Advertisement

Molecular Breeding

, Volume 34, Issue 2, pp 311–322 | Cite as

Fine mapping of a minor-effect QTL, DTH12, controlling heading date in rice by up-regulation of florigen genes under long-day conditions

  • Zhengzheng Zhong
  • Weixun Wu
  • Hongjun Wang
  • Liping Chen
  • Linglong Liu
  • Chunming Wang
  • Zhigang Zhao
  • Guangwen Lu
  • He Gao
  • Xiangjin Wei
  • Chuanyuan Yu
  • Mingjiang Chen
  • Yingyue Shen
  • Xin Zhang
  • Zhijun Cheng
  • Jiulin Wang
  • Ling Jiang
  • Jianmin Wan
Article

Abstract

Heading date is a key determinant of regional and seasonal adaptation in rice (Oryza sativa L.). A minor-effect quantitative trait locus (QTL), QTL for D ays t o h eading 12a (qDTH-12a), with unknown genetic action was previously coarsely detected in a recombinant inbred line population. The study reported here was designed to better define the qDTH-12a locus (designated as DTH12) in advanced segregating populations. DTH12 was initially verified in chromosome segment substitution line CSSL84. A CSSL84/Asominori//Asominori BC4F2 population was then developed, and a near-isogenic line (NIL), NIL(DTH12), was subsequently selected from this population using marker-assisted tracking that headed 8 days later than Asominori under long-day (LD) conditions but which was not significantly different in heading date in short-day environments. Using 358 Asominori/NIL(DTH12) F2:3 families grown under LD conditions, we were able to initially map DTH12 to a 26-cM interval between markers InDel12-1 and RM6296. F3 individuals heterozygous for the DTH12 regions were then chosen, and 2,388 F4:5 families were used for fine mapping. DTH12 was finally dissected as a single gene and delimited to a 153-kb genomic region with 32 open reading frames. Compared with Asominori, NIL(DTH12) showed reduced transcription of the florigen genes Heading date 3a and RICE FLOWERING LOCUS T 1, suggesting that DTH12 functions as an up-regulator of florigen genes during floral induction under LD conditions. DTH12 was also found to have an important role in rice adaptation and breeding for precise control of seed maturity. These findings provide a firm basis for cloning this minor-effect QTL involved in rice flowering.

Keywords

Oryza sativa DTH12 Heading date Minor-effect QTL Near-isogenic line 

Notes

Acknowledgments

We thank Dr. Atsushi Yoshimura (Kyushu University, Japan) for providing the CSSL population. This work was supported by grants from the 973 Program of China (Grants 2010CB125904-4).

Supplementary material

11032_2014_35_MOESM1_ESM.doc (1.8 mb)
Supplementary material 1 (DOC 1841 kb)

