{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,2,9]],"date-time":"2026-02-09T20:06:14Z","timestamp":1770667574907,"version":"3.49.0"},"reference-count":59,"publisher":"MDPI AG","issue":"13","license":[{"start":{"date-parts":[[2019,7,4]],"date-time":"2019-07-04T00:00:00Z","timestamp":1562198400000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"name":"Next Generation BioGreen 21 Program, Rural Development Administration, Republic of Korea","award":["Code No. PJ01322401"],"award-info":[{"award-number":["Code No. PJ01322401"]}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["IJMS"],"abstract":"<jats:p>High-intensity ultraviolet-B (UV-B) irradiation is a complex abiotic stressor resulting in excessive light exposure, heat, and dehydration, thereby affecting crop yields. In the present study, we identified quantitative trait loci (QTLs) for resistance to high-intensity UV-B irradiation in soybean (Glycine max [L.]). We used a genotyping-by-sequencing approach using an F6 recombinant inbred line (RIL) population derived from a cross between Cheongja 3 (UV-B sensitive) and Buseok (UV-B resistant). We evaluated the degree of leaf damage by high-intensity UV-B radiation in the RIL population and identified four QTLs, UVBR12-1, 6-1, 10-1, and 14-1, for UV-B stress resistance, together explaining 20% of the observed phenotypic variation. The genomic regions containing UVBR12-1 and UVBR6-1 and their syntenic blocks included other known biotic and abiotic stress-related QTLs. The QTL with the highest logarithm of odds (LOD) score of 3.76 was UVBR12-1 on Chromosome 12, containing two genes encoding spectrin beta chain, brain (SPTBN, Glyma.12g088600) and bZIP transcription factor21\/TGACG motif-binding 9 (bZIP TF21\/TGA9, Glyma.12g088700). Their amino acid sequences did not differ between the mapping parents, but both genes were significantly upregulated by UV-B stress in Buseok but not in Cheongja 3. Among five genes in UVBR6-1 on Chromosome 6, Glyma.06g319700 (encoding a leucine-rich repeat family protein) had two nonsynonymous single nucleotide polymorphisms differentiating the parental lines. Our findings offer powerful genetic resources for efficient and precise breeding programs aimed at developing resistant soybean cultivars to multiple stresses. Furthermore, functional validation of the candidate genes will improve our understanding of UV-B stress defense mechanisms.<\/jats:p>","DOI":"10.3390\/ijms20133287","type":"journal-article","created":{"date-parts":[[2019,7,4]],"date-time":"2019-07-04T11:13:18Z","timestamp":1562238798000},"page":"3287","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":14,"title":["QTL Analysis of Resistance to High-Intensity UV-B Irradiation in Soybean (Glycine max [L.] Merr.)"],"prefix":"10.3390","volume":"20","author":[{"given":"Min Young","family":"Yoon","sequence":"first","affiliation":[{"name":"Department of Plant Science and Research Institute of Agriculture and Life Sciences, Seoul National University, Seoul 08826, Korea"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Moon Young","family":"Kim","sequence":"additional","affiliation":[{"name":"Department of Plant Science and Research Institute of Agriculture and Life Sciences, Seoul National University, Seoul 08826, Korea"},{"name":"Plant Genomics and Breeding Institute, Seoul National University, Seoul 08826, Korea"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Jungmin","family":"Ha","sequence":"additional","affiliation":[{"name":"Department of Plant Science and Research Institute of Agriculture and Life Sciences, Seoul National University, Seoul 08826, Korea"},{"name":"Plant Genomics and Breeding Institute, Seoul National University, Seoul 08826, Korea"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Taeyoung","family":"Lee","sequence":"additional","affiliation":[{"name":"Department of Plant Science and Research Institute of Agriculture and Life Sciences, Seoul National University, Seoul 08826, Korea"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Kyung Do","family":"Kim","sequence":"additional","affiliation":[{"name":"Corporate R&amp;D, LG Chem, Seoul 07795, Korea"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-5946-6185","authenticated-orcid":false,"given":"Suk-Ha","family":"Lee","sequence":"additional","affiliation":[{"name":"Department of Plant Science and Research Institute of Agriculture and Life Sciences, Seoul National University, Seoul 08826, Korea"},{"name":"Plant Genomics and Breeding Institute, Seoul National University, Seoul 08826, Korea"}],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"1968","published-online":{"date-parts":[[2019,7,4]]},"reference":[{"key":"ref_1","unstructured":"World Meteorological Organization, 2008 (2019, February 20). WMO Statement on the Status of the Global Climate in 2007. Available online: https:\/\/library.wmo.int\/doc_num.php?explnum_id=3457."