\/jcs.115.4.679","article-title":"All TRAFs are not created\nequal: common and distinct molecular mechanisms of TRAF-mediated signal\ntransduction","volume":"115","author":"Chung","year":"2002","journal-title":"J. Cell Sci."},{"issue":"44","key":"2026092310082534300_cit6","doi-asserted-by":"publisher","first-page":"6482","DOI":"10.1038\/sj.onc.1204788","article-title":"Tumor necrosis factor receptor-associated\nfactors (TRAFs)","volume":"20","author":"Bradley","year":"2001","journal-title":"Oncogene"},{"issue":"46","key":"2026092310082534300_cit7","doi-asserted-by":"publisher","first-page":"45382","DOI":"10.1074\/jbc.M306708200","article-title":"Tumor necrosis\nfactor\nreceptor-associated factor 2 (TRAF2)-deficient B lymphocytes reveal\nnovel roles for TRAF2 in CD40 signaling","volume":"278","author":"Hostager","year":"2003","journal-title":"J.\nBiol. Chem."},{"issue":"7","key":"2026092310082534300_cit8","doi-asserted-by":"publisher","first-page":"244","DOI":"10.1016\/s0968-0004(96)30022-4","article-title":"TRAF protiens\nand meprins share a conserved domain","volume":"21","author":"Uren","year":"1996","journal-title":"Trends\nBiochem. Sci."},{"issue":"10","key":"2026092310082534300_cit9","doi-asserted-by":"publisher","first-page":"8782","DOI":"10.3390\/ijms24108782","article-title":"Evolution\nand expression of the meprin and TRAF homology domain-containing\nGene Family in Solanaceae","volume":"24","author":"Dai","year":"2023","journal-title":"Int. J. Mol. Sci."},{"issue":"1","key":"2026092310082534300_cit10","doi-asserted-by":"publisher","first-page":"163","DOI":"10.1111\/j.1538-7836.2010.04091.x","article-title":"TNF receptor-associated\nfactor 4\n(TRAF4) is a novel binding partner of glycoprotein Ib and glycoprotein\nVI in human platelets","volume":"9","author":"Arthur","year":"2011","journal-title":"J. Thromb. Haemostasis"},{"issue":"3","key":"2026092310082534300_cit11","doi-asserted-by":"publisher","first-page":"321","DOI":"10.1016\/S1097-2765(00)80334-2","article-title":"The structural\nbasis for the recognition of diverse receptor sequences by TRAF2","volume":"4","author":"Ye","year":"1999","journal-title":"Mol. Cell"},{"issue":"1","key":"2026092310082534300_cit12","doi-asserted-by":"publisher","first-page":"361","DOI":"10.1016\/j.fsi.2010.11.012","article-title":"Molecular\ncloning, characterization and expression analysis of TLR9, MyD88 and\nTRAF6 genes in common carp (Cyprinus carpio)","volume":"30","author":"Kongchum","year":"2011","journal-title":"Fish Shellfish Immunol."},{"issue":"12","key":"2026092310082534300_cit13","doi-asserted-by":"publisher","first-page":"4974","DOI":"10.1105\/tpc.112.107169","article-title":"Germline-specific MATH-BTB substrate\nadaptor MAB1 regulates spindle length and nuclei identity in maize","volume":"24","author":"Juranic\u0301","year":"2013","journal-title":"Plant Cell"},{"issue":"3","key":"2026092310082534300_cit14","doi-asserted-by":"publisher","first-page":"214","DOI":"10.2174\/1389202911314030007","article-title":"Phylogenetic analysis of Brassica rapa MATH-domain\nproteins","volume":"14","author":"Zhao","year":"2013","journal-title":"Curr. Genomics"},{"issue":"5","key":"2026092310082534300_cit15","doi-asserted-by":"publisher","first-page":"79","DOI":"10.1007\/s11738-020-03070-8","article-title":"Molecular\nand biochemical analyses of a novel lectin\nwith MATH domains from Brassica oleracea","volume":"42","author":"Duarte","year":"2020","journal-title":"Acta\nPhysiol. Plant."},{"issue":"2","key":"2026092310082534300_cit16","doi-asserted-by":"publisher","first-page":"152","DOI":"10.1111\/j.1399-3054.2005.00505.x","article-title":"MATH domain proteins\nrepresent a novel protein family in Arabidopsis thaliana, and at least\none member is modified in roots during the course of a plant\u2013microbe\ninteraction","volume":"124","author":"Oelmu\u0308ller","year":"2005","journal-title":"Physiol. Plant."