{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,3,9]],"date-time":"2026-03-09T06:24:59Z","timestamp":1773037499072,"version":"3.50.1"},"reference-count":43,"publisher":"MDPI AG","issue":"4","license":[{"start":{"date-parts":[[2016,3,24]],"date-time":"2016-03-24T00:00:00Z","timestamp":1458777600000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"name":"the China Agriculture Research System","award":["CARS-32-11"],"award-info":[{"award-number":["CARS-32-11"]}]},{"name":"the Key Agricultural Science and Technology Project of Fujian Province, China","award":["2015NZ0002-1"],"award-info":[{"award-number":["2015NZ0002-1"]}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["IJMS"],"abstract":"<jats:p>Copper\/zinc superoxide dismutases (Cu\/ZnSODs) play important roles in improving banana resistance to adverse conditions, but their activities depend on the copper chaperone for superoxide dismutase (CCS) delivering copper to them. However, little is known about CCS in monocots and under stress conditions. Here, a novel CCS gene (MaCCS) was obtained from a banana using reverse transcription PCR and rapid-amplification of cDNA ends (RACE) PCR. Sequence analyses showed that MaCCS has typical CCS domains and a conserved gene structure like other plant CCSs. Alternative transcription start sites (ATSSs) and alternative polyadenylation contribute to the mRNA diversity of MaCCS. ATSSs in MaCCS resulted in one open reading frame containing two in-frame start codons to form two protein versions, which is supported by the MaCCS subcellular localization of in both cytosol and chloroplasts. Furthermore, MaCCS promoter was found to contain many cis-elements associated with abiotic and hormonal responses. Quantitative real-time PCR analysis showed that MaCCS was expressed in all tested tissues (leaves, pseudostems and roots). In addition, MaCCS expression was significantly induced by light, heat, drought, abscisic acid and indole-3-acetic acid, but inhibited by relatively high concentrations of CuSO4 and under cold treatment, which suggests that MaCCS is involved in abiotic and hormonal responses.<\/jats:p>","DOI":"10.3390\/ijms17040441","type":"journal-article","created":{"date-parts":[[2016,3,24]],"date-time":"2016-03-24T11:55:16Z","timestamp":1458820516000},"page":"441","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":18,"title":["Molecular Characterization of MaCCS, a Novel Copper Chaperone Gene Involved in Abiotic and Hormonal Stress Responses in Musa acuminata cv. Tianbaojiao"],"prefix":"10.3390","volume":"17","author":[{"given":"Xin","family":"Feng","sequence":"first","affiliation":[{"name":"Institute of Horticultural Biotechnology, Fujian Agriculture and Forestry University, Fuzhou 350002, China"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Fanglan","family":"Chen","sequence":"additional","affiliation":[{"name":"Institute of Horticultural Biotechnology, Fujian Agriculture and Forestry University, Fuzhou 350002, China"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Weihua","family":"Liu","sequence":"additional","affiliation":[{"name":"Institute of Horticultural Biotechnology, Fujian Agriculture and Forestry University, Fuzhou 350002, China"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Min","family":"Thu","sequence":"additional","affiliation":[{"name":"Institute of Horticultural Biotechnology, Fujian Agriculture and Forestry University, Fuzhou 350002, China"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Zihao","family":"Zhang","sequence":"additional","affiliation":[{"name":"Institute of Horticultural Biotechnology, Fujian Agriculture and Forestry University, Fuzhou 350002, China"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-9490-4435","authenticated-orcid":false,"given":"Yukun","family":"Chen","sequence":"additional","affiliation":[{"name":"Institute of Horticultural Biotechnology, Fujian Agriculture and Forestry University, Fuzhou 350002, China"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Chunzhen","family":"Cheng","sequence":"additional","affiliation":[{"name":"Institute of Horticultural Biotechnology, Fujian Agriculture and Forestry University, Fuzhou 350002, China"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Yuling","family":"Lin","sequence":"additional","affiliation":[{"name":"Institute of Horticultural Biotechnology, Fujian Agriculture and Forestry University, Fuzhou 350002, China"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Tianchi","family":"Wang","sequence":"additional","affiliation":[{"name":"Institute