Abstract
Reductions in stratospheric ozone have resulted in increased levels of ultraviolet-B (UV-B, 280–315 nm) radiation reaching the earth’s surface. UV-B radiation can damage plant DNA and photosynthetic machinery. Therefore, enhanced UV-B levels would seriously affect crop production in several regions of the world. Here, we provide a comprehensive report of intraspecific variability in the response of soybean to UV-B radiation and the genetic variation underlying UV-B resistance. We evaluated 140 genotypes, including 94 Glycine max and 46 G. soja accessions, for their sensitivity to supplemental UV-B radiation. Differences in responses to elevated UV-B levels, such as changes in leaf area and aerial biomass, were observed among soybean genotypes, supporting the notion that there is intraspecific variability in this response in G. soja as well as G. max. To explore how genetic variation contributes to differences in UV-B resistance, we sequenced the most UV-B resistant (IT162669) and sensitive (Cheongjakong 3) genotypes at the whole-genome level. Based on their homology and functional annotation, 137 genes were determined to be “UV-B-related genes” in soybean, harboring almost 100 high-confidence single nucleotide polymorphisms between the two genotypes. Interestingly, we identified four genes with non-synonymous mutations that are related to plant protection mechanisms, such as the UV-protection, DNA damage repair and DNA damage tolerance pathways. Our results provide valuable information about UV-B-resistant soybean genotypes, UV-B-related soybean genes, and sequence variations between resistant and sensitive genotypes.
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References
Ambler JE, Krizek DT, Semeniuk P (1975) Influence of UV-B radiation on early seedling growth and translocation of 65Zn from cotyledons in cotton. Physiol Plantarum 34:177–181
Au KG, Welsh K, Modrich P (1992) Initiation of methyl-directed mismatch repair. J Biol Chem 267:12142–12148
Austin J, Wilson RJ (2006) Ensemble simulations of the decline and recovery of stratospheric ozone. J Geophys Res-Atmos. doi:10.1029/2005jd006907
Bieza K, Lois R (2001) An Arabidopsis mutant tolerant to lethal ultraviolet-B levels shows constitutively elevated accumulation of flavonoids and other phenolics. Plant Physiol 126:1105–1115. doi:10.1104/pp.126.3.1105
Biggs RH, Kossuth SV, Teramura AH (1981) Response of 19 cultivars of soybeans to ultraviolet-B irradiance. Physiol Plantarum 53:19–26
Britt AB (1996) DNA damage and repair in plants. Annu Rev Plant Phys 47:75–100
Chang DJ, Cimprich KA (2009) DNA damage tolerance: when it’s OK to make mistakes. Nat Chem Biol 5:82–90. doi:10.1038/nchembio.139
Culligan KM, Hays JB (2000) Arabidopsis MutS Homologs—AtMSH2, AtMSH3, AtMSH6, and a novel AtMSH7—form three distinct protein heterodimers with different specificities for mismatched DNA. Plant Cell 12:991–1002. doi:10.1105/tpc.12.6.991
Dai QJ, Peng SB, Chavez AQ, Vergara BS (1994) Intraspecific responses of 188 rice cultivars to enhanced UVB radiation. Environ Exp Bot 34:433–442
Dsurney SJ, Tschaplinski TJ, Edwards NT, Shugart LR (1993) Biological responses of 2 soybean cultivars exposed to enhanced UVB radiation. Environ Exp Bot 33:347–356
Fehr WR, Caviness CE (1977) Stages of soybean development. Iowa State University of Science and Technology Ames, Iowa
Feng WY, Hays JB (1995) DNA structures generated during recombination initiated by mismatch repair of UV-irradiated nonreplicating phage DNA in Escherichia coli: requirements for helicase, exonucleases, and RecF and RecBCD functions. Genetics 140:1175–1186