},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"53","DOI":"10.3844\/jastsp.2018.53.64","article-title":"NASA sees first in 2018 the direct proof of ozone hole recovery","volume":"2","author":"Petrescu","year":"2018","journal-title":"J. Aircr. Spacecr. Technolog."},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"22","DOI":"10.1016\/S0169-5347(96)10062-8","article-title":"UV-B as an environmental factor in plant life: Stress and regulation","volume":"12","author":"Rozema","year":"1997","journal-title":"Trends Ecol. Evolut."},{"key":"ref_4","first-page":"1420","article-title":"Ultraviolet-B radiation-mediated responses in plants","volume":"133","author":"Frohnmeyer","year":"2003","journal-title":"Balancing damage and protection. Plant Physiol."},{"key":"ref_5","unstructured":"UNEP (2019, February 20). 2010 Annual Report. Available online: https:\/\/wedocs.unep.org\/handle\/20.500.11822\/7915."},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"653","DOI":"10.1111\/j.1751-1097.1988.tb02877.x","article-title":"Response differences between two soybean cultivars with contrasting UV-B radiation sensitivities","volume":"48","author":"Murali","year":"1988","journal-title":"Photochem. Photobiol."},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"5","DOI":"10.1111\/j.1399-3054.1990.tb04367.x","article-title":"Effects of UV-B radiation on soybean yield and seed quality: A 6-year field study","volume":"80","author":"Teramura","year":"1990","journal-title":"Physiol. Plantarum."},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"197","DOI":"10.1590\/S1677-04202011000300003","article-title":"Intraspecific variation in sensitivity to ambient ultraviolet-B radiation in growth and yield characteristics of eight soybean cultivars grown under field conditions","volume":"23","author":"Baroniya","year":"2011","journal-title":"Braz. J. Plant Physiol."},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"109","DOI":"10.1007\/s10681-014-1233-y","article-title":"Detection of quantitative trait loci controlling UV-B resistance in soybean","volume":"202","author":"Shim","year":"2015","journal-title":"Euphytica"},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1007\/s11032-016-0471-1","article-title":"Positional mapping and identification of novel quantitative trait locus responsible for UV-B radiation tolerance in soybean (Glycine max [L.] Merr.)","volume":"36","author":"Lee","year":"2016","journal-title":"Mol. Breed."},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"207","DOI":"10.1007\/s10681-014-1271-5","article-title":"Underlying genetic variation in the response of cultivated and wild soybean to enhanced ultraviolet-B radiation","volume":"202","author":"Kim","year":"2015","journal-title":"Euphytica"},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"1917","DOI":"10.3389\/fpls.2016.01917","article-title":"Transcriptomic profiling of soybean in response to high-intensity UV-B irradiation reveals stress defense signaling","volume":"7","author":"Yoon","year":"2016","journal-title":"Front. Plant Sci."},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"178","DOI":"10.1038\/nature08670","article-title":"Genome sequence of the palaeopolyploid soybean","volume":"463","author":"Schmutz","year":"2010","journal-title":"Nature"},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1007\/s00425-003-1105-5","article-title":"Plant responses to drought, salinity and extreme temperatures: Towards genetic engineering for stress tolerance","volume":"218","author":"Wang","year":"2003","journal-title":"Planta"},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"217","DOI":"10.1016\/S1369-5266(00)80068-0","article-title":"Molecular responses to dehydration and low temperature: Differences and cross-talk between two stress signaling pathways","volume":"3","author":"Shinozaki","year":"2000","journal-title":"Curr. Opin. Plant Biol."