of Horticultural Biotechnology, Fujian Agriculture and Forestry University, Fuzhou 350002, China"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Zhongxiong","family":"Lai","sequence":"additional","affiliation":[{"name":"Institute of Horticultural Biotechnology, Fujian Agriculture and Forestry University, Fuzhou 350002, China"}],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"1968","published-online":{"date-parts":[[2016,3,24]]},"reference":[{"key":"ref_1","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_2","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_3","doi-asserted-by":"crossref","first-page":"637","DOI":"10.1104\/pp.118.2.637","article-title":"Superoxide dismutase in Arabidopsis: An eclectic enzyme family with disparate regulation and protein localization","volume":"118","author":"Kliebenstein","year":"1998","journal-title":"Plant Physiol."},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"2645","DOI":"10.1016\/S0021-9258(19)44055-6","article-title":"On the stability of bovine superoxide dismutase: The effects of metals","volume":"248","author":"Forman","year":"1973","journal-title":"J. Biol. Chem."},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"805","DOI":"10.1126\/science.284.5415.805","article-title":"Undetectable intracellular free copper: The requirement of a copper chaperone for superoxide dismutase","volume":"284","author":"Rae","year":"1999","journal-title":"Science"},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"537","DOI":"10.1146\/annurev-biochem-030409-143539","article-title":"Copper metallochaperones","volume":"79","author":"Robinson","year":"2010","journal-title":"Annu. Revi. Biochem."},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"425","DOI":"10.1104\/pp.105.065284","article-title":"A copper chaperone for superoxide dismutase that confers three types of copper\/zinc superoxide dismutase activity in Arabidopsis","volume":"139","author":"Chu","year":"2005","journal-title":"Plant Physiol."},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"5413","DOI":"10.1021\/bi992727+","article-title":"Cobalt(2+) binding to human and tomato copper chaperone for superoxide dismutase: Implications for the metal ion transfer mechanism","volume":"39","author":"Zhu","year":"2000","journal-title":"Biochemistry"},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"618","DOI":"10.1104\/pp.103.025320","article-title":"Isolation of a gene encoding a copper chaperone for the copper\/zinc superoxide dismutase and characterization of its promoter in potato","volume":"133","author":"Trindade","year":"2003","journal-title":"Plant Physiol."},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"351","DOI":"10.3724\/SP.J.1145.2012.00351","article-title":"Cloning of copper chaperone for superoxide dismutase gene CCS from embryogenic dallus of Dimocarpus longan Lour. and its expression analysis during somatic embryogenesis","volume":"18","author":"Lin","year":"2012","journal-title":"Chin. J. Appl. Environ. Biol."},{"key":"ref_11","doi-asserted-by":"crossref","unstructured":"Molina-Rueda, J.J., Tsai, C.J., and Kirby, E.G. (2013). The populus superoxide dismutase gene family and its responses to drought stress in transgenic poplar overexpressing a pine cytosolic glutamine synthetase (GS1a). PLOS ONE, 8.","DOI":"10.1371\/journal.pone.0056421"},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"144","DOI":"10.1071\/FP13134","article-title":"Regulation of the chloroplastic copper chaperone (CCS) and cuprozinc superoxide dismutase (CSD2) by alternative splicing and copper excess in Glycine max","volume":"41","author":"Sagasti","year":"2014","journal-title":"Funct. Plant Biol."},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"823","DOI":"10.1186\/s12864-015-2046-7","article-title":"Genome-wide identification and characterization of the superoxide dismutase gene family in Musa acuminata cv. Tianbaojiao (AAA group)","volume":"16","author":"Feng","year":"2015","journal-title":"BMC Genom."},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"23","DOI":"10.3389\/fpls.2015.00023","article-title":"Overexpression of copper\/zinc superoxide dismutase from mangrove Kandelia candel in tobacco enhances salinity tolerance by the reduction of reactive oxygen species in chloroplast","volume":"6","author":"Jing","year":"2015","journal-title":"Front. Plant Sci."},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"1109","DOI":"10.1007\/s00299-015-1770-4","article-title":"Overexpression of Cu\/ZnSOD from Arachis hypogaea alleviates salinity and drought stress in tobacco","volume":"34","author":"Negi","year":"2015","journal-title":"Plant Cell Rep."