},{"issue":"6986","key":"2026092310082534300_cit17","doi-asserted-by":"publisher","first-page":"945","DOI":"10.1038\/nature02516","article-title":"Regulation of ethylene\ngas biosynthesis by the Arabidopsis ETO1 protein","volume":"428","author":"Wang","year":"2004","journal-title":"Nature"},{"issue":"6","key":"2026092310082534300_cit18","doi-asserted-by":"publisher","first-page":"1116","DOI":"10.1016\/j.devcel.2011.10.018","article-title":"MATH\/BTB CRL3\nreceptors target the homeodomain-leucine zipper ATHB6 to modulate\nabscisic acid signaling","volume":"21","author":"Lechner","year":"2011","journal-title":"Dev. Cell"},{"issue":"5","key":"2026092310082534300_cit19","doi-asserted-by":"publisher","first-page":"1214","DOI":"10.1111\/jipb.13842","article-title":"Generation of novel\nbpm6 and dmr6 mutants with broad-spectrum resistance\nusing a modified CRISPR\/Cas9 system in Brassica oleracea","volume":"67","author":"Zhang","year":"2025","journal-title":"J. Integr. Plant Biol."},{"issue":"1","key":"2026092310082534300_cit20","doi-asserted-by":"publisher","first-page":"83","DOI":"10.1104\/pp.104.052654","article-title":"Arabidopsis AtCUL3a\nand AtCUL3b form complexes with members of the BTB\/POZ-MATH protein\nfamily","volume":"137","author":"Weber","year":"2005","journal-title":"Plant Physiol."},{"key":"2026092310082534300_cit21","doi-asserted-by":"publisher","first-page":"923","DOI":"10.3389\/fpls.2016.00923","article-title":"MATH-domain\nfamily shows response toward abiotic stress in Arabidopsis and rice","volume":"7","author":"Kushwaha","year":"2016","journal-title":"Front. 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Plant Biol."},{"key":"2026092310082534300_cit25","doi-asserted-by":"publisher","first-page":"1788","DOI":"10.3389\/fpls.2017.01788","article-title":"Current status\nand challenges in\nidentifying disease resistance genes in Brassica napus","volume":"8","author":"Neik","year":"2017","journal-title":"Front. Plant Sci."},{"issue":"4","key":"2026092310082534300_cit26","doi-asserted-by":"publisher","first-page":"4159","DOI":"10.1104\/pp.104.052142","article-title":"Exploring the temperature-stress\nmetabolome of Arabidopsis","volume":"136","author":"Kaplan","year":"2004","journal-title":"Plant Physiol."},{"issue":"10","key":"2026092310082534300_cit27","doi-asserted-by":"publisher","first-page":"444","DOI":"10.1016\/j.tplants.2007.07.002","article-title":"Cold stress\nregulation of gene expression in plants","volume":"12","author":"Chinnusamy","year":"2007","journal-title":"Trends\nPlant Sci."},{"key":"2026092310082534300_cit28","unstructured":"Zhang XueKun, Z. X.; Zhang ChunLei, Z. C.; Liao Xin, L. X.; Wang HaiZhong, W. H.\n          Investigation\non 2008 Low Temperature and Freeze Injury on Winter Rape Along Yangtze\nRiver, 2008."},{"issue":"2","key":"2026092310082534300_cit29","doi-asserted-by":"publisher","first-page":"431","DOI":"10.1111\/jipb.13182","article-title":"TRAF proteins as key\nregulators of plant development and stress responses","volume":"64","author":"Qi","year":"2022","journal-title":"J. Integr. Plant Biol."},{"issue":"1","key":"2026092310082534300_cit30","doi-asserted-by":"publisher","first-page":"226","DOI":"10.1093\/plphys\/kiac266","article-title":"The Brassicaceae\ngenome resource (TBGR): A comprehensive genome platform for Brassicaceae\nplants","volume":"190","author":"Liu","year":"2022","journal-title":"Plant Physiol."},{"issue":"D1","key":"2026092310082534300_cit31","doi-asserted-by":"publisher","first-page":"D1202","DOI":"10.1093\/nar\/gkr1090","article-title":"The Arabidopsis Information\nResource (TAIR): improved gene annotation and new tools","volume":"40","author":"Lamesch","year":"2012","journal-title":"Nucleic Acids Res."