Feng HY, An LZ, Chen T, Qiang WY, Xu SJ, Zhang MX, Wang XL, Cheng GD (2003) The effect of enhanced ultraviolet-B radiation on growth, photosynthesis and stable carbon isotope composition (d13C) of two soybean cultivars (Glycine max) under field conditions. Environ Exp Bot 49:1–8
Frohnmeyer H, Staiger D (2003) Ultraviolet-B radiation-mediated responses in plants. Balancing damage and protection. Plant Physiol 133:1420–1428. doi:10.1104/pp.103.030049
Ghosal G, Chen J (2013) DNA damage tolerance: a double-edged sword guarding the genome. Transl Cancer Res 2:107–129. doi:10.3978/j.issn.2218-676X.2013.04.01
Gonzalez R, Mepsted R, Wellburn AR, Paul ND (1998) Non-photosynthetic mechanisms of growth reduction in pea (Pisum sativum L.) exposed to UV-B radiation. Plant Cell Environ 21:23–32
Harfe BD, Jinks-Robertson S (2000) DNA mismatch repair and genetic instability. Ann Rev Gen 34:359–399. doi:10.1146/annurev.genet.34.1.359
Hidema J, Teranishi M, Iwamatsu Y, Hirouchi T, Ueda T, Sato T, Burr B, Sutherland BM, Yamamoto K, Kumagai T (2005) Spontaneously occurring mutations in the cyclobutane pyrimidine dimer photolyase gene cause different sensitivities to ultraviolet-B in rice. Plant J 43:57–67. doi:10.1111/j.1365-313X.2005.02428.x
Hofmann RW, Campbell BD, Fountain DW, Jordan BR, Greer DH, Hunt DY, Hunt CL (2001) Multivariate analysis of intraspecific responses to UV-B radiation in white clover (Trifolium repens L.). Plant Cell Environ 24:917–927
Hyten DL, Song Q, Zhu Y, Choi IY, Nelson RL, Costa JM, Specht JE, Shoemaker RC, Cregan PB (2006) Impacts of genetic bottlenecks on soybean genome diversity. Proc Natl Acad Sci USA 103:16666–16671. doi:10.1073/pnas.0604379103
Iwamatsu Y, Aoki C, Takahashi M, Teranishi M, Ding Y, Sun CQ, Kumagai T, Hidema J (2008) UVB sensitivity and cyclobutane pyrimidine dimer (CPD) photolyase genotypes in cultivated and wild rice species. Photoch Photobio Sci 7:311–320. doi:10.1039/b719034d
Jansen MAK, Gaba V, Greenberg BM (1998) Higher plants and UV-B radiation: balancing damage, repair and acclimation. Trends Plant Sci 3:131–135
Jiricny J, Nyström-Lahti M (2000) Mismatch repair defects in cancer. Curr Opin Genet Dev 10:157–161. doi:10.1016/S0959-437X(00)00066-6
Kakani VG, Reddy KR, Zhao D, Mohammed AR (2003a) Effects of ultraviolet-B radiation on cotton (Gossypium hirsutum L.) morphology and anatomy. Ann Bot-London 91:817–826. doi:10.1093/aob/mcg086
Kakani VG, Reddy KR, Zhao D, Sailaja K (2003b) Field crop responses to ultraviolet-B radiation: a review. Agr Forest Meteorol 120:191–218. doi:10.1016/j.agrformet.2003.08.015
Koti S, Reddy KR, Kakani VG, Zhao D, Reddy VR (2004) Soybean (Glycine max) pollen germination characteristics, flower and pollen morphology in response to enhanced ultraviolet-B radiation. Ann Bot-London 94:855–864
Krizek DT, Kramer GF, Upadhyaya A, Mirecki RM (1993) UV-B response of cucumber seedlings grown under metal halide and high pressure sodium/deluxe lamps. Physiol Plant 88:350–358
Lemontt JF (1971) Mutants of yeast deffective in mutation induced by ultraviolet light. Genetics 68:21–33
Li H, Durbin R (2009) Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 25:1754–1760. doi:10.1093/bioinformatics/btp324
Li Y, Zu YQ, Chen JJ, Chen HY (2002) Intraspecific responses in crop growth and yield of 20 soybean cultivars to enhanced ultraviolet-B radiation under field conditions. Field Crop Res 78:1–8
Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, Homer N, Marth G, Abecasis G, Durbin R, Genome Project Data Processing S (2009) The sequence alignment/map format and SAMtools. Bioinformatics 25:2078–2079. doi:10.1093/bioinformatics/btp352
Madronich S, McKenzie RL, Bjorn LO, Caldwell MM (1998) Changes in biologically active ultraviolet radiation reaching the Earth’s surface. J Photoch Photobio B 46:5–19
McKenzie R, Conner B, Bodeker G (1999) Increased summertime UV radiation in New Zealand in response to ozone loss. Science 285:1709–1711
McKenzie RL, Aucamp PJ, Bais AF, Bjorn LO, Ilyas M (2007) Changes in biologically-active ultraviolet radiation reaching the Earth’s surface. Photoch Photobio Sci 6:218–231. doi:10.1039/B700017k
McKenzie RL, Aucamp PJ, Bais AF, Bjorn LO, Ilyas M, Madronich S (2011) Ozone depletion and climate change: impacts on UV radiation. Photochem Photobiol Sci 10:182–198. doi:10.1039/c0pp90034f
Meissner D, Albert A, Bottcher C, Strack D, Milkowski C (2008) The role of UDP-glucose:hydroxycinnamate glucosyltransferases in phenylpropanoid metabolism and the response to UV-B radiation in Arabidopsis thaliana. Planta 228:663–674. doi:10.1007/s00425-008-0768-3
Nogues S, Allen DJ, Morison JIL, Baker NR (1998) Ultraviolet-B radiation effects on water relations, leaf development, and photosynthesis in droughted pea plants. Plant Physiol 117:173–181
Reddy KR, Kakani VG, Zhao D, Mohammed AR, Gao W (2003) Cotton responses to ultraviolet-B radiation: experimentation and algorithm development. Agr Forest Meteorol 120:249–265. doi:10.1016/j.agrformet.2003.08.029
Reed HE, Teramura AH, Kenworthy WJ (1992) Ancestral U.S. soybean cultivars characterized for tolerance to ultraviolet-B radiation. Crop Sci 32:1214–1219
Roldan-Arjona T, Ariza RR (2009) Repair and tolerance of oxidative DNA damage in plants. Mutat Res 681:169–179. doi:10.1016/j.mrrev.2008.07.003
Schmutz J, Cannon SB, Schlueter J, Ma J, Mitros T, Nelson W, Hyten DL, Song Q, Thelen JJ, Cheng J, Xu D, Hellsten U, May GD, Yu Y, Sakurai T, Umezawa T, Bhattacharyya MK, Sandhu D, Valliyodan B, Lindquist E, Peto M, Grant D, Shu S, Goodstein D, Barry K, Futrell-Griggs M, Abernathy B, Du J, Tian Z, Zhu L, Gill N, Joshi T, Libault M, Sethuraman A, Zhang XC, Shinozaki K, Nguyen HT, Wing RA, Cregan P, Specht J, Grimwood J, Rokhsar D, Stacey G, Shoemaker RC, Jackson SA (2010) Genome sequence of the palaeopolyploid soybean. Nature 463:178–183. doi:10.1038/nature08670
Shindell DT, Rind D, Lonergan P (1998) Increased polar stratospheric ozone losses and delayed eventual recovery owing to increasing greenhouse-gas concentrations. Nature 392:589–592
Shure M, Wessler S, Fedoroff N (1983) Molecular identification and isolation of the Waxy locus in maize. Cell 35:225–233
Sinha RP, Hader DP (2002a) UV-induced DNA damage and repair: a review. Photoch Photobio Sci 1:225–236. doi:10.1039/B201230h
Sinha RP, Hader DP (2002b) UV-induced DNA damage and repair: a review. Photochem Photobiol Sci 1:225–236
Smith JL, Burritt DJ, Bannister P (2000) Shoot dry weight, chlorophyll and UV-B-absorbing compounds as indicators of a plant’s sensitivity to UV-B radiation. Ann Bot-London 86:1057–1063. doi:10.1006/anbo.2000.1270
Strid A, Chow WS, Anderson JM (1994) UV-B damage and protection at the molecular level in plants. Photosynth Res 39:475–489
Sullivan JH, Teramura AH (1990) Field study of the interaction between solar ultraviolet-B radiation and drought on photosynthesis and growth in soybean. Plant Physiol 92:141–146