},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"262","DOI":"10.1016\/S1360-1385(01)01946-X","article-title":"Abiotic stress signaling pathways: Specificity and cross-talk","volume":"6","author":"Knight","year":"2001","journal-title":"Trends Plant Sci."},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"909","DOI":"10.1071\/FP02062","article-title":"Review: Molecular response of plant cells to UV-B stress","volume":"29","author":"Jordan","year":"2002","journal-title":"Funct. Plant Biol."},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"48","DOI":"10.1016\/S0169-5347(02)00014-9","article-title":"Ecological roles of solar UV radiation: Towards an integrated approach","volume":"18","author":"Paul","year":"2003","journal-title":"Trends Ecol. Evolut."},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"407","DOI":"10.1146\/annurev.arplant.59.032607.092953","article-title":"Signal transduction in responses to UV-B radiation","volume":"60","author":"Jenkins","year":"2009","journal-title":"Annu. Rev. Plant Biol."},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"1113","DOI":"10.1073\/pnas.1214237110","article-title":"Reversion of the Arabidopsis UV-B photoreceptor UVR8 to the homodimeric ground state","volume":"110","author":"Heijde","year":"2013","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_21","first-page":"474","article-title":"Footprints of the sun: Memory of UV and light stress in plants","volume":"5","author":"Xing","year":"2014","journal-title":"Front. Plant Sci."},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"334","DOI":"10.1016\/j.jphotobiol.2015.10.004","article-title":"Changing scenario in plant UV-B research: UV-B from a generic stressor to a specific regulator","volume":"153","author":"Parihar","year":"2015","journal-title":"J. Photochem. Photobiol. B Biol."},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"32","DOI":"10.1111\/nph.12797","article-title":"Abiotic and biotic stress combinations","volume":"203","author":"Suzuki","year":"2014","journal-title":"New Phytol."},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"225","DOI":"10.1007\/s13258-016-0490-7","article-title":"Transcriptomic profiling of soybean in response to UV-B and Xanthomonas axonopodis treatment reveals shared gene components in stress defense pathways","volume":"39","author":"Yoon","year":"2017","journal-title":"Genes Genom."},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"620","DOI":"10.1016\/j.bbamem.2013.05.002","article-title":"Spectrins: A structural platform for stabilization and activation of membrane channels, receptors and transporters","volume":"1838","author":"Machnicka","year":"2014","journal-title":"Biochim. Biophys. Acta Biomembr"},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"1353","DOI":"10.1152\/physrev.2001.81.3.1353","article-title":"Spectrin and ankyrin-based pathways: Metazoan inventions for integrating cells into tissues","volume":"81","author":"Bennett","year":"2001","journal-title":"Physiol. Rev."},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"13","DOI":"10.1111\/j.1469-8137.2004.01076.x","article-title":"The role of the actin cytoskeleton in plant cell signaling","volume":"163","author":"Staiger","year":"2004","journal-title":"New Phytol."},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"144","DOI":"10.1002\/bies.20177","article-title":"Spectrin repeat proteins in the nucleus","volume":"2 7","author":"Young","year":"2005","journal-title":"BioEssays"},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"335","DOI":"10.1006\/cbir.1999.0365","article-title":"Spectrin-like proteins in green algae (Desmidiaceae)","volume":"23","author":"Holzinger","year":"1999","journal-title":"Cell Biol. Int."},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"1611","DOI":"10.1104\/pp.125.4.1611","article-title":"Association of spectrin-like proteins with the actin-organized aggregate of endoplasmic reticulum in the spitzenk\u00f6rper of gravitropically tip-growing plant cells","volume":"125","author":"Braun","year":"2001","journal-title":"Plant Physiol."},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"145","DOI":"10.1042\/BC20100083","article-title":"Nuclear spectrin-like proteins are structural actin-binding proteins in plants","volume":"103","year":"2011","journal-title":"Biol. Cell"},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"77","DOI":"10.1016\/0014-5793(91)81347-B","article-title":"Identification of a 220-kDa membrane-associated plant cell protein immunologically related to human \u03b2-spectrin","volume":"294","author":"Michaud","year":"1991","journal-title":"FEBS Lett."