Plant Cell Reports

, Volume 30, Issue 12, pp 2243–2254

Heading date gene, dth3 controlled late flowering in O. Glaberrima Steud. by down-regulating Ehd1

  • X. F. Bian
  • X. Liu
  • Z. G. Zhao
  • L. Jiang
  • H. Gao
  • Y. H. Zhang
  • M. Zheng
  • L. M. Chen
  • S. J. Liu
  • H. Q. Zhai
  • J. M. Wan
Original Paper

Abstract

Heading date in rice is an important agronomic trait controlled by several genes. In this study, flowering time of variety Dianjingyou 1 (DJY1) was earlier than a near-isogenic line (named NIL) carried chromosome segment from African rice on chromosome 3S, when grown in both long-day (LD) and short-day (SD) conditions. By analyzing a large F2 population from NIL × DJY1, the locus DTH3 (QTL for days to heading on chromosome 3) controlling early heading date in DJY1 was fine mapped to a 64-kb segment which contained only one annotated gene, a MIKC-type MADS-box protein. We detected a 6-bp deletion and a single base substitution in the C-domain by sequencing DTH3 in DJY1 compared with dth3 in NIL, and overexpression of DTH3 caused early flowering in callus. Quantitative real-time PCR revealed that the transcript level of dth3 in NIL was lower than that DTH3 in DJY1 in both LD and SD conditions. The Early heading date 1 (Ehd1) which promotes the RFT1, was up-regulated by DTH3 in both LD and SD conditions. Based on Indel and dCAPs marker analysis, the dth3 allele was only present in African rice accessions. A phylogenetic analysis based on microsatellite genotyping suggested that African rice had a close genetic relationship to O. rufipogon and O. latifolia, and was similar to japonica cultivars. DTH3 affected flowering time and had no significant effect on the main agronomic traits.

Keywords

Near-isogenic lines Days to heading Flowering regulator African rice MADS-box 

Abbreviations

DJY1

Dianjingyou 1

Ehd1

Early heading date 1

LD

Long-day

MAS

Marker-assisted selection

NILs

Near-isogenic lines

SD

Short-day

SSR

Simple sequence repeat

Supplementary material

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Supplementary Fig. 1 (DOC 100 kb)
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Supplementary Table 1 (DOC 46 kb)
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Supplementary Table 2 (DOC 50 kb)
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Supplementary Table 3 (DOC 526 kb)

