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Genetic control of flowering time in rice: integration of Mendelian genetics and genomics

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Integration of previous Mendelian genetic analyses and recent molecular genomics approaches, such as linkage mapping and QTL cloning, dramatically strengthened our current understanding of genetic control of rice flowering time.

Abstract

Flowering time is one of the most important agronomic traits for seed production in rice (Oryza sativa L.). It is controlled mainly by genes associated with photoperiod sensitivity, particularly in short-day plants such as rice. Since the early twentieth century, rice breeders and researchers have been interested in elucidating the genetic basis of flowering time because its modification is important for regional adaptation and yield optimization. Although flowering time is a complex trait controlled by many quantitative trait loci (QTLs), classical genetic studies have shown that many associated genes are inherited in accordance with Mendelian laws. Decoding the rice genome sequence opened a new era in understanding the genetic control of flowering time on the basis of genome-wide mapping and gene cloning. Heading date 1 (Hd1) was the first flowering time QTL to be isolated using natural variation in rice. Recent accumulation of information on rice genome has facilitated the cloning of other QTLs, including those with minor effects on flowering time. This information has allowed us to rediscover some of the flowering genes that were identified by classical Mendelian genetics. The genes characterized so far, including Hd1, have been assigned to specific photoperiod pathways. In this review, we provide an overview of the studies that led to an in-depth understanding of the genetic control of flowering time in rice, and of the current state of improving and fine-tuning this trait for rice breeding.

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References

  • Bentley A, Jensen E, Mackay I et al (2013) Flowering time. In: Kole C (ed) Genomics and breeding for climate-resilient crops, vol 2. Springer-Verlag, Berlin, pp 1–66

    Chapter  Google Scholar 

  • Bian XF, Liu X, Zhao ZG et al (2011) Heading date gene, dth3 controlled late flowering in O. glaberrima Steud. by down-regulating Ehd1. Plant Cell Rep 30:2243–2254

    Article  CAS  PubMed  Google Scholar 

  • Chandraratna MF (1953) A gene for photoperiod sensitivity in rice linked with apiculus colour. Nature 171:1162–1163

    Article  CAS  PubMed  Google Scholar 

  • Chandraratna MF (1955) Genetics of photoperiod sensitivity in rice. J Genet 53:215–223

    Article  Google Scholar 

  • Chandraratna MF (1964) Flowering in rice with particular reference to photoperiod control. In: Chandraratna MF (ed) Genetics and breeding of rice. Longmans, London, pp 181–214

    Google Scholar 

  • Chao LF (1928) Linkage studies in rice. Genetics 13:133–169

    CAS  PubMed  PubMed Central  Google Scholar 

  • Chen J, Li X, Cheng C et al (2014) Characterization of epistatic interaction of QTLs LH8 and EH3 controlling heading date in rice. Sci Rep 4:4263

    PubMed  PubMed Central  Google Scholar 

  • Choi SC, Lee S, Kim SR et al (2014) Trithorax group protein Oryza sativa Trithorax1 controls flowering time in rice via interaction with early heading date3. Plant Physiol 164:1326–1337

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dai C, Xue HW (2010) Rice early flowering1, a CKI, phosphorylates DELLA protein SLR1 to negatively regulate gibberellin signalling. EMBO J 29:1916–1927

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dai X, Ding Y, Tan L et al (2012) LHD1, an allele of DTH8/Ghd8, controls late heading date in common wild rice (Oryza rufipogon). J Integr Plant Biol 54:790–799

    Article  CAS  PubMed  Google Scholar 

  • Doi K, Izawa T, Fuse T et al (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 18:926–936

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ebana K, Shibaya T, Wu J et al (2011) Uncovering of major genetic factors generating naturally occurring variation in heading date among Asian rice cultivars. Theor Appl Genet 122:1199–1210

    Article  PubMed  PubMed Central  Google Scholar 

  • Fujino K, Wu J, Sekiguchi H et al (2010) Multiple introgression events surrounding the Hd1 flowering-time gene in cultivated rice, Oryza sativa L. Mol Genet Genom 284:137–146

    Article  CAS  Google Scholar 

  • Fujino K, Yamanouchi U, Yano M (2013) Roles of the Hd5 gene controlling heading date for adaptation to the northern limits of rice cultivation. Theor Appl Genet 126:611–618

