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.
Similar content being viewed by others
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
References
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 18:79–91
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 95:553–567
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):419–429
Dellaporta S, Wood J, Hicks J (1983) A plant DNA minipreparation: VersionII. Plant Mol Biol Rep 1:19–21
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):926–936
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):999–1010
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):719–722
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):271–282
Honma T, Goto K (2001) Complexes of MADS-box proteins are sufficient to convert leaves into floral organs. Nature 409(6819):525–529
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 31:239–250
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):113–120
Jones MP, Mande S, Aluko K (1997) Diversity and potential of Oryza glaberrima Steud. in upland rice breeding. Jpn J Breed 47:395–398
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):1962–1965
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):183–198
Khush GS (1997) Origin, dispersal, cultivation and variation of rice. Plant Mol Biol 35(1–2):25–34
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):1484–1494
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):1960–1962
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):1096–1105
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):3443–3450
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):4063–4070
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):2366–2376
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):832–843
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):18–30
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):35–41
Linares OF (2002) African rice (Oryza glaberrima): history and future potential. Proc Natl Acad Sci USA 99(25):16360–16365
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):1481–1491
Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2 −ΔΔCT method. Methods 25(4):402–408
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):1425–1435
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):199–207
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):772–778
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):613–623
Nei M (1987) Molecular evolutionary genetics. Columbia University Press, New York, pp 106–107
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):885–900
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):1579–1582
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):1018–1029
Rohlf E (1992) Numerical taxonomy and multivariate analysis system. NTSYS-pc program. Applied Biostatistics Inc., Setauket
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):1412–1427
Sanguinetti C, Dias N, Simpson A (1994) Rapid silver staining and recover of PCR products separated on polyacrylamide gels. Biotechniques 17:915–919
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 33:111–118
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):517–527
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):931–936
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):1005–1022
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):3311–3325
Tsai K (1986) Genes controlling heading time found in a tropical Japonica variety. Rice Genet Newslett 3:71–73
Wang JW, Czech B, Weigel D (2009) miR156-regulated SPL transcription factors define an endogenous flowering pathway in Arabidopsis thaliana. Cell 138(4):738–749
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):1747–1758
Wu G, Poethig RS (2006) Temporal regulation of shoot development in Arabidopsis thaliana by miR156 and its target SPL3. Development 133(18):3539–3547
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):12915–12920
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):761–767
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
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):45–59
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):495–500
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):2473–2484
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):675–684
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):8675–8679
Acknowledgments
We thank Professor Tao Dayun, Yunnan Academy of Agricultural Sciences, for kindly providing us with the Dianjingyou 1 (DJY1) and near-isogenic line (NIL). This research is supported by the grants from the National Natural Science Foundation of China (30871497), National Transform Science and Technology Program (2008ZX08001-06), Jiangsu Science and Technology Development Program (BE2009301-3), Doctor Foundation of Education Development of China (20090097110011), the earmarked fund for Modern Agro-industry Technology Research System and Jiangsu PAPD Program.
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by K. Chong.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Bian, X.F., Liu, X., Zhao, Z.G. et al. Heading date gene, dth3 controlled late flowering in O. Glaberrima Steud. by down-regulating Ehd1 . Plant Cell Rep 30, 2243–2254 (2011). https://doi.org/10.1007/s00299-011-1129-4
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00299-011-1129-4