Takahashi S, Sakamoto A, Sato S, Kato T, Tabata S, Tanaka A (2005) Roles of Arabidopsis AtREV1 and AtREV7 in translesion synthesis. Plant Physiol 138:870–881. doi:10.1104/pp.105.060236
Teramura AH (1983) Effects of ultraviolet-B radiation on the growth and yield of crop plants. Physiol Plantarum 58:415–427
Teramura AH, Murali NS (1986) Intraspecific differences in growth and yield of soybean exposed to ultraviolet-B radiation under greenhouse and field conditions. Environ Exp Bot 26:89–95
Teramura AH, Sullivan JH (1994) Effects of UV-B radiation on photosynthesis and growth of terrestrial plants. Photosynth Res 39:463–473
Teranishi M, Iwamatsu Y, Hidema J, Kumagai T (2004) Ultraviolet-B sensitivities in Japanese lowland rice cultivars: cyclobutane pyrimidine dimer photolyase activity and gene mutation. Plant Cell Physiol 45:1848–1856. doi:10.1093/pcp/pch215
Tuteja N, Singh MB, Misra MK, Bhalla PL, Tuteja R (2001) Molecular mechanisms of DNA damage and repair: progress in plants. Crit Rev Biochem Mol Biol 36:337–397. doi:10.1080/20014091074219
Umlas ME, Franklin WA, Chan GL, Haseltine WA (1985) Ultraviolet-light irradiation of defined-sequence DNA under conditions of chemical photosensitization. Photochem & Photobiol 42:265–273. doi:10.1111/j.1751-1097.1985.tb08941.x
Untergasser A, Nijveen H, Rao X, Bisseling T, Geurts R, Leunissen JA (2007) Primer3Plus, an enhanced web interface to Primer3. Nucleic Acids Res 35:W71–W74. doi:10.1093/nar/gkm306
Verslues PE, Guo Y, Dong C-H, Ma W, Zhu J-K (2006) Mutation of SAD2, an importin β-domain protein in Arabidopsis, alters abscisic acid sensitivity. Plant J 47:776–787. doi:10.1111/j.1365-313X.2006.02833.x
Weatherhead EC, Reinsel GC, Tiao GC, Jackman CH, Bishop L, Frith SMH, DeLuisi J, Keller T, Oltmans SJ, Fleming EL, Wuebbles DJ, Kerr JB, Miller AJ, Herman J, McPeters R, Nagatani RM, Frederick JE (2000) Detecting the recovery of total column ozone. J Geophys Res-Atmos 105:22201–22210
World Meteorological Organization (WMO) (2010) Scientific assessment of ozone depletion: 2010. Global Ozone Res. Monit. Proj. 52, Geneva, Switzerland.
Yonekura-Sakakibara K, Tohge T, Niida R, Saito K (2007) Identification of a flavonol 7-O-rhamnosyltransferase gene determining flavonoid pattern in Arabidopsis by transcriptome coexpression analysis and reverse genetics. J Biol Chem 282:14932–14941. doi:10.1074/jbc.M611498200
Zhao J, Zhang W, Zhao Y, Gong X, Guo L, Zhu G, Wang X, Gong Z, Schumaker KS, Guo Y (2007) SAD2, an Importin β-Like Protein, is required for UV-B response in Arabidopsis by mediating MYB4 nuclear trafficking. Plant Cell 19:3805–3818. doi:10.1105/tpc.106.048900
Zu YQ, Li Y, Chen HY, Chen JJ (2003) Intraspecific differences in physiological response of 20 soybean cultivars to enhanced ultraviolet-B radiation under field conditions. Environ Exp Bot 50:87–97. doi:10.1016/S0098-8472(03)00004-2
Acknowledgments
This study was supported by a grant from the Next Generation BioGreen 21 Program (No. PJ008060) of the Rural Development Administration, Republic of Korea. Suk-Ha Lee and Moon-Young Kim thank International Atomic Energy Agency (Research Contract No. 15664) and National Research Foundation of Korea (2012R1A1A3014252), respectively.
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Kim, K.D., Yun, M.Y., Shin, J.H. et al. Underlying genetic variation in the response of cultivated and wild soybean to enhanced ultraviolet-B radiation. Euphytica 202, 207–217 (2015). https://doi.org/10.1007/s10681-014-1271-5
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DOI: https://doi.org/10.1007/s10681-014-1271-5