References

  1. Andrés F, Galbraith DW, Talón M, Domingo C (2009) Analysis of PHOTOPERIOD SENSITIVITY5 sheds light on the role of phytochromes in photoperiodic flowering in rice. Plant Physiol 151:681–690PubMedCentralPubMedCrossRefGoogle Scholar
  2. Bassam BJ, Caetano-Anollés G, Gresshoff PM (1991) Fast and sensitive silver staining of DNA in polyacrylamide gels. Anal Biochem 196:80–83PubMedCrossRefGoogle Scholar
  3. Brambilla V, Fornara F (2013) Molecular control of flowering in response to day length in rice. J Integr Plant Biol 55:410–418PubMedCrossRefGoogle Scholar
  4. Buckler ES, Holland JB, Bradbury PJ, Acharya CB, Brown PJ, Browne C, Ersoz E, Flint-Garcia S, Garcia A, Glaubitz JC, Goodman MM, Harjes C, Guill K, Kroon DE, Larsson S, Lepak NK, Li H, Mitchell SE, Pressoir G, Peiffer JA, Rosas MO, Rocheford TR, Romay MC, Romero S, Salvo S, Sanchez Villeda H, da Silva HS, Sun Q, Tian F, Upadyayula N, Ware D, Yates H, Yu J, Zhang Z, Kresovich S, McMullen MD (2009) The genetic architecture of maize flowering time. Science 325:714–718PubMedCrossRefGoogle Scholar
  5. Doi K, Izawa T, Fuse T, Yamanouchi U, Kubo T, Shimatani Z, Yano M, Yoshimura A (2004) Ehd1, a B-type response regulator in rice, confers short-day promotion of flowering and controls FT-like gene expression independently of Hd1. Genes Dev 18:926–936PubMedCentralPubMedCrossRefGoogle Scholar
  6. Gao H, Zheng XM, Fei G, Chen J, Jin M, Ren Y, Wu W, Zhou K, Sheng P, Zhou F, Jiang L, Wang J, Zhang X, Guo X, Wang JL, Cheng Z, Wu C, Wang H, Wan JM (2013) Ehd4 encodes a novel and Oryza-genus-specific regulator of photoperiodic flowering in rice. PLoS Genet 9:e1003281PubMedCentralPubMedCrossRefGoogle Scholar
  7. Harushima Y, Nakagahra M, Yano M, Sasaki T, Kurata N (2001) A genome-wide survey of reproductive barriers in an intraspecific hybrid. Genetics 159:883–892PubMedCentralPubMedGoogle Scholar
  8. Hayama R, Coupland G (2004) The molecular basis of diversity in the photoperiodic flowering responses of Arabidopsis and rice. Plant Physiol 135:677–684PubMedCentralPubMedCrossRefGoogle Scholar
  9. Hayama R, Yokoi S, Tamaki S, Yano M, Shimamoto K (2003) Adaptation of photoperiodic control pathways produces short-day flowering in rice. Nature 422:719–722PubMedCrossRefGoogle Scholar
  10. Huang X, Zhao Y, Wei X, Li C, Wang A, Zhao Q, Li W, Guo Y, Deng L, Zhu C, Fan D, Lu Y, Weng Q, Liu K, Zhou T, Jing Y, Si L, Dong G, Huang T, Lu T, Feng Q, Qian Q, Li J, Han B (2011) Genome-wide association study of flowering time and grain yield traits in a worldwide collection of rice germplasm. Nat Genet 44:32–39PubMedCrossRefGoogle Scholar
  11. International Rice Genome Sequencing Project (2005) The map-based sequence of the rice genome. Nature 436:793–800CrossRefGoogle Scholar
  12. Ishikawa R, Aoki M, Kurotani K, Yokoi S, Shinomura T, Takano M, Shimamoto K (2011) Phytochrome B regulates Heading date 1 (Hd1)- mediated expression of rice florigen Hd3a and critical day length in rice. Mol Genet Genomics 285:461–470PubMedCrossRefGoogle Scholar
  13. Izawa T (2007) Adaptation of flowering-time by natural and artificial selection in Arabidopsis and rice. J Exp Bot 58:3091–3097PubMedCrossRefGoogle Scholar
  14. Jacquemin J, Laudié M, Cooke R (2009) A recent duplication revisited: phylogenetic analysis reveals an ancestral duplication highly-conserved throughout the Oryza genus and beyond. BMC Plant Biol 9:146PubMedCentralPubMedCrossRefGoogle Scholar
  15. Jiang H, Liu D, Gu Z, Wang W (2007) Rapid evolution in a pair of recent duplicate segments of rice. J Exp Zool B Mol Dev Evol 308:50–57PubMedCrossRefGoogle Scholar
