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Identification of candidate genes for an early-maturing soybean mutant by genome resequencing analysis

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Abstract

Flowering is indicative of the transition from vegetative to reproductive phase, a critical event in the life cycle of plants. In this study, we performed whole genome resequencing by Illumina HiSeq to identify changes in flowering genes using an early-flowering phenotype of soybean mutant line Josaengserori (JS) derived from Korean landrace, Seoritae (SR), and we obtained mapped reads of 131,769,690 and 167,669,640 bp in JS and SR, respectively. From the whole genome sequencing results between JS and SR, we identified 332,821 polymorphic SNPs and 65,178 indels, respectively. Among these, 30 flowering genes were in SNPs and 25 were in indels. Among 30 flowering genes detected in SNPs, Glyma02g33040, Glyma06g22650, Glyma10g36600, Glyma13g01290, Glyma14g10530, Glyma16g01980, Glyma17g11040, Glyma18g53690, and Glyma20g29300 were non-synonymous substitutions between JS and SR. Changes in Glyma10g36600 (GI), Glya02g33040 (AGL18), Glyma17g11040 (TOC1), and Glyma14g10530 (ELF3) in JS affected the expression of GmFT2a and resulted in early flowering. These results provide insight into the regulatory pathways of flowering in soybean mutants and help to improve our knowledge of soybean mutation breeding.

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References

  • Adamczyk BJ, Lehti-Shiu MD, Fernandez DE (2007) The MADS domain factors AGL15 and AGL18 act redundantly as repressors of the floral transition in Arabidopsis. Plant J 50:1007–1019

    Article  CAS  PubMed  Google Scholar 

  • Ahloowalia BS, Maluszynski M, Nichterlein K (2004) Global impact of mutation-derived varieties. Euphytica 135:187–204

    Article  Google Scholar 

  • Alabadi D, Oyama T, Yanovsky MJ, Harmon FG, Mas P, Kay SA (2001) Reciprocal regulation between TOC1 and LHY/CCA1 within the Arabidopsis circadian clock. Science 293:880–883

    Article  CAS  PubMed  Google Scholar 

  • Breen AP, Murphy JA (1995) Reactions of Oxyl Radicals with DNA. Free Radic Biol Med 18:1033–1077

    Article  CAS  PubMed  Google Scholar 

  • Cox MP, Peterson DA, Biggs PJ (2010) SolexaQA: At-a-glance quality assessment of Illumina second-generation sequencing data. BMC Bioinform 11:485–490

    Article  Google Scholar 

  • Ding ZJ, Doyle MR, Amasino RM, Davis SJ (2007) A complex genetic interaction between Arabidopsis thaliana TOC1 and CCA1/LHY in driving the circadian clock and in output regulation. Genetics 176:1501–1510

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fernandez DE, Wang CT, Zheng YM, Adamczyk BJ, Singhal R, Hall PK, Perry SE (2014) The MADS-domain factors AGAMOUS-LIKE15 and AGAMOUS-LIKE18, along with SHORT VEGETATIVE PHASE and AGAMOUS-LIKE24, are necessary to block floral gene expression during the vegetative phase. Plant Physiol 165:1591–1603

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fowler S, Lee K, Onouchi H, Samach A, Richardson K, Coupland G, Putterill J (1999) GIGANTEA: a circadian clock-controlled gene that regulates photoperiodic flowering in Arabidopsis and encodes a protein with several possible membrane-spanning domains. EMBO J 118:4679–4688

    Article  Google Scholar 

  • Fuciarelli AF, Wegher BJ, Blakely WF, Dizdaroglu M (1990) Yields of radiation-induced base products in DNA—effects of DNA conformation and gassing conditions. Int J Radiat Biol 58:397–415

    Article  CAS  PubMed  Google Scholar 

  • Gutierrez-Gonzalez JJ, Guttikonda SK, Tran LSP, Aldrich DL, Zhong R, Yu O, Nguyen HT, Sleper DA (2010) Differential expression of isoflavone biosynthetic genes in soybean during water deficits. Plant Cell Physiol 51:936–948

