{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,22]],"date-time":"2026-09-22T08:22:17Z","timestamp":1790065337860,"version":"4.0.1"},"reference-count":54,"publisher":"MDPI AG","issue":"2","license":[{"start":{"date-parts":[[2017,1,30]],"date-time":"2017-01-30T00:00:00Z","timestamp":1485734400000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["IJMS"],"abstract":"<jats:p>Laccases are encoded by a multigene family and widely distributed in plant genomes where they play roles oxidizing monolignols to produce higher-order lignin involved in plant development and stress responses. We identified 30 laccase genes (OsLACs) from rice, which can be divided into five subfamilies, mostly expressed during early development of the endosperm, growing roots, and stems. OsLACs can be induced by hormones, salt, drought, and heavy metals stresses. The expression level of OsLAC10 increased 1200-fold after treatment with 20 \u03bcM Cu for  12 h. The laccase activities of OsLAC10 were confirmed in an Escherichia coli expression system. Lignin accumulation increased in the roots of Arabidopsis over-expressing OsLAC10 (OsLAC10-OX) compared to wild-type controls. After growth on 1\/2 Murashige and Skoog (MS) medium containing toxic levels of Cu for seven days, roots of the OsLAC10-OX lines were significantly longer than those of the wild type. Compared to control plants, the Cu concentration decreased significantly in roots of the OsLAC10-OX line under hydroponic conditions. These results provided insights into the evolutionary expansion and functional divergence of OsLAC family. In addition, OsLAC10 is likely involved in lignin biosynthesis, and reduces the uptake of Cu into roots required for Arabidopsis to develop tolerance to Cu.<\/jats:p>","DOI":"10.3390\/ijms18020209","type":"journal-article","created":{"date-parts":[[2017,1,30]],"date-time":"2017-01-30T11:36:30Z","timestamp":1485776190000},"page":"209","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":155,"title":["Comprehensive Analysis of Rice Laccase Gene (OsLAC) Family and Ectopic Expression of OsLAC10 Enhances Tolerance to Copper Stress in Arabidopsis"],"prefix":"10.3390","volume":"18","author":[{"given":"Qingquan","family":"Liu","sequence":"first","affiliation":[{"name":"College of Life Sciences, Nanjing Agricultural University, Nanjing 210095, China"},{"name":"Institute of Botany, Jiangsu Province and Chinese Academy of Sciences, Nanjing 210014, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Le","family":"Luo","sequence":"additional","affiliation":[{"name":"College of Resources and Environmental Sciences, Nanjing Agricultural University, Nanjing 210095, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Xiaoxiao","family":"Wang","sequence":"additional","affiliation":[{"name":"College of Life Sciences, Nanjing Agricultural University, Nanjing 210095, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Zhenguo","family":"Shen","sequence":"additional","affiliation":[{"name":"College of Life Sciences, Nanjing Agricultural University, Nanjing 210095, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Luqing","family":"Zheng","sequence":"additional","affiliation":[{"name":"College of Life Sciences, Nanjing Agricultural University, Nanjing 210095, China"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2017,1,30]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"472","DOI":"10.1039\/CT8834300472","article-title":"Chemistry of lacquer (urushi). Part I","volume":"43","author":"Yoshida","year":"1883","journal-title":"J. Chem. Soc."},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"624","DOI":"10.1016\/j.foodchem.2007.11.029","article-title":"Evidence of an active laccase-like enzyme in deepwater pink shrimp (Parapenaeus longirostris)","volume":"108","author":"Montero","year":"2008","journal-title":"Food Chem."},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"919","DOI":"10.1016\/S0038-0717(99)00221-7","article-title":"Purification and characterization of the first bacterial laccase in the rhizospheric bacterium Azospirillum lipoferum","volume":"32","author":"Diamantidis","year":"2000","journal-title":"Soil Biol. Biochem."},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"385","DOI":"10.1016\/S0040-4020(00)00949-2","article-title":"Oxidative conjugation of catechols with proteins in insect skeletal systems","volume":"57","author":"Kramer","year":"2001","journal-title":"Tetrahedron"},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"1162","DOI":"10.1104\/pp.99.3.1162","article-title":"Laccase from sycamore maple (Acer pseudoplatanus) polymerizes monolignols","volume":"99","author":"Sterjiades","year":"1992","journal-title":"Plant Physiol."