  16. Khush GS (1997) Origin, dispersal, cultivation and variation of rice. Plant Mol Biol 35(1–2):25–34PubMedCrossRefGoogle Scholar
  17. Kim SL, Lee S, Kim HJ, Nam HG, An G (2007) OsMADS51 is a short-day flowering promoter that functions upstream of Ehd1, OsMADS14, and Hd3a. Plant Physiol 145:1484–1494PubMedCentralPubMedCrossRefGoogle Scholar
  18. Kojima S, Takahashi Y, Kobayashi Y, Monna L, Sasaki T, Araki T, Yano M (2002) Hd3a, a rice ortholog of the Arabidopsis FT gene, promotes transition to flowering downstream of Hd1 under short-day conditions. Plant Cell Physiol 43:1096–1105PubMedCrossRefGoogle Scholar
  19. Komiya R, Yokoi S, Shimamoto K (2009) A gene network for long-day flowering activates RFT1 encoding a mobile flowering signal in rice. Development 136:3443–3450PubMedCrossRefGoogle Scholar
  20. Koo BH, Yoo SC, Park JW, Kwon CT, Lee BD, An G, Zhang Z, Li J, Li Z, Paek NC (2013) Natural variation in OsPRR37 regulates heading date and contributes to rice cultivation at a wide range of latitudes. Mol Plant 6(6):1877–1888. doi: 10.1093/mp/sst088 PubMedCrossRefGoogle Scholar
  21. Kubo T, Nakamura K, Yoshimura A (1999) Development of a series of Indica chromosome segment substitution lines in Japonica background of rice. Rice Genet Newsl 16:104–106Google Scholar
  22. Kwon CT, Yoo SC, Koo BH, Cho SH, Park JW, Zhang Z, Li J, Li Z, Paek NC (2014) Natural variation in Early flowering1 contributes to early flowering in japonica rice under long days. Plant, Cell Environ 37(1):101–112. doi: 10.1111/pce.12134 CrossRefGoogle Scholar
  23. Lander ES, Green P, Abrahamson J, Barlow A, Daly MJ, Lincoln SE, Newberg LA (1987) MAPMAKER: an interactive computer package for constructing primary genetic linkage maps of experimental and natural populations. Genomics 1:174–181PubMedCrossRefGoogle Scholar
  24. Lee S, Kim J, Han JJ, Han MJ, An G (2004) Functional analyses of the flowering time gene OsMADS50, the putative SUPPRESSOR OF OVEREXPRESSION OF CO 1/AGAMOUS-LIKE 20 (SOC1/AGL20) ortholog in rice. Plant J 38:754–764PubMedCrossRefGoogle Scholar
  25. Lee YS, Jeong DH, Lee DY, Yi J, Ryu CH, Kim SL, Jeong HJ, Choi SC, Jin P, Yang J, Cho LH, Choi H, An G (2010) OsCOL4 is a constitutive flowering repressor upstream of Ehd1 and downstream of OsphyB. Plant J 63:18–30PubMedGoogle Scholar
  26. Li H, Ye G, Wang J (2007) A modified algorithm for the improvement of composite interval mapping. Genetics 175:361–374PubMedCentralPubMedCrossRefGoogle Scholar
  27. Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C (T)) method. Methods 25:402–408PubMedCrossRefGoogle Scholar
  28. Matsubara K, Kono I, Hori K, Nonoue Y, Ono N, Shomura A, Mizubayashi T, Yamamoto S, Yamanouchi U, Shirasawa K, Nishio T, Yano M (2008a) Novel QTLs for photoperiodic flowering revealed by using reciprocal backcross inbred lines from crosses between japonica rice cultivars. Theor Appl Genet 117:935–945PubMedCrossRefGoogle Scholar
  29. Matsubara K, Yamanouchi U, Wang ZX, Minobe Y, Izawa T, Yano M (2008b) Ehd2, a rice ortholog of the maize INDETERMINATE1 gene, promotes flowering by up-regulating Ehd1. Plant Physiol 148:1425–1435PubMedCentralPubMedCrossRefGoogle Scholar
  30. Matsubara K, Yamanouchi U, Nonoue Y, Sugimoto K, Wang ZX, Minobe Y, Yano M (2011) Ehd3, encoding a plant homeodomain finger-containing protein, is a critical promoter of rice flowering. Plant J 66:603–612PubMedCrossRefGoogle Scholar