},{"issue":"W1","key":"2026092310082534300_cit32","doi-asserted-by":"publisher","first-page":"W200","DOI":"10.1093\/nar\/gky448","article-title":"HMMER web server: 2018 update","volume":"46","author":"Potter","year":"2018","journal-title":"Nucleic Acids Res."},{"key":"2026092310082534300_cit33","doi-asserted-by":"publisher","first-page":"421","DOI":"10.1186\/1471-2105-10-421","article-title":"BLAST+: architecture and applications","volume":"10","author":"Camacho","year":"2009","journal-title":"BMC Bioinf."},{"issue":"D1","key":"2026092310082534300_cit34","doi-asserted-by":"publisher","first-page":"D222","DOI":"10.1093\/nar\/gku1221","article-title":"CDD: NCBI\u2019s conserved domain database","volume":"43","author":"Marchler-Bauer","year":"2015","journal-title":"Nucleic Acids Res."},{"issue":"D1","key":"2026092310082534300_cit35","doi-asserted-by":"publisher","first-page":"D458","DOI":"10.1093\/nar\/gkaa937","article-title":"SMART: recent updates, new developments\nand status in 2020","volume":"49","author":"Letunic","year":"2021","journal-title":"Nucleic Acids Res."},{"issue":"11","key":"2026092310082534300_cit36","doi-asserted-by":"publisher","first-page":"1733","DOI":"10.1016\/j.molp.2023.09.010","article-title":"TBtools-II:\nA \u201cone for all, all for one\u201d bioinformatics platform\nfor biological big-data mining","volume":"16","author":"Chen","year":"2023","journal-title":"Mol. Plant"},{"issue":"3","key":"2026092310082534300_cit37","doi-asserted-by":"publisher","first-page":"643","DOI":"10.1002\/prot.21018","article-title":"Prediction of protein\nsubcellular localization","volume":"64","author":"Yu","year":"2006","journal-title":"Proteins: Struct.,\nFunct., Bioinf."},{"issue":"6","key":"2026092310082534300_cit38","doi-asserted-by":"publisher","DOI":"10.1371\/journal.pone.0011335","article-title":"Plant-mPLoc: a top-down strategy to augment the power\nfor predicting plant protein subcellular localization","volume":"5","author":"Chou","year":"2010","journal-title":"PLoS One"},{"issue":"Web Server","key":"2026092310082534300_cit39","doi-asserted-by":"publisher","first-page":"W585","DOI":"10.1093\/nar\/gkm259","article-title":"WoLF PSORT: protein\nlocalization\npredictor","volume":"35","author":"Horton","year":"2007","journal-title":"Nucleic Acids Res."},{"issue":"5","key":"2026092310082534300_cit40","doi-asserted-by":"publisher","first-page":"1530","DOI":"10.1093\/molbev\/msaa015","article-title":"IQ-TREE 2: new models and efficient\nmethods for phylogenetic inference in the genomic era","volume":"37","author":"Minh","year":"2020","journal-title":"Mol. Biol. Evol."},{"issue":"Web\nServer","key":"2026092310082534300_cit41","doi-asserted-by":"publisher","first-page":"W202","DOI":"10.1093\/nar\/gkp335","article-title":"MEME SUITE:\ntools for motif discovery and searching","volume":"37","author":"Bailey","year":"2009","journal-title":"Nucleic\nAcids Res."},{"issue":"1","key":"2026092310082534300_cit42","doi-asserted-by":"publisher","first-page":"178","DOI":"10.1186\/s12859-022-04707-w","article-title":"CFVisual:\nan interactive desktop platform for drawing gene structure and protein\narchitecture","volume":"23","author":"Chen","year":"2022","journal-title":"BMC Bioinf."},{"key":"2026092310082534300_cit43","doi-asserted-by":"publisher","first-page":"W78","DOI":"10.1093\/nar\/gkae268","article-title":"Interactive Tree of Life (iTOL) v6:\nrecent updates to the phylogenetic\ntree display and annotation tool","volume":"52","author":"Letunic","year":"2024","journal-title":"Nucleic Acids\nRes."},{"issue":"7","key":"2026092310082534300_cit44","doi-asserted-by":"publisher","DOI":"10.1093\/nar\/gkr1293","article-title":"MCScanX: a toolkit for detection and evolutionary analysis\nof gene synteny and collinearity","volume":"40","author":"Wang","year":"2012","journal-title":"Nucleic Acids\nRes."