},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"213","DOI":"10.1038\/nature11241","article-title":"The banana (Musa acuminata) genome and the evolution of monocotyledonous plants","volume":"488","author":"Denoeud","year":"2012","journal-title":"Nature"},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"683","DOI":"10.1186\/1471-2164-14-683","article-title":"A draft Musa balbisiana genome sequence for molecular genetics in polyploid, inter- and intra-specific Musa hybrids","volume":"14","author":"Davey","year":"2013","journal-title":"BMC Genom."},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"69","DOI":"10.1016\/j.gene.2012.11.048","article-title":"Structure, gene expression, and evolution of primate copper chaperone for superoxide dismutase","volume":"516","author":"Fukuhara","year":"2013","journal-title":"Gene"},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"23719","DOI":"10.1074\/jbc.274.34.23719","article-title":"Multiple protein domains contribute to the action of the copper chaperone for superoxide dismutase","volume":"274","author":"Schmidt","year":"1999","journal-title":"J. Biol. Chem."},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"33771","DOI":"10.1074\/jbc.M006254200","article-title":"Copper activation of superoxide dismutase 1 (SOD1) in vivo: Role for protein-protein interactions with the copper chaperone for SOD1","volume":"275","author":"Schmidt","year":"2000","journal-title":"J. Biol. Chem."},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"751","DOI":"10.1038\/nsb0901-751","article-title":"Heterodimeric structure of superoxide dismutase in complex with its metallochaperone","volume":"8","author":"Lamb","year":"2001","journal-title":"Nat. Struct. Biol."},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"506","DOI":"10.1016\/S0968-0004(00)89118-5","article-title":"The G-box: A ubiquitous regulatory DNA element in plants bound by the GBF family of bZIP proteins","volume":"20","author":"Menkens","year":"1995","journal-title":"Trends Biochem. Sci."},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"595","DOI":"10.1007\/s11032-013-9892-2","article-title":"Superoxide dismutase multigene family in longan somatic embryos: A comparison of CuZn-SOD, Fe-SOD, and Mn-SOD gene structure, splicing, phylogeny, and expression","volume":"32","author":"Lin","year":"2013","journal-title":"Mol. Breed."},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"741","DOI":"10.1023\/A:1005921914384","article-title":"Identification of UV\/blue light-response elements in the Arabidopsis thaliana chalcone synthase promoter using a homologous protoplast transient expression system","volume":"36","author":"Hartmann","year":"1998","journal-title":"Plant Mol. Biol."},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"1119","DOI":"10.1104\/pp.101.3.1119","article-title":"Arabidopsis DNA encoding two desiccation-responsive rd29 genes","volume":"101","author":"Shinozaki","year":"1993","journal-title":"Plant Physiol."},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"489","DOI":"10.1071\/PP9930489","article-title":"Auxin-regulated transcription","volume":"20","author":"Guilfoyle","year":"1993","journal-title":"Funct. Plant Biol."},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"5690","DOI":"10.1002\/j.1460-2075.1996.tb00953.x","article-title":"Interaction of elicitor-induced DNA-binding proteins with elicitor response elements in the promoters of parsley PR1 genes","volume":"15","author":"Rushton","year":"1996","journal-title":"EMBO J."},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"565","DOI":"10.1007\/BF00042229","article-title":"Phytohormone control of the tobacco anionic peroxidase promoter","volume":"31","author":"Klotz","year":"1996","journal-title":"Plant Mol. Biol."},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"550","DOI":"10.1007\/s00438-004-1086-5","article-title":"Genomic organization of the Neurospora crassa gsn gene: Possible involvement of the STRE and HSE elements in the modulation of transcription during heat shock","volume":"272","author":"Freitas","year":"2004","journal-title":"Mol. Genet. Genom."},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"1117","DOI":"10.1104\/pp.101.3.1117","article-title":"Nucleotide sequence of the tobacco (Nicotiana tabacum) anionic peroxidase gene","volume":"101","author":"Klotz","year":"1993","journal-title":"Plant Physiol."