    Article  CAS  PubMed  Google Scholar 

  • Ha BK, Lee KJ, Velusamy V, Kim JB, Kim SH, Ahn JW, Kang SY, Kim DS (2014) Improvement of soybean through radiation-induced mutation breeding techniques in Korea. Plant Genetic Plant Genet Resour C 12:S54–S57

    Article  CAS  Google Scholar 

  • Hayama R, Yokoi S, Tamaki S, Yano M, Shimamoto K (2003) Adaptation of photoperiodic control pathways produces short-day flowering in rice. Nature 422:719–722

    Article  CAS  PubMed  Google Scholar 

  • Hicks KA, Millar AJ, Carre IA, Somers DE, Straume M, MeeksWagner DR, Kay SA (1996) Conditional circadian dysfunction of the Arabidopsis early-flowering 3 mutant. Science 274:790–792

    Article  CAS  PubMed  Google Scholar 

  • Hirano T, Hirano H, Yamaguchi R, Asami S, Tsurudome Y, Kasai H (2001) Sequence specificity of the 8-hydroxyguanine repair activity in rat organs. J Radiat Res 42:247–254

    Article  CAS  PubMed  Google Scholar 

  • Hwang SG, Hwang JG, Kim DS, Jang CS (2014) Genome-wide DNA polymorphism and transcriptome analysis of an early-maturing rice mutant. Genetica 142:73–85

    Article  CAS  PubMed  Google Scholar 

  • Hwang WJ, Kim MY, Kang YJ, Shim S, Stacey MG, Stacey G, Lee SH (2015) Genome-wide analysis of mutations in a dwarf soybean mutant induced by fast neutron bombardment. Euphytica 203:399–408

    Article  Google Scholar 

  • Jung JH, Seo YH, Seo PJ, Reyes JL, Yun J, Chua NH, Park CM (2007) The GIGANTEA-regulated MicroRNA172 mediates photoperiodic flowering independent of CONSTANS in Arabidopsis. Plant Cell 19:2736–2748

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kim DH, Doyle MR, Sung S, Amasino RM (2009) Vernalization: winter and the timing of flowering in plants. Annu Rev Cell Dev Biol 25:277–299

    Article  CAS  PubMed  Google Scholar 

  • Kim DS, Lee KJ, Kim JB, Kim SH, Song JY, Seo YW, Lee BM, Kang SY (2010) Identification of Kunitz trypsin inhibitor mutations using SNAP markers in soybean mutant lines. Theor Appl Genet 121:751–760

    Article  CAS  PubMed  Google Scholar 

  • Kim MY, Shin JH, Kang YJ, Shim SR, Lee SH (2012) Divergence of flowering genes in soybean. J Biosci 37:857–870

    Article  CAS  PubMed  Google Scholar 

  • Koornneef M, Alonso-Blanco C, Blankestijn-de Vries H, Hanhart CJ, Peeters AJM (1998) Genetic interactions among late-flowering mutants of Arabidopsis. Genetics 148:885–892

    CAS  PubMed  PubMed Central  Google Scholar 

  • Lee KJ, Kim JB, Kim SH, Ha BK, Lee BM, Kang SY, Kim DS (2011) Alteration of seed storage protein composition in soybean [Glycine max (L.) Merrill] mutant lines induced by gamma-irradiation mutagenesis. J Agric Food Chem 59:12405–12410

    Article  CAS  PubMed  Google Scholar 

  • Lee KJ, Hwang JE, Velusamy V, Ha BK, Kim JB, Kim SH, Ahn JW, Kang SY, Kim DS (2014) Selection and molecular characterization of a lipoxygenase-free soybean mutant line induced by gamma irradiation. Theor Appl Genet 127:2405–2413

    Article  CAS  PubMed  Google Scholar 

  • Li H, Durbin R (2009) Fast and accurate short read alignment with Burrows–Wheeler transform. Bioinformatics 25:1754–1760

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, Homer N, Marth G, Abecasis G, Durbin R, Proc GPD (2009) The sequence alignment/map format and SAMtools. Bioinformatics 25:2078–2079