},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"229","DOI":"10.1016\/S0031-9422(96)00489-X","article-title":"A laccase-type polyphenol oxidase from lignifying xylem of tobacco","volume":"44","author":"Richardson","year":"1997","journal-title":"Phytochemistry"},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"23","DOI":"10.1023\/A:1026437406859","article-title":"Characterization and heterologous expression of laccase cDNAs from xylem tissues of yellow-poplar (Liriodendron tulipifera)","volume":"40","author":"LaFayette","year":"1999","journal-title":"Plant Mol. Biol."},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"873","DOI":"10.1016\/S0168-9452(02)00035-3","article-title":"Isolation and characterisation of laccase cDNAs from meristematic and stem tissues of ryegrass (Lolium perenne)","volume":"162","author":"Gavnholt","year":"2002","journal-title":"Plant Sci."},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"145","DOI":"10.1104\/pp.010988","article-title":"Laccase down-regulation causes alterations in phenolic metabolism and cell wall structure in poplar","volume":"129","author":"Ranocha","year":"2002","journal-title":"Plant Physiol."},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"893","DOI":"10.1038\/nbt982","article-title":"Ex planta phytoremediation of trichlorophenol and phenolic allelochemicals via an engineered secretory laccase","volume":"22","author":"Wang","year":"2004","journal-title":"Nat. Biotechnol."},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"619","DOI":"10.1007\/s00425-004-1472-6","article-title":"Gene structure and molecular analysis of the laccase-like multicopper oxidase (LMCO) gene family in Arabidopsis thaliana","volume":"221","author":"McCaig","year":"2005","journal-title":"Planta"},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"387","DOI":"10.1007\/s002530000590","article-title":"Modification of lignin for the production of new compounded materials","volume":"55","author":"Mai","year":"2001","journal-title":"Appl. Microbiol. Biotechnol."},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"672","DOI":"10.1126\/science.260.5108.672","article-title":"A laccase associated with lignification in loblolly pine xylem","volume":"260","author":"Bao","year":"1993","journal-title":"Science"},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"1124","DOI":"10.1105\/tpc.110.082792","article-title":"Disruption of LACCASE4 and 17 results in tissue-specific alterations to lignification of Arabidopsis thaliana stems","volume":"23","author":"Berthet","year":"2011","journal-title":"Plant Cell"},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"3976","DOI":"10.1105\/tpc.113.117770","article-title":"Laccase is necessary and nonredundant with peroxidase for lignin polymerization during vascular development in Arabidopsis","volume":"25","author":"Zhao","year":"2013","journal-title":"Plant Cell"},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"29","DOI":"10.1016\/j.tplants.2006.11.006","article-title":"Flavonoid oxidation in plants: From biochemical properties to physiological functions","volume":"12","author":"Pourcel","year":"2007","journal-title":"Trends Plant Sci."},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"439","DOI":"10.1007\/s00425-010-1298-3","article-title":"The laccase multigene family in Arabidopsis thaliana: Towards addressing the mystery of their gene function (s)","volume":"233","author":"Turlapati","year":"2011","journal-title":"Planta"},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"2563","DOI":"10.1093\/jxb\/erl022","article-title":"Mutant identification and characterization of the laccase gene family in Arabidopsis","volume":"57","author":"Cai","year":"2006","journal-title":"J. Exp. Bot."},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"1185","DOI":"10.1007\/s00425-006-0300-6","article-title":"Involvement of AtLAC15 in lignin synthesis in seeds and in root elongation of Arabidopsis","volume":"224","author":"Liang","year":"2006","journal-title":"Planta"},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"98","DOI":"10.1016\/j.gene.2014.09.018","article-title":"Overexpression of the OsChI1 gene, encoding a putative laccase precursor, increases tolerance to drought and salinity stress in transgenic Arabidopsis","volume":"552","author":"Cho","year":"2014","journal-title":"Gene"},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"746","DOI":"10.1111\/j.1365-3040.2005.01435.x","article-title":"Expression of a putative laccase gene, ZmLAC1, in maize primary roots under stress","volume":"29","author":"Liang","year":"2006","journal-title":"Plant Cell Environ."},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"360","DOI":"10.1111\/j.1744-7909.2010.00892.x","article-title":"Abiotic and Biotic Stresses and Changes in the Lignin Content and Composition in Plants","volume":"52","author":"Moura","year":"2010","journal-title":"J. Integr. Plant Biol."},{"key":"ref_23","unstructured":"Marschner, H. (2012). Mineral Nutrition of Higher Plants, Academic Press. [3rd ed.]