},{"issue":"10","key":"2026092310082534300_cit45","doi-asserted-by":"publisher","first-page":"1483","DOI":"10.1093\/oxfordjournals.molbev.a026248","article-title":"Comparative\nevolutionary analysis\nof chalcone synthase and alcohol dehydrogenase loci in Arabidopsis,\nArabis, and related genera (Brassicaceae)","volume":"17","author":"Koch","year":"2000","journal-title":"Mol.\nBiol. Evol."},{"issue":"6","key":"2026092310082534300_cit46","doi-asserted-by":"publisher","first-page":"1278","DOI":"10.1105\/tpc.17.00312","article-title":"Phylogenomic synteny network analysis\nof MADS-box transcription factor genes reveals lineage-specific transpositions,\nancient tandem duplications, and deep positional conservation","volume":"29","author":"Zhao","year":"2017","journal-title":"Plant Cell"},{"issue":"6","key":"2026092310082534300_cit47","doi-asserted-by":"publisher","first-page":"2165","DOI":"10.1073\/pnas.1801757116","article-title":"Network-based microsynteny analysis identifies major\ndifferences and genomic outliers in mammalian and angiosperm genomes","volume":"116","author":"Zhao","year":"2019","journal-title":"Proc. Natl. Acad. Sci. U.S.A."},{"issue":"7043","key":"2026092310082534300_cit48","doi-asserted-by":"publisher","first-page":"814","DOI":"10.1038\/nature03607","article-title":"Uncovering the overlapping\ncommunity structure of complex networks in nature and society","volume":"435","author":"Palla","year":"2005","journal-title":"Nature"},{"issue":"11","key":"2026092310082534300_cit49","doi-asserted-by":"publisher","first-page":"2498","DOI":"10.1101\/gr.1239303","article-title":"Cytoscape: a software environment for integrated models\nof biomolecular interaction networks","volume":"13","author":"Shannon","year":"2003","journal-title":"Genome\nRes."},{"issue":"5","key":"2026092310082534300_cit50","doi-asserted-by":"publisher","first-page":"1506","DOI":"10.1111\/nph.16445","article-title":"Evolutionary strategies\ndrive a balance of the interacting gene products for the CBL and CIPK\ngene families","volume":"226","author":"Zhang","year":"2020","journal-title":"New Phytol."},{"issue":"D1","key":"2026092310082534300_cit51","doi-asserted-by":"publisher","first-page":"D1432","DOI":"10.1093\/nar\/gkab1057","article-title":"BRAD V3. 0:\nan upgraded Brassicaceae database","volume":"50","author":"Chen","year":"2022","journal-title":"Nucleic Acids\nRes."},{"key":"2026092310082534300_cit52","doi-asserted-by":"publisher","first-page":"198","DOI":"10.3389\/fpls.2012.00198","article-title":"Syntenic gene analysis between Brassica\nrapa and other Brassicaceae species","volume":"3","author":"Cheng","year":"2012","journal-title":"Front.\nPlant Sci."},{"key":"2026092310082534300_cit53","doi-asserted-by":"publisher","first-page":"uhac035","DOI":"10.1093\/hr\/uhac035","article-title":"Large-scale analyses of heat shock transcription factors and database\nconstruction based on whole-genome genes in horticultural and representative\nplants","volume":"9","author":"Yu","year":"2022","journal-title":"Hortic. Res."},{"key":"2026092310082534300_cit54","doi-asserted-by":"publisher","first-page":"38","DOI":"10.1186\/s13059-019-1650-2","article-title":"Gene duplication\nand evolution in\nrecurring polyploidization\u2013diploidization cycles in plants","volume":"20","author":"Qiao","year":"2019","journal-title":"Genome Biol."},{"issue":"4","key":"2026092310082534300_cit55","doi-asserted-by":"publisher","first-page":"557","DOI":"10.1111\/tpj.12313","article-title":"The sacred lotus genome\nprovides insights into the evolution of flowering\nplants","volume":"76","author":"Wang","year":"2013","journal-title":"Plant J."},{"key":"2026092310082534300_cit56","doi-asserted-by":"publisher","first-page":"112484","DOI":"10.1016\/j.scienta.2023.112484","article-title":"Two major duplication events shaped the transcription factor repertoires\nin Solanaceae species","volume":"323","author":"Song","year":"2024","journal-title":"Sci. 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