References

  1. Chang TT, Vergara BS, Li CC (1969) Component analysis of duration from seeding to heading in rice by the basic vegetative phase and photoperiod sensitive phase. Euphytica 18:79–91Google Scholar
  2. Chen X, Temnykh S, Xu Y, Cho Y, McCouch S (1997) Development of a microsatellite framework map providing genome-wide coverage in rice (Oryza sativa L.). Theor Appl Genet 95:553–567CrossRefGoogle Scholar
  3. Cho S, Jang S, Chae S, Chung KM, Moon YH, An G, Jang SK (1999) Analysis of the C-terminal region of Arabidopsis thaliana APETALA1 as a transcription activation domain. Plant Mol Biol 40(3):419–429PubMedCrossRefGoogle Scholar
  4. Dellaporta S, Wood J, Hicks J (1983) A plant DNA minipreparation: VersionII. Plant Mol Biol Rep 1:19–21CrossRefGoogle 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(8):926–936PubMedCrossRefGoogle Scholar
  6. Fan HY, Hu Y, Tudor M, Ma H (1997) Specific interactions between the K domains of AG and AGLs, members of the MADS domain family of DNA binding proteins. Plant J 12(5):999–1010PubMedCrossRefGoogle Scholar
  7. Hayama R, Yokoi S, Tamaki S, Yano M, Shimamoto K (2003) Adaptation of photoperiodic control pathways produces short-day flowering in rice. Nature 422(6933):719–722PubMedCrossRefGoogle Scholar
  8. Hiei Y, Ohta S, Komari T, Kumashiro T (1994) Efficient transformation of rice (Oryza sativa L.) mediated by Agrobacterium and sequence analysis of the boundaries of the T-DNA. Plant J 6(2):271–282PubMedCrossRefGoogle Scholar
  9. Honma T, Goto K (2001) Complexes of MADS-box proteins are sufficient to convert leaves into floral organs. Nature 409(6819):525–529PubMedCrossRefGoogle Scholar
  10. Hosoi N (1981) Studies on meteorological fluctuation in the growth of rice plants. V. Regional differences of thermo-sensitivity, photosensitivity, basic vegetative growth and factors determining the growth duration of Japanese varieties. Jpn J Breed 31:239–250Google Scholar
  11. Izawa T, Takahashi Y, Yano M (2003) Comparative biology comes into bloom: genomic and genetic comparison of flowering pathways in rice and Arabidopsis. Curr Opin Plant Biol 6(2):113–120PubMedCrossRefGoogle Scholar
  12. Jones MP, Mande S, Aluko K (1997) Diversity and potential of Oryza glaberrima Steud. in upland rice breeding. Jpn J Breed 47:395–398Google Scholar
  13. Kardailsky I, Shukla VK, Ahn JH, Dagenais N, Christensen SK, Nguyen JT, Chory J, Harrison MJ, Weigel D (1999) Activation tagging of the floral inducer FT. Science 286(5446):1962–1965PubMedCrossRefGoogle Scholar
  14. Kaufmann K, Melzer R, Theissen G (2005) MIKC-type MADS-domain proteins: structural modularity, protein interactions and network evolution in land plants. Gene 347(2):183–198PubMedCrossRefGoogle Scholar
  15. Khush GS (1997) Origin, dispersal, cultivation and variation of rice. Plant Mol Biol 35(1–2):25–34PubMedCrossRefGoogle Scholar
  16. 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(4):1484–1494PubMedCrossRefGoogle Scholar
  17. Kobayashi Y, Kaya H, Goto K, Iwabuchi M, Araki T (1999) A pair of related genes with antagonistic roles in mediating flowering signals. Science 286(5446):1960–1962PubMedCrossRefGoogle 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(10):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(20):3443–3450PubMedCrossRefGoogle Scholar
  20. Krizek BA, Meyerowitz EM (1996) Mapping the protein regions responsible for the functional specificities of the Arabidopsis MADS domain organ-identity proteins. Proc Natl Acad Sci USA 93(9):4063–4070PubMedCrossRefGoogle Scholar
  21. Lee H, Suh SS, Park E, Cho E, Ahn JH, Kim SG, Lee JS, Kwon YM, Lee I (2000) The AGAMOUS-LIKE 20 MADS domain protein integrates floral inductive pathways in Arabidopsis. Genes Dev 14(18):2366–2376PubMedCrossRefGoogle Scholar