    Article  CAS  PubMed  Google Scholar 

  • Fuke Y (1955) On the genes controlling the heading time of leading rice varieties in Japan and their specific response to day length and temperature. Bull Nat Inst Agric Sci Ser D 5:1–71 (in Japanese with English summary)

    Google Scholar 

  • Gao H, Zheng XM, Fei G et al (2013) Ehd4 encodes a novel and Oryza-genus-specific regulator of photoperiodic flowering in rice. PLoS Genet 9:e1003281

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Garner WW, Allard HA (1920) Agricultural United States Department of Agriculture and for the Association. J Agric Res XVIII:553–606

  • Garner WW, Allard HA (1923) Further studies in photoperiodism, the response of the plant to relative length of day and night. J Agric Res XXIII:871–920

  • Gómez-Ariza J, Galbiati F, Goretti D et al (2015) Loss of floral repressor function adapts rice to higher latitudes in Europe. J Exp Bot 66:2027–2039

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Hayama R, Coupland G (2004) The molecular basis of diversity in the photoperiodic flowering responses of Arabidopsis and Rice. Plant Physiol 135:677–684

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hayama R, Izawa T, Shimamoto K (2002) Isolation of rice genes possibly involved in the photoperiodic control of flowering by a fluorescent differential display method. Plant Cell Physiol 43:494–504

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Hori K, Kataoka T, Miura K et al (2012) Variation in heading date conceals quantitative trait loci for other traits of importance in breeding selection of rice. Breed Sci 62:223–234

    Article  PubMed  PubMed Central  Google Scholar 

  • Hori K, Ogiso-Tanaka E, Matsubara K et al (2013) Hd16, a gene for casein kinase I, is involved in the control of rice flowering time by modulating the day-length response. Plant J 76:36–46

    CAS  PubMed  PubMed Central  Google Scholar 

  • Hori K, Nonoue Y, Ono N et al (2015) Genetic architecture of variation in heading date among Asian rice accessions. BMC Plant Biol 15:1–16

    Article  Google Scholar 

  • Hoshino Y (1915) On the inheritance of the flowering time in peas and rice. J Coll Agric Tohoku Imp Univ Sapporo, Japan 6:229–288

    Google Scholar 

  • Huang X, Zhao Y, Wei X et al (2012) Genome-wide association study of flowering time and grain yield traits in a worldwide collection of rice germplasm. Nat Genet 44:32–39

    Article  CAS  Google Scholar 

  • Ichitani K, Okumoto Y, Tanisaka T (1998a) Genetic analyses of low photoperiod sensitivity of rice varieties from the northernmost regions of Japan. Plant Breed 117:543–547

    Article  Google Scholar 

  • Ichitani K, Okumoto Y, Tanisaka T (1998b) Genetic analysis of the rice cultivar Kasalath with special reference to two photoperiod sensitivity loci, E1 and Se-1. Breed Sci 48:51–57

    Google Scholar 

  • Itoh H, Nonoue Y, Yano M et al (2010) A pair of floral regulators sets critical day length for Hd3a florigen expression in rice. Nat Genet 42:635–638

    Article  CAS  PubMed  Google Scholar 

  • Izawa T (2007) Daylength measurements by rice plants in photoperiodic short-day flowering. In: Kwang WJ (ed) International Review of Cytology. Academic Press, Cambridge, pp 191–222

    Google Scholar 

  • Izawa T, Oikawa T, Tokutomi S et al (2000) Phytochromes confer the photoperiodic control of flowering in rice (a short-day plant). Plant J 22:391–399

    Article  CAS  PubMed  Google Scholar 

  • Jodon NE (1940) Inheritance and linkage relationships of a chlorophyll mutation in rice. Agron J 32:342–346

    Article  Google Scholar 

  • Jones JW (1928) Inheritance of earliness and other agronomic characters in rice. J Agric Res 36:581–601

    Google Scholar 

  • Jones JW (1933) Inheritance of characters in rice. J Agric Res 47:771–782

    Google Scholar 

  • Jones JW, Adair CR, Beachell HM et al (1935) Inheritance of earliness and length of kernel in rice. J Amer Soc Agron 27:910–921

    Article  Google Scholar 

  • Khun LH, Hiraiwa M, Sato S et al (2004) Location of new gene for late heading in rice, Oryza sativa L. using interchange homozygotes. Breed Sci 54:259–263

