{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,11]],"date-time":"2026-09-11T02:18:37Z","timestamp":1789093117547,"version":"build-2803163510"},"reference-count":51,"publisher":"MDPI AG","issue":"1","license":[{"start":{"date-parts":[[2017,12,28]],"date-time":"2017-12-28T00:00:00Z","timestamp":1514419200000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Genes"],"abstract":"<jats:p>In plants, exposure to solar ultraviolet (UV) light is unavoidable, resulting in DNA damage. Damaged DNA causes mutations, replication arrest, and cell death, thus efficient repair of the damaged DNA is essential. A light-independent DNA repair pathway called nucleotide excision repair (NER) is conserved throughout evolution. For example, the damaged DNA-binding protein Radiation sensitive 4 (Rad4) in Saccharomyces cerevisiae is homologous to the mammalian NER protein Xeroderma Pigmentosum complementation group C (XPC). In this study, we examined the role of the Arabidopsis thaliana Rad4\/XPC homologue (AtRAD4) in plant UV tolerance by generating overexpression lines. AtRAD4 overexpression, both with and without an N-terminal yellow fluorescent protein (YFP) tag, resulted in increased UV tolerance. YFP-RAD4 localized to the nucleus, and UV treatment did not alter this localization. We also used yeast two-hybrid analysis to examine the interaction of AtRAD4 with Arabidopsis RAD23 and found that RAD4 interacted with RAD23B as well as with the structurally similar protein HEMERA (HMR). In addition, we found that hmr and rad23 mutants exhibited increased UV sensitivity. Thus, our analysis suggests a role for RAD4 and RAD23\/HMR in plant UV tolerance.<\/jats:p>","DOI":"10.3390\/genes9010008","type":"journal-article","created":{"date-parts":[[2017,12,28]],"date-time":"2017-12-28T11:24:33Z","timestamp":1514460273000},"page":"8","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":22,"title":["RAD4 and RAD23\/HMR Contribute to Arabidopsis UV Tolerance"],"prefix":"10.3390","volume":"9","author":[{"given":"Triparna","family":"Lahari","sequence":"first","affiliation":[{"name":"Department of Biological Sciences, University of Manitoba, Winnipeg, MB R3T 2N2, Canada"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Janelle","family":"Lazaro","sequence":"additional","affiliation":[{"name":"Department of Biological Sciences, University of Manitoba, Winnipeg, MB R3T 2N2, Canada"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Dana","family":"Schroeder","sequence":"additional","affiliation":[{"name":"Department of Biological Sciences, University of Manitoba, Winnipeg, MB R3T 2N2, Canada"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2017,12,28]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"592980","DOI":"10.4061\/2010\/592980","article-title":"Molecular mechanisms of ultraviolet radiation-induced DNA damage and repair","volume":"2010","author":"Rastogi","year":"2010","journal-title":"J. Nucleic Acids"},{"key":"ref_2","first-page":"16","article-title":"Multiple DNA damage recognition factors involved in mammalian nucleotide excision repair","volume":"76","author":"Sugasawa","year":"2011","journal-title":"Biochemistry"},{"key":"ref_3","doi-asserted-by":"crossref","unstructured":"Chen, C.C. (2011). UV Damaged DNA Repair & Tolerance in Plants. Selected Topics in DNA Repair, INTECH Open Access Publisher.","DOI":"10.5772\/1749"},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"430","DOI":"10.1016\/j.tig.2006.06.006","article-title":"When transcription and repair meet: A complex system","volume":"22","author":"Laine","year":"2006","journal-title":"Trends Genet."},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"116","DOI":"10.1016\/j.yexcr.2014.08.010","article-title":"Insight in the multilevel regulation of NER","volume":"329","author":"Dijk","year":"2014","journal-title":"Exp. Cell Res."},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"196","DOI":"10.1016\/j.mad.2013.03.008","article-title":"The role of Cockayne syndrome group A (CSA) protein in transcription-coupled nucleotide excision repair","volume":"134","author":"Saijo","year":"2013","journal-title":"Mech. Ageing Dev."},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"29","DOI":"10.1016\/j.mrfmmm.2009.08.004","article-title":"Regulation of damage recognition in mammalian global genomic nucleotide excision repair","volume":"685","author":"Sugasawa","year":"2010","journal-title":"Mutat. Res."