  22. Lee J, Oh M, Park H, Lee I (2008) SOC1 translocated to the nucleus by interaction with AGL24 directly regulates leafy. Plant J 55(5):832–843PubMedCrossRefGoogle Scholar
  23. 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(1):18–30PubMedGoogle Scholar
  24. Lin H, Ashikari M, Yamanouchi U, Sasaki T, Yano M (2002) Identification and characterization of a Quantitative Trait Locus, Hd9, controlling heading date in rice. Breed Sci 52(1):35–41CrossRefGoogle Scholar
  25. Linares OF (2002) African rice (Oryza glaberrima): history and future potential. Proc Natl Acad Sci USA 99(25):16360–16365PubMedCrossRefGoogle Scholar
  26. Liu C, Chen HY, Er HL, Soo HM, Kumar PP, Han JH, Liou YC, Yu H (2008) Direct interaction of AGL24 and SOC1 integrates flowering signals in Arabidopsis. Development 135(8):1481–1491PubMedCrossRefGoogle Scholar
  27. Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2T−ΔΔC method. Methods 25(4):402–408PubMedCrossRefGoogle Scholar
  28. Matsubara K, Yamanouchi U, Wang ZX, Minobe Y, Izawa T, Yano M (2008) Ehd2, a rice ortholog of the maize INDETERMINATE1 gene, promotes flowering by up-regulating Ehd1. Plant Physiol 148(3):1425–1435PubMedCrossRefGoogle Scholar
  29. 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(6):199–207PubMedCrossRefGoogle Scholar
  30. Monna L, Lin X, Kojima S, Sasaki T, Yano M (2002) Genetic dissection of a genomic region for a quantitative trait locus, Hd3, into two loci, Hd3a and Hd3b, controlling heading date in rice. Theor Appl Genet 104(5):772–778PubMedCrossRefGoogle Scholar
  31. Moon J, Suh SS, Lee H, Choi KR, Hong CB, Paek NC, Kim SG, Lee I (2003) The SOC1 MADS-box gene integrates vernalization and gibberellin signals for flowering in Arabidopsis. Plant J 35(5):613–623PubMedCrossRefGoogle Scholar
  32. Nei M (1987) Molecular evolutionary genetics. Columbia University Press, New York, pp 106–107Google Scholar
  33. Onouchi H, Igeno MI, Perilleux C, Graves K, Coupland G (2000) Mutagenesis of plants overexpressing CONSTANS demonstrates novel interactions among Arabidopsis flowering-time genes. Plant Cell 12(6):885–900PubMedCrossRefGoogle Scholar
  34. Park DH, Somers DE, Kim YS, Choy YH, Lim HK, Soh MS, Kim HJ, Kay SA, Nam HG (1999) Control of circadian rhythms and photoperiodic flowering by the Arabidopsis GIGANTEA gene. Science 285(5433):1579–1582PubMedCrossRefGoogle Scholar
  35. Park SJ, Kim SL, Lee S, Je BI, Piao HL, Park SH, Kim CM, Ryu CH, 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(6):1018–1029PubMedCrossRefGoogle Scholar
  36. Rohlf E (1992) Numerical taxonomy and multivariate analysis system. NTSYS-pc program. Applied Biostatistics Inc., SetauketGoogle Scholar
  37. 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(10):1412–1427PubMedCrossRefGoogle Scholar
  38. Sanguinetti C, Dias N, Simpson A (1994) Rapid silver staining and recover of PCR products separated on polyacrylamide gels. Biotechniques 17:915–919Google Scholar
  39. Sato T, Takahashi N (1983) The effect of air and water temperature on the number of days to heading in Japonica rice cultivars. Jpn J Breed 33:111–118Google Scholar
  40. Schwab R, Palatnik JF, Riester M, Schommer C, Schmid M, Weigel D (2005) Specific effects of microRNAs on the plant transcriptome. Dev Cell 8(4):517–527PubMedCrossRefGoogle Scholar
  41. Schwarz-Sommer Z, Huijser P, Nacken W, Saedler H, Sommer H (1990) Genetic control of flower development by homeotic genes in Antirrhinum majus. Science 250(4983):931–936PubMedCrossRefGoogle Scholar