  31. Matsubara K, Ogiso-Tanaka E, Hori K, Ebana K, Ando T, Yano M (2012) Natural variation in Hd17, a homolog of Arabidopsis ELF3 that is involved in rice photoperiodic flowering. Plant Cell Physiol 53:709–716PubMedCrossRefGoogle Scholar
  32. McCouch SR, Teytelman L, Xu Y, Lobos KB, Clare K, Walton M, Fu B, Maghirang R, Li Z, Xing Y, Zhang Q, Kono I, Yano M, Fjellstrom R, DeClerck G, Schneider D, Cartinhour S, Ware D, Stein L (2002) Development and mapping of 2240 new SSR markers for rice (Oryza sativa L.). DNA Res 9:199–207PubMedCrossRefGoogle Scholar
  33. Murray MG, Thompson WF (1980) Rapid isolation of high molecular weight plant DNA. Nucleic Acids Res 8:4321–4325PubMedCentralPubMedCrossRefGoogle Scholar
  34. Park SJ, Kim SL, Lee S, Je BI, Piao HL, Park SH, Kim CM, Ryu CH, Park SH, Xuan YH, Colasanti J, An G, Han CD (2008) Rice Indeterminate 1 (OsId1) is necessary for the expression of Ehd1 (Early heading date 1) regardless of photoperiod. Plant J 56:1018–1029PubMedCrossRefGoogle Scholar
  35. Putterill J, Laurie R, Macknight R (2004) It’s time to flower: the genetic control of flowering time. BioEssays 26:363–373PubMedCrossRefGoogle Scholar
  36. Ryu CH, Lee S, Cho LH, Kim SL, Lee YS, Choi SC, Jeong HJ, Yi J, Park SJ, Han CD, An G (2009) OsMADS50 and OsMADS56 function antagonistically in regulating long-day (LD)-dependent flowering in rice. Plant, Cell Environ 32:1412–1427CrossRefGoogle Scholar
  37. Saito H, Ogiso-Tanaka E, Okumoto Y, Yoshitake Y, Izumi H, Yokoo T, Matsubara K, Hori K, Yano M, Inoue H, Tanisaka T (2012) Ef7 encodes an ELF3-like protein and promotes rice flowering by negatively regulating the floral repressor gene Ghd7 under both short- and long-day conditions. Plant Cell Physiol 53:717–728PubMedCrossRefGoogle Scholar
  38. Sun C, Fang J, Zhao T, Xu B, Zhang F, Liu L, Tang J, Zhang G, Deng X, Chen F, Qian Q, Cao X, Chu C (2012) The histone methyltransferase SDG724 mediates H3K36me2/3 deposition at MADS50 and RFT1 and promotes flowering in rice. Plant Cell 24:3235–3247PubMedCentralPubMedCrossRefGoogle Scholar
  39. Tamaki S, Matsuo S, Wong HL, Yokoi S, Shimamoto K (2007) Hd3a protein is a mobile flowering signal in rice. Science 316:1033–1036PubMedCrossRefGoogle Scholar
  40. Tsuji H, Taoka K, Shimamoto K (2011) Regulation of flowering in rice: two florigen genes, a complex gene network, and natural variation. Curr Opin Plant Biol 14:45–52PubMedCrossRefGoogle Scholar
  41. Tsuji H, Taoka K, Shimamoto K (2013) Florigen in rice: complex gene network for florigen transcription, florigen activation complex, and multiple functions. Curr Opin Plant Biol 16:228–235PubMedCrossRefGoogle Scholar
  42. Tsunematsu H, Yoshimura A, Harushima Y, Nagamura Y, Kurata N, Yano M, Sasaki T, Iwata N (1996) RFLP framework map using recombinant inbred lines in rice. Breed Sci 46:279–284Google Scholar
  43. Uga Y, Nonoue Y, Liang ZW, Lin HX, Yamamoto S, Yamanouchi U, Yano M (2007) Accumulation of additive effects generates a strong photoperiod sensitivity in the extremely late-heading rice cultivar ‘Nona Bokra’. Theor Appl Genet 114:1457–1466PubMedCrossRefGoogle Scholar
  44. Vega-Sánchez ME, Zeng L, Chen S, Leung H, Wang GL (2008) SPIN1, a K homology domain protein negatively regulated and ubiquitinated by the E3 ubiquitin ligase SPL11, is involved in flowering time control in rice. Plant Cell 20:1456–1469PubMedCentralPubMedCrossRefGoogle Scholar
  45. Wei X, Xu J, Guo H, Jiang L, Chen S, Yu C, Zhou Z, Hu P, Zhai H, Wan J (2010) DTH8 suppresses flowering in rice, influencing plant height and yield potential simultaneously. Plant Physiol 153:1747–1758PubMedCentralPubMedCrossRefGoogle Scholar