},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"2177","DOI":"10.1007\/s00018-015-1859-5","article-title":"Orchestral maneuvers at the damaged sites in nucleotide excision repair","volume":"72","author":"Alekseev","year":"2015","journal-title":"Cell. Mol. Life Sci."},{"key":"ref_9","first-page":"2529","article-title":"Distinct functions of the ubiquitin-proteasome pathway influence nucleotide excision repair","volume":"25","author":"Gillette","year":"2006","journal-title":"EMBO J."},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"557","DOI":"10.1023\/A:1005870227632","article-title":"Characterization and expression of a rice RAD23 gene","volume":"34","author":"Schultz","year":"1997","journal-title":"Plant Mol. Biol."},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"815","DOI":"10.1046\/j.1365-313X.1998.00075.x","article-title":"Two isoforms of plant RAD23 complement a UV-sensitive rad23 mutant in yeast","volume":"13","author":"Sturm","year":"1998","journal-title":"Plant J."},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"124","DOI":"10.1105\/tpc.109.072660","article-title":"The RAD23 family provides an essential connection between the 26S proteasome and ubiquitylated proteins in Arabidopsis","volume":"22","author":"Farmer","year":"2010","journal-title":"Plant Cell"},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"1230","DOI":"10.1016\/j.cell.2010.05.007","article-title":"Arabidopsis HEMERA\/pTAC12 initiates photomorphogenesis by phytochromes","volume":"141","author":"Chen","year":"2010","journal-title":"Cell"},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"176","DOI":"10.1105\/tpc.105.036392","article-title":"PTAC2,-6, and-12 are components of the transcriptionally active plastid chromosome that are required for plastid gene expression","volume":"18","author":"Pfalz","year":"2010","journal-title":"Plant Cell"},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"1633","DOI":"10.1105\/tpc.021378","article-title":"CENTRIN2 modulates homologous recombination and nucleotide excision repair in Arabidopsis","volume":"16","author":"Molinier","year":"2004","journal-title":"Plant Cell"},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"345","DOI":"10.1007\/s11103-006-0016-9","article-title":"CENTRIN2 interacts with the Arabidopsis homologue of the human XPC protein (AtRAD4) and contributes to efficient synthesis-dependent repair of bulky DNA lesions","volume":"61","author":"Liang","year":"2006","journal-title":"Plant Mol. Biol."},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"1409","DOI":"10.1105\/tpc.114.136093","article-title":"HEMERA couples the proteolysis and transcriptional activity of PHYTOCHROME INTERACTING FACTORs in Arabidopsis photomorphogenesis","volume":"27","author":"Qiu","year":"2015","journal-title":"Plant Cell"},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"616","DOI":"10.1111\/j.1365-313X.2005.02617.x","article-title":"Gateway compatible vectors for plant functional genomics and proteomics","volume":"45","author":"Earley","year":"2006","journal-title":"Plant J."},{"key":"ref_19","unstructured":"Weigel, D., and Glazebrook, J. (2002). Arabidopsis: A Laboratory Manual, Cold Spring Harbor Library Press."},{"key":"ref_20","doi-asserted-by":"crossref","unstructured":"Hossain, Z., Amyot, L., McGarvey, B., Gruber, M., Jung, J., and Hannoufa, A. (2012). The translation elongation factor eEF-1B\u03b21 is involved in cell wall biosynthesis and plant development in Arabidopsis thaliana. PLoS ONE, 7.","DOI":"10.1371\/journal.pone.0030425"},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"646","DOI":"10.1016\/j.bbrc.2006.04.140","article-title":"Validation of housekeeping genes as internal control for studying gene expression in rice by quantitative real-time PCR","volume":"345","author":"Jain","year":"2006","journal-title":"Biochem. Biophys. Res. Commun."},{"key":"ref_22","first-page":"227","article-title":"Isolation of uvh1, an Arabidopsis mutant hypersensitive to ultraviolet light and ionizing radiation","volume":"6","author":"Harlow","year":"1994","journal-title":"Plant Cell"},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"220","DOI":"10.3109\/10520299509108199","article-title":"DAPI: A DNA-specific fluorescent probe","volume":"70","author":"Kapuscinski","year":"1995","journal-title":"Biotech. Histochem."