    Article  CAS  Google Scholar 

  • Khun LH, Miyaji S, Motomura K et al (2006) Trisomic analysis of new gene for late heading in rice, Oryza sativa L. Euphytica 151:235–241

    Article  CAS  Google Scholar 

  • Kim SL, Lee S, Kim HJ et al (2007) OsMADS51 is a short-day flowering promoter that functions upstream of Ehd1, OsMADS14, and Hd3a. Plant Physiol 145:1484–1494

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kojima S, Takahashi Y, Kobayashi Y et al (2002) Hd3a, a rice ortholog of the Arabidopsis FT gene, promotes transition to flowering downstream of Hd1 under short-day conditions. Plant Cell Physiol 43:1096–1105

    Article  CAS  PubMed  Google Scholar 

  • Komiya R, Ikegami A, Tamaki S et al (2008) Hd3a and RFT1 are essential for flowering in rice. Development 135:767–774

    Article  CAS  PubMed  Google Scholar 

  • Komiya R, Yokoi S, Shimamoto K (2009) A gene network for long-day flowering activates RFT1 encoding a mobile flowering signal in rice. Development 136:3443–3450

    Article  CAS  PubMed  Google Scholar 

  • Koo BH, Yoo SC, Park JW et al (2013) Natural variation in OsPRR37 regulates heading date and contributes to rice cultivation at a wide range of latitudes. Mol Plant 6:1877–1888

    Article  CAS  PubMed  Google Scholar 

  • Kuromori T, Takahashi S, Kondou Y et al (2009) Phenome analysis in plant species using loss-of-function and gain-of-function mutants. Plant Cell Physiol 50:1215–1231

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kwon CT, Yoo SC, Koo BH et al (2014) Natural variation in Early flowering1 contributes to early flowering in japonica rice under long days. Plant, Cell Environ 37:101–112

    Article  CAS  Google Scholar 

  • Lee S, Kim J, Han JJ et al (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 38:754–764

    Article  CAS  PubMed  Google Scholar 

  • Lee YS, Jeong DH, Lee DY et al (2010) OsCOL4 is a constitutive flowering repressor upstream of Ehd1 and downstream of OsphyB. Plant J 63:18–30

    CAS  PubMed  Google Scholar 

  • Li Z, Pinson SRM, Stansel JW et al (1995) Identification of quantitative trait loci (QTLs) for heading date and plant height in cultivated rice (Oryza sativa L.). Theor Appl Genet 91:374–381

    CAS  PubMed  Google Scholar 

  • Lim J, Moon YH, An G et al (2000) Two rice MADS domain proteins interact with OsMADS1. Plant Mol Biol 44:513–527

    Article  CAS  PubMed  Google Scholar 

  • Lin SY, Sasaki T, Yano M (1998) Mapping quantitative trait loci controlling seed dormancy and heading date in rice, Oryza sativa L., using backcross inbred lines. Theor Appl Genet 96:997–1003

    Article  CAS  Google Scholar 

  • Lin HX, Yamamoto T, Sasaki T et al (2000) Characterization and detection of epistatic interactions of 3 QTLs, Hd1, Hd2, and Hd3, controlling heading date in rice using nearly isogenic lines. Theor Appl Genet 101:1021–1028

    Article  CAS  Google Scholar 

  • Lin H, Ashikari M, Yamanouchi U et al (2002) Identification and characterization of a quantitative trait locus, Hd9, controlling heading date in rice. Breed Sci 52:35–41

    Article  CAS  Google Scholar 

  • Lin X, Wu F, Du X et al (2014) The pleiotropic SEPALLATA-like gene OsMADS34 reveals that the ‘empty glumes’ of rice (Oryza sativa) spikelets are in fact rudimentary lemmas. New Phytol 202:689–702

    Article  CAS  PubMed  Google Scholar 

  • Lu SJ, Wei H, Wang Y et al (2012) Overexpression of a transcription factor OsMADS15 modifies plant architecture and flowering time in rice (Oryza sativa L.). Plant Mol Biol Rep 30:1461–1469

    Article  CAS  Google Scholar 

  • Matsubara K, Kono I, Hori K et al (2008a) Novel QTLs for photoperiodic flowering revealed by using reciprocal backcross inbred lines from crosses between japonica rice varieties. Theor Appl Genet 117:935–945