    Article  PubMed  PubMed Central  Google Scholar 

  • Liu B, Kanazawa A, Matsumura H, Takahashi R, Harada K, Abe J (2008) Genetic redundancy in soybean photoresponses associated with duplication of the phytochrome A Gene. Genetics 180:995–1007

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lukowitz W, Gillmor CS, Scheible WR (2000) Positional cloning in arabidopsis. Why it feels good to have a genome initiative working for you. Plant Physiol 123:795–805

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • McWatters HG, Bastow RM, Hall A, Millar AJ (2000) The ELF3 zeitnehmer regulates light signalling to the circadian clock. Nature 408:716–720

    Article  CAS  PubMed  Google Scholar 

  • Mizoguchi T, Wheatley K, Hanzawa Y, Wright L, Mizoguchi M, Song HR, Carre IA, Coupland G (2002) LHY and CCA1 are partially redundant genes required to maintain circadian rhythms in Arabidopsis. Dev Cell 2:629–641

    Article  CAS  PubMed  Google Scholar 

  • Mizoguchi T, Wright L, Fujiwara S, Cremer F, Lee K, Onouchi H, Mouradov A, Fowler S, Kamada H, Putterill J, Coupland G (2005) Distinct roles of GIGANTEA in promoting flowering and regulating circadian rhythms in Arabidopsis. Plant Cell 17:2255–2270

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Morita R, Kusaba M, Iida S, Yamaguchi H, Nishio T, Nishimura M (2009) Molecular characterization of mutations induced by gamma irradiation in rice. Genes Genet Syst 84:361–370

    Article  CAS  PubMed  Google Scholar 

  • Salvi S, Tuberosa R (2005) To clone or not to clone plant QTLs: present and future challenges. Trends Plant Sci 10:297–304

    Article  CAS  PubMed  Google Scholar 

  • Sato Y, Shirasawa K, Takahashi Y, Nishimura M, Nishio T (2006) Mutant selection from progeny of gamma-ray-irradiated rice by DNA heteroduplex cleavage using Brassica petiole extract. Breed Sci 56:179–183

    Article  CAS  Google Scholar 

  • Schneeberger K (2014) Using next-generation sequencing to isolate mutant genes from forward genetic screens. Nat Rev Genet 15:662–676

    Article  CAS  PubMed  Google Scholar 

  • Shibutani S, Takeshita M, Grollman AP (1991) Insertion of specific bases during DNA-synthesis past the oxidation-damaged base 8-Oxodg. Nature 349:431–434

    Article  CAS  PubMed  Google Scholar 

  • Somers DE, Webb AAR, Pearson M, Kay SA (1998) The short-period mutant, toc1-1, alters circadian clock regulation of multiple outputs throughout development in Arabidopsis thaliana. Development 125:485–494

    CAS  PubMed  Google Scholar 

  • Song HS, Kim J-B, Lee KJ, Kim DS, Kim SH, Lee SJ, Kang S-Y (2010) A new improved soybean variety, “Josaengseori” by mutation breeding. Korean J Breed Sci 42:222–225

    Google Scholar 

  • Strayer C, Oyama T, Schultz TF, Raman R, Somers DE, Mas P, Panda S, Kreps JA, Kay SA (2000) Cloning of the Arabidopsis clock cone TOC1, an autoregulatory response regulator homolog. Science 289:768–771

    Article  CAS  PubMed  Google Scholar 

  • Varshney RK, Nayak SN, May GD, Jackson SA (2009) Next-generation sequencing technologies and their implications for crop genetics and breeding. Trends Biotechnol 27:522–530

    Article  CAS  PubMed  Google Scholar 

  • Varshney RK, Terauchi R, McCouch SR (2014) Harvesting the promising fruits of genomics: applying genome sequencing technologies to crop breeding. Plos Biol 12:e1001883

    Article  PubMed  PubMed Central  Google Scholar 

  • Wallace SS (1998) Enzymatic processing of radiation-induced free radical damage in DNA. Radiat Res 150:S60–S79