},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"653","DOI":"10.1126\/science.1086391","article-title":"Genome-wide insertional mutagenesis of Arabidopsis thaliana","volume":"301","author":"Alonso","year":"2003","journal-title":"Science"},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"94","DOI":"10.1093\/nar\/30.1.94","article-title":"FLAGdb\/FST: A database of mapped flanking insertion sites (FSTs) of Arabidopsis thaliana T-DNA transformants","volume":"30","author":"Samson","year":"2002","journal-title":"Nucleic Acids Res."},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"D1185","DOI":"10.1093\/nar\/gks1151","article-title":"SUBA3: A database for integrating experimentation and prediction to define the SUBcellular location of proteins in Arabidopsis","volume":"41","author":"Tanz","year":"2013","journal-title":"Nucleic Acids Res."},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"3356","DOI":"10.1093\/bioinformatics\/btu550","article-title":"SUBAcon: A consensus algorithm for unifying the subcellular localization data of the Arabidopsis proteome","volume":"30","author":"Hooper","year":"2014","journal-title":"Bioinformatics"},{"key":"ref_28","doi-asserted-by":"crossref","unstructured":"Liu, L., Zhang, Z., Mei, Q., and Chen, M. (2013). PSI: A comprehensive and integrative approach for accurate plant subcellular localization prediction. PLoS ONE, 8.","DOI":"10.1371\/journal.pone.0075826"},{"key":"ref_29","doi-asserted-by":"crossref","unstructured":"Lei, Z., and Dai, Y. (2005). An SVM-based system for predicting protein subnuclear localizations. BMC Bioinform., 6.","DOI":"10.1186\/1471-2105-6-291"},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"2","DOI":"10.1016\/j.mrfmmm.2014.08.007","article-title":"DNA damage and gene therapy of xeroderma pigmentosum, a human DNA repair-deficient disease","volume":"776","author":"Dupuy","year":"2016","journal-title":"Mutat. Res."},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"570","DOI":"10.1038\/nature06155","article-title":"Recognition of DNA damage by the Rad4 nucleotide excision repair protein","volume":"449","author":"Min","year":"2007","journal-title":"Nature"},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"5981","DOI":"10.1093\/nar\/gkh934","article-title":"Roles of Rad23 protein in yeast nucleotide excision repair","volume":"32","author":"Xie","year":"2004","journal-title":"Nucleic Acids Res."},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"288","DOI":"10.1016\/j.jhep.2005.02.020","article-title":"Overexpression of the two nucleotide excision repair genes ERCC1 and XPC in human hepatocellular carcinoma","volume":"43","author":"Fautrel","year":"2005","journal-title":"J. Hepatol."},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"213","DOI":"10.1091\/mbc.e13-05-0293","article-title":"XPC promotes MDM2-mediated degradation of the p53 tumor suppressor","volume":"25","author":"Krzeszinski","year":"2014","journal-title":"Mol. Biol. Cell"},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"371","DOI":"10.1007\/s11103-009-9479-9","article-title":"Overexpression of Arabidopsis damaged DNA binding protein 1A (DDB1A) enhances UV tolerance","volume":"70","author":"Schroeder","year":"2009","journal-title":"Plant Mol. Biol."},{"key":"ref_36","doi-asserted-by":"crossref","unstructured":"Molinier, J., Lechner, E., Dumbliauskas, E., and Genschik, P. (2008). Regulation and role of Arabidopsis CUL4-DDB1A-DDB2 in maintaining genome integrity upon UV stress. PLoS Genet., 4.","DOI":"10.1371\/journal.pgen.1000093"},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"404","DOI":"10.1111\/j.1365-313X.2010.04157.x","article-title":"The DDB1a interacting proteins ATCSA 1 and DDB2 are critical factors for UV B tolerance and genomic integrity in Arabidopsis thaliana","volume":"62","author":"Biedermann","year":"2010","journal-title":"Plant J."},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"686","DOI":"10.1038\/nature02026","article-title":"Global analysis of protein localization in budding yeast","volume":"425","author":"Huh","year":"2003","journal-title":"Nature"},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"177","DOI":"10.1091\/mbc.e09-04-0305","article-title":"Rad4 regulates protein turnover at a postubiquitylation step","volume":"21","author":"Li","year":"2010","journal-title":"Mol. Biol. Cell"},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"2551","DOI":"10.1093\/nar\/24.13.2551","article-title":"XPC and human homologs of RAD23: Intracellular localization and relationship to other nucleotide excision repair complexes","volume":"24","author":"Eker","year":"1996","journal-title":"Nucleic Acids Res."