  46. Wu C, You C, Li C, Long T, Chen G, Byrne ME, Zhang Q (2008) RID1, encoding a Cys2/His2-type zinc finger transcription factor, acts as a master switch from vegetative to floral development in rice. Proc Natl Acad Sci USA 105:12915–12920PubMedCentralPubMedCrossRefGoogle Scholar
  47. Wu W, Zheng XM, Lu G, Zhong Z, Gao H, Chen L, Wu C, Wang HJ, Wang Q, Zhou K, Wang JL, Wu F, Zhang X, Guo X, Cheng Z, Lei C, Lin Q, Jiang L, Wang H, Ge S, Wan J (2013) Association of functional nucleotide polymorphisms at DTH2 with the northward expansion of rice cultivation in Asia. Proc Natl Acad Sci USA 110:2275–2280Google Scholar
  48. Xue W, Xing Y, Weng X, Zhao Y, Tang W, Wang L, Zhou H, Yu S, Xu C, Li X, Zhang Q (2008) Natural variation in Ghd7 is an important regulator of heading date and yield potential in rice. Nat Genet 40:761–767PubMedCrossRefGoogle Scholar
  49. Yan WH, Wang P, Chen HX, Zhou HJ, Li QP, Wang CR, Ding ZH, Zhang YS, Yu SB, Xing YZ, Zhang QF (2011) A major QTL, Ghd8, plays pleiotropic roles in regulating grain productivity, plant height, and heading date in rice. Mol Plant 4:319–330PubMedCrossRefGoogle Scholar
  50. Yan W, Liu H, Zhou X, Li Q, Zhang J, Lu L, Liu T, Liu H, Zhang C, Zhang Z, Shen G, Yao W, Chen H, Yu S, Xie W, Xing Y (2013) Natural variation in Ghd7.1 plays an important role in grain yield and adaptation in rice. Cell Res 23:969–971PubMedCentralPubMedCrossRefGoogle Scholar
  51. Yano M, Katayose Y, Ashikari M, Yamanouchi U, Monna L, Fuse T, Baba T, Yamamoto K, Umehara Y, Nagamura Y, Sasaki T (2000) Hd1, a major photoperiod sensitivity quantitative trait locus in rice, is closely related to the Arabidopsis flowering line gene CONSTANS. Plant Cell 12:2473–2483PubMedCentralPubMedCrossRefGoogle Scholar
  52. Yano M, Kojima S, Takahashi Y, Lin H, Sasaki T (2001) Genetic control of flowering time in rice, a short-day plant. Plant Physiol 127:1425–1429PubMedCentralPubMedCrossRefGoogle Scholar
  53. Yu C (2005) Study on genetic basis of heterosis exploitation of inter-subspecific hybrid rice (Oryza sativa L.). PhD thesis. Nanjing Agricultural University, NanjingGoogle Scholar
  54. Zhang H, Zhang CQ, Sun ZZ, Yu W, Gu MH, Liu QQ, Li YS (2011) A major locus qS12, located in a duplicated segment of chromosome 12, causes spikelet sterility in an indica-japonica rice hybrid. Theor Appl Genet 123:1247–1256PubMedCrossRefGoogle Scholar
  55. Zhao J, Huang X, Ouyang X, Chen W, Du A, Zhu L, Wang S, Deng XW, Li S (2012) OsELF3-1, an ortholog of Arabidopsis early flowering 3, regulates rice circadian rhythm and photoperiodic flowering. PLoS ONE 7:e43705PubMedCentralPubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2014

Authors and Affiliations

  • Zhengzheng Zhong
    • 1
    • 2
  • Weixun Wu
    • 2
  • Hongjun Wang
    • 2
  • Liping Chen
    • 2
  • Linglong Liu
    • 2
  • Chunming Wang
    • 2
  • Zhigang Zhao
    • 2
  • Guangwen Lu
    • 2
  • He Gao
    • 2
  • Xiangjin Wei
    • 2
  • Chuanyuan Yu
    • 2
  • Mingjiang Chen
    • 2
  • Yingyue Shen
    • 2
  • Xin Zhang
    • 1
  • Zhijun Cheng
    • 1
  • Jiulin Wang
    • 1
  • Ling Jiang
    • 2
  • Jianmin Wan
    • 1
    • 2
  1. 1.National Key Facility for Crop Gene Resources and Genetic Improvement, Institute of Crop SciencesChinese Academy of Agricultural SciencesBeijingChina
  2. 2.National Key Laboratory for Crop Genetics and Germplasm Enhancement, Jiangsu Plant Gene Engineering Research CenterNanjing Agricultural UniversityNanjingChina

Personalised recommendations