    Article  CAS  PubMed  Google Scholar 

  • Matsubara K, Yamanouchi U, Wang ZX et al (2008b) Ehd2, a rice ortholog of the maize INDETERMINATE1 gene promotes flowering by up-regulating Ehd1. Plant Physiol 148:1425–1435

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Matsubara K, Yamanouchi U, Nonoue Y et al (2011) Ehd3, encoding a plant homeodomain finger-containing protein, is a critical promoter of rice flowering. Plant J 66:603–612

    Article  CAS  PubMed  Google Scholar 

  • Matsubara K, Ogiso-Tanaka E, Hori K et al (2012) Natural variation in Hd17, a homolog of Arabidopsis ELF3 that is involved in rice photoperiodic flowering. Plant Cell Physiol 53:709–716

    Article  CAS  PubMed  Google Scholar 

  • Matsuzaki J, Kawahara Y, Izawa T (2015) Punctual transcriptional regulation by the rice circadian clock under fluctuating field conditions. Plant Cell 27:633–648

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Monden Y, Naito K, Okumoto Y et al (2009) High potential of a transposon mPing as a marker system in japonica × japonica cross in rice. DNA Res 16:131–140

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Monna L, Lin HX, Kojima S et al (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 104:772–778

    Article  CAS  PubMed  Google Scholar 

  • Nemoto Y, Nonoue Y, Yano M et al (2016) Hd1, a CONSTANS orthlog in rice, functions as an Ehd1 repressor through interaction with monocot-specific CCT-domain protein Ghd7. Plant J 86:221–233

    Article  CAS  PubMed  Google Scholar 

  • Nomura M, Yamazaki R (1925) A study of the inheritance of the shooting time in rice. Jpn J Genet 3:112–130 (in Japanese with English summary)

    Article  Google Scholar 

  • Ogiso E, Takahashi Y, Sasaki T et al (2010) The role of casein kinase II in flowering time regulation has diversified during evolution. Plant Physiol 152:808–820

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ogiso-Tanaka E, Matsubara K, Yamamoto S et al (2013) Natural variation of the RICE FLOWERING LOCUS T 1 contributes to flowering time divergence in rice. PLoS ONE 8:e75959

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ohshima I, Kikuchi F, Watanabe Y et al (1993) Analysis of heading time in a cross between two Indica varieties with inhibitor genes for photoperiod sensitivity. Jpn J Breed 43:101–106 (in Japanese with English summary)

    Article  CAS  Google Scholar 

  • Okumoto Y, Tanisaka T (1997) Trisomic analysis of a strong photoperiod-sensitivity gene E1 in rice (Oryza sativa L.). Euphytica 95:301–307

    Article  Google Scholar 

  • Okumoto Y, Tanisaka T, Yanagata H (1991) Heading-time genes of the rice varieties grown in south-west-warm region in Japan. Jpn J Breed 41:135–152 (in Japanese with English summary)

    Article  CAS  Google Scholar 

  • Okumoto Y, Yoshimura A, Tanisaka T et al (1992) Analysis of a rice variety Taichung 65 and its isogenic early-heading lines for late-heading genes E 1 , E 2 and E 3 . Jpn J Breed 42:415–429 (in Japanese with English summary)

    Article  Google Scholar 

  • Okumoto Y, Ichitani K, Inoue H et al (1996) Photoperiod insensitivity gene essential to the varieties grown in the northern limit region of paddy rice (Oryza sativa L.) cultivation. Euphytica 92:63–66

    Article  Google Scholar 

  • Peng LT, Shi ZY, Li L et al (2008) Overexpression of transcription factor OsLFL1 delays flowering time in Oryza sativa. J Plant Physiol 165:876–885

    Article  CAS  PubMed  Google Scholar 

  • Poonyarit M, Mackill DJ, Vergara BS (1989) Genetics of photoperiod sensitivity and critical daylength in rice. Crop Sci 29:647–652

    Article  Google Scholar 

  • Purwestri YA, Ogaki Y, Tamaki S et al (2009) The 14-3-3 protein GF14c acts as a negative regulator of flowering in rice by interacting with the florigen Hd3a. Plant Cell Physiol 50:429–438