},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"2850","DOI":"10.1242\/jcs.031708","article-title":"Versatile DNA damage detection by the global genome nucleotide excision repair protein XPC","volume":"121","author":"Hoogstraten","year":"2008","journal-title":"J. Cell Sci."},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"83","DOI":"10.1242\/jcs.031062","article-title":"Spatial organization of nucleotide excision repair proteins after UV-induced DNA damage in the human cell nucleus","volume":"122","author":"Solimando","year":"2009","journal-title":"J. Cell Sci."},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"1437","DOI":"10.1105\/tpc.108.058891","article-title":"Arabidopsis DDB1-CUL4 ASSOCIATED FACTOR1 forms a nuclear E3 ubiquitin ligase with DDB1 and CUL4 that is involved in multiple plant developmental processes","volume":"20","author":"Zhang","year":"2008","journal-title":"Plant Cell"},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"1101","DOI":"10.1007\/s00425-014-2042-1","article-title":"Overexpression of rice OsREX1-S, encoding a putative component of the core general transcription and DNA repair factor IIH, renders plant cells tolerant to cadmium-and UV-induced damage by enhancing DNA excision repair","volume":"239","author":"Kunihiro","year":"2014","journal-title":"Planta"},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"387","DOI":"10.1016\/j.cell.2005.02.035","article-title":"UV-induced ubiquitylation of XPC protein mediated by UV-DDB-ubiquitin ligase complex","volume":"121","author":"Sugasawa","year":"2005","journal-title":"Cell"},{"key":"ref_46","doi-asserted-by":"crossref","first-page":"635","DOI":"10.1128\/MCB.17.2.635","article-title":"The RAD7, RAD16, and RAD23 genes of Saccharomyces cerevisiae: Requirement for transcription-independent nucleotide excision repair in vitro and interactions between the gene products","volume":"17","author":"Wang","year":"1997","journal-title":"Mol. Cell. Biol."},{"key":"ref_47","doi-asserted-by":"crossref","first-page":"858","DOI":"10.1016\/j.dnarep.2008.02.004","article-title":"The NER protein Rad33 shows functional homology to human Centrin2 and is involved in modification of Rad4","volume":"7","author":"Brandsma","year":"2008","journal-title":"DNA Repair"},{"key":"ref_48","doi-asserted-by":"crossref","first-page":"197","DOI":"10.1016\/S0921-8777(97)00002-5","article-title":"XPC interacts with both HHR23B and HHR23A in vivo","volume":"383","author":"Li","year":"1997","journal-title":"Mutat. Res."},{"key":"ref_49","doi-asserted-by":"crossref","first-page":"449","DOI":"10.1016\/S1568-7864(02)00031-9","article-title":"The carboxy-terminal domain of the XPC protein plays a crucial role in nucleotide excision repair through interactions with transcription factor IIH","volume":"1","author":"Uchida","year":"2002","journal-title":"DNA Repair"},{"key":"ref_50","doi-asserted-by":"crossref","first-page":"1733","DOI":"10.1104\/pp.111.184762","article-title":"A functional component of the transcriptionally active chromosome complex, Arabidopsis pTAC14, interacts with pTAC12\/HEMERA and regulates plastid gene expression","volume":"157","author":"Gao","year":"2011","journal-title":"Plant Physiol."},{"key":"ref_51","first-page":"10161","article-title":"Arabidopsis rad23-4 gene is required for pollen development under UV-B light","volume":"11","author":"Li","year":"2012","journal-title":"Afr. J. Biotechnol."}],"container-title":["Genes"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2073-4425\/9\/1\/8\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,11]],"date-time":"2025-10-11T18:55:54Z","timestamp":1760208954000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2073-4425\/9\/1\/8"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2017,12,28]]},"references-count":51,"journal-issue":{"issue":"1","published-online":{"date-parts":[[2018,1]]}},"alternative-id":["genes9010008"],"URL":"https:\/\/doi.org\/10.3390\/genes9010008","relation":{},"ISSN":["2073-4425"],"issn-type":[{"value":"2073-4425","type":"electronic"}],"subject":[],"published":{"date-parts":[[2017,12,28]]}}}