."},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"162","DOI":"10.1007\/s11356-008-0079-z","article-title":"Implications of metal accumulation mechanisms to phytoremediation","volume":"16","author":"Memon","year":"2009","journal-title":"Environ. Sci. Pollut. Res. Int."},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"445","DOI":"10.1093\/jxb\/52.suppl_1.445","article-title":"Partitioning of nutrient transport processes in roots","volume":"52","author":"Tester","year":"2001","journal-title":"J. Exp. Bot."},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"171","DOI":"10.1016\/S1367-5931(02)00298-3","article-title":"Molecular mechanisms of copper uptake and distribution","volume":"6","author":"Puig","year":"2002","journal-title":"Curr. Opin. Chem. Biol."},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"2601","DOI":"10.1093\/jxb\/erg303","article-title":"Transition metal transporters in plants","volume":"54","author":"Hall","year":"2003","journal-title":"J. Exp. Bot."},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"577","DOI":"10.1023\/A:1022345507112","article-title":"Identification of a copper transporter family in Arabidopsis thaliana","volume":"51","author":"Puig","year":"2003","journal-title":"Plant Mol. Biol."},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"225","DOI":"10.1111\/j.1365-313X.2005.02601.x","article-title":"The Arabidopsis heavy metal P-type ATPase HMA5 interacts with metallochaperones and functions in copper detoxification of roots","volume":"45","author":"Mayo","year":"2006","journal-title":"Plant J."},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"3767","DOI":"10.1105\/tpc.112.103820","article-title":"YSL16 is a phloem-localized transporter of the copper-nicotianamine complex that is responsible for copper distribution in rice","volume":"24","author":"Zheng","year":"2012","journal-title":"Plant Cell"},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"147","DOI":"10.1111\/j.1399-3054.1995.tb00821.x","article-title":"Transport of metal micronutrients in the phloem of castor bean (Ricinus communis) seedlings","volume":"95","author":"Schmidke","year":"1995","journal-title":"Physiol. Plant."},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"111","DOI":"10.1111\/j.1399-3054.1996.tb00486.x","article-title":"Cadmium and copper uptake and distribution in Mediterranean tree seedlings","volume":"97","author":"Arduini","year":"1996","journal-title":"Physiol. Plant."},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"323","DOI":"10.1007\/s11104-014-2290-7","article-title":"Transcriptional and physiological analyses identify a regulatory role for hydrogen peroxide in the lignin biosynthesis of copper-stressed rice roots","volume":"387","author":"Liu","year":"2015","journal-title":"Plant Soil."},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"1091","DOI":"10.1093\/jxb\/49.324.1091","article-title":"Effects of N-glycosylation on the folding and structure of plant proteins","volume":"49","author":"Ceriotti","year":"1998","journal-title":"J. Exp. Bot."},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"5933","DOI":"10.1073\/pnas.0800237105","article-title":"Salt tolerance of Arabidopsis thaliana requires maturation of N-glycosylated proteins in the Golgi apparatus","volume":"105","author":"Kang","year":"2008","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"217","DOI":"10.1016\/j.plantsci.2006.03.007","article-title":"Isolation and characterisation of a family of laccases in maize","volume":"171","author":"Civardi","year":"2006","journal-title":"Plant Sci."},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"147","DOI":"10.1007\/PL00013978","article-title":"Molecular Cloning and Expression of Eight Laccase cDNAs in Loblolly Pine (Pinus taeda)","volume":"114","author":"Sato","year":"2001","journal-title":"J. Plant Res."},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"1956","DOI":"10.1126\/science.1090022","article-title":"A gene expression map of the Arabidopsis root","volume":"302","author":"Birnbaum","year":"2003","journal-title":"Science"},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"15932","DOI":"10.1074\/jbc.M801406200","article-title":"MicroRNA-mediated systemic down-regulation of copper protein expression in response to low copper availability in Arabidopsis","volume":"283","author":"Pilon","year":"2008","journal-title":"J. Biol. Chem."},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"2966","DOI":"10.1105\/tpc.105.035154","article-title":"TRANSPARENT TESTA10 encodes a laccase-like enzyme involved in oxidative polymerization of flavonoids in Arabidopsis seed coat","volume":"17","author":"Pourcel","year":"2005","journal-title":"Plant Cell"},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"125","DOI":"10.1016\/S0162-0134(02)00440-3","article-title":"Primary structure of a Japanese lacquer tree laccase as a prototype enzyme of multicopper oxidases","volume":"91","author":"Nitta","year":"2002","journal-title":"J. Inorg. Biochem."