},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"727","DOI":"10.1104\/pp.112.2.727","article-title":"The promoter for tomato 3-hydroxy-3-methylglutaryl coenzyme A reductase gene 2 has unusual regulatory elements that direct high-level expression","volume":"112","author":"Daraselia","year":"1996","journal-title":"Plant Physiol."},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"302","DOI":"10.1111\/j.1095-8339.1955.tb00015.x","article-title":"The taxonomy and origins of the cultivated bananas","volume":"55","author":"Simmonds","year":"1955","journal-title":"J. Linn. Soc. Lond. Bot."},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"840","DOI":"10.1111\/tpj.12169","article-title":"Heat stress induction of miR398 triggers a regulatory loop that is critical for thermotolerance in Arabidopsis","volume":"74","author":"Guan","year":"2013","journal-title":"Plant J."},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"446","DOI":"10.1186\/s12864-015-1551-z","article-title":"Comparative transcriptomics analysis reveals difference of key gene expression between banana and plantain in response to cold stress","volume":"16","author":"Yang","year":"2015","journal-title":"BMC Genom."},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"454","DOI":"10.1111\/j.1365-313X.2010.04162.x","article-title":"microRNA-directed cleavage and translational repression of the copper chaperone for superoxide dismutase mRNA in Arabidopsis","volume":"62","author":"Beauclair","year":"2010","journal-title":"Plant J."},{"key":"ref_36","first-page":"509","article-title":"Development of a transgenic acceptor system for banana","volume":"35","author":"Zhang","year":"2006","journal-title":"J. Fujian Agric. For. Univ. (Nat. Sci. Ed.)"},{"key":"ref_37","doi-asserted-by":"crossref","unstructured":"Droc, G., Lariviere, D., Guignon, V., Yahiaoui, N., This, D., Garsmeur, O., Dereeper, A., Hamelin, C., Argout, X., and Dufayard, J.F. (2013). The Banana Genome Hub. Database.","DOI":"10.1093\/database\/bat035"},{"key":"ref_38","doi-asserted-by":"crossref","unstructured":"Finn, R.D., Bateman, A., Clements, J., Coggill, P., Eberhardt, R.Y., Eddy, S.R., Heger, A., Hetherington, K., Holm, L., and Mistry, J. (2013). Pfam: The protein families database. Nucleic Acids Res.","DOI":"10.1093\/nar\/gkt1223"},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"2731","DOI":"10.1093\/molbev\/msr121","article-title":"MEGA5: Molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods","volume":"28","author":"Tamura","year":"2011","journal-title":"Mol. Biol. Evol."},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"325","DOI":"10.1093\/nar\/30.1.325","article-title":"PlantCARE, a database of plant cis-acting regulatory elements and a portal to tools for in silico analysis of promoter sequences","volume":"30","author":"Lescot","year":"2002","journal-title":"Nucleic Acids Res."},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"978","DOI":"10.1110\/ps.8.5.978","article-title":"ChloroP, a neural network-based method for predicting chloroplast transit peptides and their cleavage sites","volume":"8","author":"Emanuelsson","year":"1999","journal-title":"Protein Sci."},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"481","DOI":"10.1016\/j.plaphy.2010.03.010","article-title":"A mitogen-activated protein kinase, AhMPK6 from peanut localizes to the nucleus and also induces defense responses upon transient expression in tobacco","volume":"48","author":"Kumar","year":"2010","journal-title":"Plant Physiol. Biochem."},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"377","DOI":"10.1007\/s00425-011-1410-3","article-title":"Validation of reference genes for RT-qPCR studies of gene expression in banana fruit under different experimental conditions","volume":"234","author":"Chen","year":"2011","journal-title":"Planta"}],"container-title":["International Journal of Molecular Sciences"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/1422-0067\/17\/4\/441\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,11]],"date-time":"2025-10-11T19:21:12Z","timestamp":1760210472000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/1422-0067\/17\/4\/441"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2016,3,24]]},"references-count":43,"journal-issue":{"issue":"4","published-online":{"date-parts":[[2016,4]]}},"alternative-id":["ijms17040441"],"URL":"https:\/\/doi.org\/10.3390\/ijms17040441","relation":{},"ISSN":["1422-0067"],"issn-type":[{"value":"1422-0067","type":"electronic"}],"subject":[],"published":{"date-parts":[[2016,3,24]]}}}