  42. Sothern RB, Tseng TS, Orcutt SL, Olszewski NE, Koukkari WL (2002) GIGANTEA and SPINDLY genes linked to the clock pathway that controls circadian characteristics of transpiration in Arabidopsis. Chronobiol Int 19(6):1005–1022PubMedCrossRefGoogle Scholar
  43. Takano M, Inagaki N, Xie X, Yuzurihara N, Hihara F, Ishizuka T, Yano M, Nishimura M, Miyao A, Hirochika H, Shinomura T (2005) Distinct and cooperative functions of phytochromes A, B, and C in the control of deetiolation and flowering in rice. Plant Cell 17(12):3311–3325PubMedCrossRefGoogle Scholar
  44. Tsai K (1986) Genes controlling heading time found in a tropical Japonica variety. Rice Genet Newslett 3:71–73Google Scholar
  45. Wang JW, Czech B, Weigel D (2009) miR156-regulated SPL transcription factors define an endogenous flowering pathway in Arabidopsis thaliana. Cell 138(4):738–749PubMedCrossRefGoogle Scholar
  46. Wei XJ, Xu JF, Guo HN, Jiang L, Chen SH, Yu CY, Zhou ZL, Hu PS, Zhai HQ, Wan JM (2010) DTH8 suppresses flowering in rice, influencing plant height and yield potential simultaneously. Plant Physiol 153(4):1747–1758PubMedCrossRefGoogle Scholar
  47. Wu G, Poethig RS (2006) Temporal regulation of shoot development in Arabidopsis thaliana by miR156 and its target SPL3. Development 133(18):3539–3547PubMedCrossRefGoogle Scholar
  48. Wu CY, You CJ, Li CS, Long T, Chen GX, Byrne ME, Zhang QF (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(35):12915–12920PubMedCrossRefGoogle Scholar
  49. Xue WY, Xing YZ, Weng XY, Zhao Y, Tang WJ, Wang L, Zhou HJ, Yu SB, Xu CG, Li XH, Zhang QF (2008) Natural variation in Ghd7 is an important regulator of heading date and yield potential in rice. Nat Genet 40(6):761–767PubMedCrossRefGoogle Scholar
  50. Yan WH, Wang P, Chen HX, Zhou HJ, Li QP, Wang CR, Ding ZH, Zhang YS, Yu SB, Xing YZ, Zhang QF (2010) A major QTL, Ghd8, plays pleiotropic roles in regulating grain productivity, plant height, and heading date in rice. Mol Plant. doi:10.1093/mp/ssq070
  51. Yang Y, Jack T (2004) Defining subdomains of the K domain important for protein–protein interactions of plant MADS proteins. Plant Mol Biol 55(1):45–59PubMedCrossRefGoogle Scholar
  52. Yang YJ, Wang XD, Wu XJ, Zhang HY, Zhang P, Zhao HX (2005) The discovery, genetic analysis and gene mapping of earliness rice D64B (Oryza sativa L.). Yi Chuan Xue Bao 32(5):495–500PubMedGoogle Scholar
  53. 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 time gene CONSTANS. Plant Cell 12(12):2473–2484PubMedCrossRefGoogle Scholar
  54. Yuan Q, Saito H, Okumoto Y, Inoue H, Nishida H, Tsukiyama T, Teraishi M, Tanisaka T (2009) Identification of a novel gene ef7 conferring an extremely long basic vegetative growth phase in rice. Theor Appl Genet 119(4):675–684PubMedCrossRefGoogle Scholar
  55. Zhang Q, Shen BZ, Dai XK, Mei MH, Saghai Maroof MA, Li ZB (1994) Using bulked extremes and recessive class to map genes for photoperiod-sensitive genic male sterility in rice. Proc Natl Acad Sci USA 91(18):8675–8679PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2011

Authors and Affiliations

  • X. F. Bian
    • 1
  • X. Liu
    • 1
  • Z. G. Zhao
    • 1
  • L. Jiang
    • 1
  • H. Gao
    • 1
  • Y. H. Zhang
    • 1
  • M. Zheng
    • 1
  • L. M. Chen
    • 1
  • S. J. Liu
    • 1
  • H. Q. Zhai
    • 2
  • J. M. Wan
    • 1
    • 2
  1. 1.National Key Laboratory for Crop Genetics and Germplasm Enhancement, Jiangsu Plant Gene Engineering Research CenterNanjing Agricultural UniversityNanjingChina
  2. 2.Institute of Crop Science, The National Key Facility for Crop Gene Resources and Genetic ImprovementChinese Academy of Agricultural Sciences (CAAS)BeijingChina

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