},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"169","DOI":"10.1006\/cbir.1993.1053","article-title":"Immunodetection of spectrin in plant cells","volume":"17","author":"Emons","year":"1993","journal-title":"Cell Biol. Int."},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"14600","DOI":"10.1074\/jbc.M707818200","article-title":"Dematin and adducing provide a novel link between the spectrin cytoskeleton and human erythrocyte membrane by directly interacting with glucose transporter-1","volume":"283","author":"Khan","year":"2008","journal-title":"J. Biol. Chem."},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"8026","DOI":"10.1073\/pnas.0803225105","article-title":"Protein 4.1R-dependent multiprotein complex: New insights into the structural organization of the red blood cell membrane","volume":"105","author":"Salomao","year":"2008","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"191","DOI":"10.1007\/s00018-011-0804-5","article-title":"Spectrin-based skeleton as an actor in cell signaling","volume":"69","author":"Machnicka","year":"2012","journal-title":"Cell Mol. Life Sci."},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"309","DOI":"10.1038\/363309b0","article-title":"Pleckstrin domain homology","volume":"363","author":"Haslam","year":"1993","journal-title":"Nature"},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"343","DOI":"10.1016\/0968-0004(93)90071-T","article-title":"The PH domain: A common piece in the structural patchwork of signaling proteins","volume":"18","author":"Musacchio","year":"1993","journal-title":"Trends Biochem. Sci."},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"675","DOI":"10.1038\/369675a0","article-title":"Structure of the pleckstrin homology domain from beta-spectrin","volume":"369","author":"Macias","year":"1994","journal-title":"Nature"},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"759","DOI":"10.1104\/pp.126.2.759","article-title":"Rapid accumulation of phosphatidylinositol 4,5-bisphosphate and inositol 1,4,5-trisphosphate correlates with calcium mobilization in salt-stressed Arabidopsis","volume":"126","author":"DeWald","year":"2001","journal-title":"Plant Physiol."},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"1397","DOI":"10.1073\/pnas.0308044100","article-title":"Genome-wide analysis of gene expression reveals function of the bZIP transcription factor HY5 in the UV-B response of Arabidopsis","volume":"101","author":"Ulm","year":"2004","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"591","DOI":"10.1038\/emboj.2009.4","article-title":"Interaction of COP1 and UVR8 regulates UV-B-induced photomorphogenesis and stress acclimation in Arabidopsis","volume":"28","author":"Favory","year":"2009","journal-title":"EMBO J."},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"106","DOI":"10.1016\/S1360-1385(01)02223-3","article-title":"bZIP transcription factors in Arabidopsis","volume":"7","author":"Jakoby","year":"2002","journal-title":"Trends Plant Sci."},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"1492","DOI":"10.1104\/pp.110.159111","article-title":"Arabidopsis basic leucine-zipper transcription factors TGA9 and TGA10 interact with floral glutaredoxins ROXY1 and ROXY2 and are redundantly required for anther development","volume":"154","author":"Murmu","year":"2010","journal-title":"Plant Physiol."},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"1457","DOI":"10.1080\/09168451.2014.942254","article-title":"Cellular redox regulation, signaling, and stress response in plants","volume":"78","author":"Shigeoka","year":"2014","journal-title":"Biosci. Biotechnol. Biochem."},{"key":"ref_46","doi-asserted-by":"crossref","first-page":"12","DOI":"10.1016\/j.plantsci.2016.06.019","article-title":"Arabidopsis clade IV TGA transcription factors, TGA10 and TGA9, are involved in ROS-mediated responses to bacterial PAMP flg22","volume":"252","author":"Noshi","year":"2016","journal-title":"Plant Sci."},{"key":"ref_47","doi-asserted-by":"crossref","first-page":"10897","DOI":"10.1074\/jbc.M110.168179","article-title":"Unambiguous characterization of site-specific phosphorylation of leucine-rich repeat Fli-I-interacting protein 2 (LRRFIP2) in toll-like receptor 4 (TLR4)-mediated signaling","volume":"286","author":"Gunawardena","year":"2011","journal-title":"J. Biol. Chem."