    Article  CAS  PubMed  Google Scholar 

  • Wallace SS (2002) Biological consequences of free radical-damaged DNA bases. Free Radic Biol Med 33:1–14

    Article  CAS  PubMed  Google Scholar 

  • Wang D, Kreutzer DA, Essigmann JM (1998) Mutagenicity and repair of oxidative DNA damage: insights from studies using defined lesions. Mutat Res 400:99–115

    Article  CAS  PubMed  Google Scholar 

  • Watanabe S, Hideshima R, Xia ZJ, Tsubokura Y, Sato S, Nakamoto Y, Yamanaka N, Takahashi R, Ishimoto M, Anai T, Tabata S, Harada K (2009) Map-based cloning of the gene associated with the soybean maturity locus E3. Genetics 182:1251–1262

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Watanabe S, Xia ZJ, Hideshima R, Tsubokura Y, Sato S, Yamanaka N, Takahashi R, Anai T, Tabata S, Kitamura K, Harada K (2011) A Map-based cloning strategy employing a residual heterozygous line reveals that the GIGANTEA gene is involved in soybean maturity and flowering. Genetics 188:U260–U395

    Article  Google Scholar 

  • Wu JY, Morimyo M, Hongo E, Higashi T, Okamoto M, Kawano A, Ohmachi Y (2006) Radiation-induced germline mutations detected by a direct comparison of parents and first-generation offspring DNA sequences containing SNPs. Mutat Res 596:1–11

    Article  CAS  PubMed  Google Scholar 

  • Xia ZJ, Watanabe S, Yamada T, Tsubokura Y, Nakashima H, Zhai H, Anai T, Sato S, Yamazaki T, Lu SX, Wu HY, Tabata S, Harada K (2012a) Positional cloning and characterization reveal the molecular basis for soybean maturity locus E1 that regulates photoperiodic flowering. Proc Natl Acad Sci USA 109:E2155–E2164

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Xia ZJ, Zhai H, Liu BH, Kong FJ, Yuan XH, Wu HY, Cober ER, Harada K (2012b) Molecular identification of genes controlling flowering time, maturity, and photoperiod response in soybean. Plant Syst Evol 298:1217–1227

    Article  CAS  Google Scholar 

  • Yoshihara R, Hase Y, Sato R, Takimoto K, Narumi I (2010) Mutational effects of different LET radiations in rpsL transgenic Arabidopsis. Int J Radiat Biol 86:125–131

    Article  CAS  PubMed  Google Scholar 

  • Yu JW, Rubio V, Lee NY, Bai SL, Lee SY, Kim SS, Liu LJ, Zhang YY, Irigoyen ML, Sullivan JA, Zhang Y, Lee I, Xie Q, Paek NC, Deng XW (2008) COP1 and ELF3 control circadian function and photoperiodic flowering by regulating GI stability. Mol Cell 32:617–630

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhai H, Lu SX, Liang S, Wu HY, Zhang XZ, Liu BH, Kong FJ, Yuan XH, Li J, Xia ZJ (2014) GmFT4, a Homolog of FLOWERING LOCUS T, Is Positively Regulated by E1 and Functions as a Flowering Repressor in Soybean. Plos One 9:e89030

    Article  PubMed  PubMed Central  Google Scholar 

  • Zhu MJ, Zhao SH (2007) Candidate gene identification approach: progress and challenges. Int J Biol Sci 3:420–427

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgments

This work was supported by the Korea Atomic Energy Research Institute (KAERI) and the National Research Foundation of Korea (NRF) grant funded by the Korea government (MSIP) (No. 2012M2A2A6010566) and Chonnam National University, 2014, Republic of Korea.

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Correspondence to Jin-Baek Kim or Bo-Keun Ha.

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Communicated by R. K. Varshney.

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Lee, K.J., Kim, D.S., Kim, JB. et al. Identification of candidate genes for an early-maturing soybean mutant by genome resequencing analysis. Mol Genet Genomics 291, 1561–1571 (2016). https://doi.org/10.1007/s00438-016-1183-2

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