},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"341","DOI":"10.1111\/jipb.12333","article-title":"Norway spruce (Picea abies) laccases: Characterization of a laccase in a lignin-forming tissue culture","volume":"57","author":"Koutaniemi","year":"2015","journal-title":"J. Integr. Plant Biol."},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"337","DOI":"10.1146\/annurev-genet-102209-163508","article-title":"The genetics of lignin biosynthesis: Connecting genotype to phenotype","volume":"44","author":"Bonawitz","year":"2010","journal-title":"Annu. Rev. Genet."},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"1207","DOI":"10.1016\/j.cub.2012.04.064","article-title":"AtABCG29 is a monolignol transporter involved in lignin biosynthesis","volume":"22","author":"Alejandro","year":"2012","journal-title":"Curr. Biol."},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"473","DOI":"10.1111\/j.1399-3054.1962.tb08052.x","article-title":"A revised medium for rapid growth and bio assays with tobacco tissue cultures","volume":"15","author":"Murashige","year":"1962","journal-title":"Physiol. Plant."},{"key":"ref_46","doi-asserted-by":"crossref","first-page":"3148","DOI":"10.1111\/j.1742-4658.2009.07033.x","article-title":"Transcript profiling reveals diverse roles of auxin-responsive genes during reproductive development and abiotic stress in rice","volume":"276","author":"Jain","year":"2009","journal-title":"FEBS J."},{"key":"ref_47","doi-asserted-by":"crossref","first-page":"609","DOI":"10.1007\/s11103-006-9112-0","article-title":"Genome-wide transcriptional analysis of salinity stressed japonica and indica rice genotypes during panicle initiation stage","volume":"63","author":"Walia","year":"2007","journal-title":"Plant Mol. Biol."},{"key":"ref_48","doi-asserted-by":"crossref","unstructured":"Wang, D., Pan, Y., Zhao, X., Zhu, L., Fu, B., and Li, Z. (2011). Genome-wide temporal-spatial gene expression profiling of drought responsiveness in rice. BMC Genom., 12.","DOI":"10.1186\/1471-2164-12-149"},{"key":"ref_49","doi-asserted-by":"crossref","unstructured":"Dubey, S., Misra, P., Dwivedi, S., Chatterjee, S., Bag, S.K., Mantri, S., Asif, M.H., Rai, A., Kumar, S., and Shri, M. (2010). Transcriptomic and metabolomic shifts in rice roots in response to Cr (VI) stress. BMC Genom., 11.","DOI":"10.1186\/1471-2164-11-648"},{"key":"ref_50","doi-asserted-by":"crossref","first-page":"1136","DOI":"10.3389\/fpls.2015.01136","article-title":"RNA-Seq analysis of rice roots reveals the involvement of post-transcriptional regulation in response to cadmium stress","volume":"6","author":"He","year":"2015","journal-title":"Front. Plant Sci."},{"key":"ref_51","doi-asserted-by":"crossref","first-page":"735","DOI":"10.1046\/j.1365-313x.1998.00343.x","article-title":"Floral dip: A simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana","volume":"16","author":"Clough","year":"1998","journal-title":"Plant J."},{"key":"ref_52","doi-asserted-by":"crossref","first-page":"507","DOI":"10.1007\/s11104-012-1486-y","article-title":"Metallothioneins BcMT1 and BcMT2 from Brassica campestris enhance tolerance to cadmium and copper and decrease production of reactive oxygen species in Arabidopsis thaliana","volume":"367","author":"Lv","year":"2013","journal-title":"Plant Soil."},{"key":"ref_53","doi-asserted-by":"crossref","first-page":"303","DOI":"10.1007\/s11240-008-9377-x","article-title":"Generation and characterization of transgenic poplar plants overexpressing a cotton laccase gene","volume":"93","author":"Wang","year":"2008","journal-title":"Plant Cell Tissue Org."},{"key":"ref_54","doi-asserted-by":"crossref","first-page":"673","DOI":"10.1016\/j.plaphy.2010.05.005","article-title":"Response to copper excess in Arabidopsis thaliana: Impact on the root system architecture, hormone distribution, lignin accumulation and mineral profile","volume":"48","author":"Lequeux","year":"2010","journal-title":"Plant Physiol. Biochem."}],"container-title":["International Journal of Molecular Sciences"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/1422-0067\/18\/2\/209\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,11]],"date-time":"2025-10-11T18:27:16Z","timestamp":1760207236000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/1422-0067\/18\/2\/209"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2017,1,30]]},"references-count":54,"journal-issue":{"issue":"2","published-online":{"date-parts":[[2017,2]]}},"alternative-id":["ijms18020209"],"URL":"https:\/\/doi.org\/10.3390\/ijms18020209","relation":{},"ISSN":["1422-0067"],"issn-type":[{"value":"1422-0067","type":"electronic"}],"subject":[],"published":{"date-parts":[[2017,1,30]]}}}