},{"key":"ref_48","doi-asserted-by":"crossref","first-page":"235","DOI":"10.1007\/s00299-016-2084-x","article-title":"The role of receptor-like protein kinases (RLKs) in abiotic stress response in plants","volume":"36","author":"Ye","year":"2017","journal-title":"Plant Cell Rep."},{"key":"ref_49","doi-asserted-by":"crossref","unstructured":"Fu, S.F., Chen, P.Y., Nguyen, Q.T.T., Huang, L.Y., Zeng, G.R., Huang, T.L., Lin, C.Y., and Huang, H.J. (2014). Transcriptome profiling of genes and pathways associated with arsenic toxicity and tolerance in Arabidopsis. BMC Plant Biol., 14.","DOI":"10.1186\/1471-2229-14-94"},{"key":"ref_50","doi-asserted-by":"crossref","first-page":"138","DOI":"10.1016\/j.jplph.2015.01.001","article-title":"Molecular characterization of the cold- and heat-induced Arabidopsis PXL1 gene and its potential role in transduction pathways under temperature fluctuations","volume":"176","author":"Chang","year":"2015","journal-title":"J. Plant Physiol."},{"key":"ref_51","doi-asserted-by":"crossref","first-page":"40","DOI":"10.1111\/ppl.12337","article-title":"Functional study of a salt-inducible TaSR gene in Triticum aestivum","volume":"156","author":"Ma","year":"2015","journal-title":"Physiol. Plant."},{"key":"ref_52","doi-asserted-by":"crossref","first-page":"271","DOI":"10.1093\/jxb\/eru417","article-title":"Plasma membrane receptor-like kinase leaf panicle 2 acts downstream of the drought and salt tolerance transcription factor to regulate drought sensitivity in rice","volume":"66","author":"Wu","year":"2015","journal-title":"J. Exp. Bot."},{"key":"ref_53","doi-asserted-by":"crossref","first-page":"131","DOI":"10.1016\/B978-0-12-282606-1.50010-6","article-title":"Solar UV irradiation and the growth and development of higher plants","volume":"6","author":"Caldwell","year":"1971","journal-title":"Photophysiology"},{"key":"ref_54","doi-asserted-by":"crossref","unstructured":"Elshire, R.J., Glaubitz, J.C., Sun, Q., Poland, J.A., Kawamoto, K., Buckler, E.S., and Mitchellet, S.E. (2011). A robust, simple genotyping-by-sequencing (GBS) approach for high diversity species. PLoS ONE, 6.","DOI":"10.1371\/journal.pone.0019379"},{"key":"ref_55","doi-asserted-by":"crossref","first-page":"357","DOI":"10.1038\/nmeth.1923","article-title":"Fast gapped-read alignment with Bowtie 2","volume":"9","author":"Langmead","year":"2012","journal-title":"Nat. Methods"},{"key":"ref_56","doi-asserted-by":"crossref","unstructured":"Glaubitz, J.C., Casstevens, T.M., Lu, F., Harriman, J., Elshire, R.J., Sun, Q., and Buckler, E.S. (2014). TASSEL-GBS: A high capacity genotyping by sequencing analysis pipeline. PLoS ONE, 9.","DOI":"10.1371\/journal.pone.0090346"},{"key":"ref_57","doi-asserted-by":"crossref","first-page":"402","DOI":"10.1006\/meth.2001.1262","article-title":"Analysis of relative gene expression data using real-time quantitative PCR and the 2\u2212\u0394\u0394CT method","volume":"25","author":"Livak","year":"2001","journal-title":"Methods"},{"key":"ref_58","doi-asserted-by":"crossref","first-page":"D843","DOI":"10.1093\/nar\/gkp798","article-title":"SoyBase, the USDA-ARS soybean genetics and genomics database","volume":"38","author":"Grant","year":"2010","journal-title":"Nucleic Acids Res."},{"key":"ref_59","doi-asserted-by":"crossref","first-page":"e49","DOI":"10.1093\/nar\/gkr1293","article-title":"MCScanX: A toolkit for detection and evolutionary analysis of gene synteny and collinearity","volume":"40","author":"Wang","year":"2012","journal-title":"Nucleic. Acids Res."}],"container-title":["International Journal of Molecular Sciences"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/1422-0067\/20\/13\/3287\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,11]],"date-time":"2025-10-11T13:02:33Z","timestamp":1760187753000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/1422-0067\/20\/13\/3287"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2019,7,4]]},"references-count":59,"journal-issue":{"issue":"13","published-online":{"date-parts":[[2019,7]]}},"alternative-id":["ijms20133287"],"URL":"https:\/\/doi.org\/10.3390\/ijms20133287","relation":{},"ISSN":["1422-0067"],"issn-type":[{"value":"1422-0067","type":"electronic"}],"subject":[],"published":{"date-parts":[[2019,7,4]]}}}