    Article  CAS  PubMed  Google Scholar 

  • Ryu CH, Lee S, Cho LH et al (2009) OsMADS50 and OsMADS56 function antagonistically in regulating long day (LD)-dependent flowering in rice. Plant, Cell Environ 32:1412–1427

    Article  CAS  Google Scholar 

  • Saito H, Yuan Q, Okumoto Y et al (2009) Multiple alleles at Early flowering 1 locus making variation in the basic vegetative growth period in rice (Oryza sativa L.). Theor Appl Genet 119:315–323

    Article  CAS  PubMed  Google Scholar 

  • Saito H, Ogiso-Tanaka E, Okumoto Y et al (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 53:717–728

    Article  CAS  PubMed  Google Scholar 

  • Sampath S, Seshu DV (1961) Genetics of photoperiod response in rice. Indian J Genet Plant Breed 21:38–42

    Google Scholar 

  • Sato S, Sakamoto I, Shirakawa K et al (1988) Chromosomal location of an earliness gene Ef 1 of rice, Oryza sativa L. Jpn J Breed 38:385–396

    Article  Google Scholar 

  • Sato S, Ogata K, Shinjyo C (1992) Thermo-sensitive action of an earliness gene Ef-x in rice, Oryza sativa L. Jpn J Genet 67:473–482

    Article  CAS  Google Scholar 

  • Shibaya T, Nonoue Y, Ono N et al (2011) Genetic interactions involved in the inhibition of heading by heading date QTL, Hd2 in rice under long-day conditions. Theor Appl Genet 123:1133–1143

    Article  PubMed  Google Scholar 

  • Shibaya T, Hori K, Ogiso-Tanaka E et al (2016) Hd18, encoding histone acetylase related to Arabidopsis FLOWERING LOCUS D, is involved in the control of flowering time in rice. Plant Cell Physiol. doi:10.1093/pcp/pcw105

    PubMed  Google Scholar 

  • Shrestha R, Gómez-Ariza J, Brambilla V et al (2014) Molecular control of seasonal flowering in rice, arabidopsis and temperate cereals. Ann Bot 114:1445–1458

    Article  PubMed  PubMed Central  Google Scholar 

  • Syakudo K, Kawase T (1953) Studies on the quantitative inheritance (11) A. Rice (Oryza sativa L.) (d) Inheritance of the heading duration and the quantitative function of the causal genes E 1 , E 2 and D 1 . Jpn J Breed 3:6–12 (in Japanese with English summary)

    Article  Google Scholar 

  • Syakudo K, Kawase T, Yoshino K (1954) Studies on the quantitative inheritance (13) A. Rice (Oryza sativa L.) (d) Inheritance of the heading period and the quantitative function of the causal genes in its determination. (2) On the quantitative function of the genes E 3 , E 4 and E 5 . Jpn J Breed 4:83–91 (in Japanese with English summary)

    Article  Google Scholar 

  • Takahashi Y, Shimamoto K (2011) Heading date 1 (Hd1), an ortholog of Arabidopsis CONSTANS, is a possible target of human selection during domestication to diversify flowering times of cultivated rice. Genes Genet Syst 86:175–182

    Article  CAS  PubMed  Google Scholar 

  • Takahashi Y, Shomura A, Sasaki T et al (2001) Hd6, a rice quantitative trait locus involved in photoperiod sensitivity, encodes the alpha subunit of protein kinase CK2. Proc Natl Acad Sci USA 98:7922–7927

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Takahashi Y, Teshima KM, Yokoi S et al (2009) Variations in Hd1 proteins, Hd3a promoters, and Ehd1 expression levels contribute to diversity of flowering time in cultivated rice. Proc Natl Acad Sci USA 106:4555–4560

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Takeuchi Y (2011) Developing isogenic lines of Japanese rice cultivar ‘Koshihikari’ with early and late heading. Jpn Agric Res 45:15–22

    Article  Google Scholar 

  • Takeuchi Y, Ebitani T, Yamamoto T et al (2006) Development of isogenic lines of rice cultivar Koshihikari with early and late heading by marker-assisted selection. Breed Sci 56:405–413

    Article  CAS  Google Scholar 

  • Tamaki S, Matsuo S, Wong HL et al (2007) Hd3a protein is a mobile flowering signal in rice. Science 316:1033–1036

    Article  CAS  PubMed  Google Scholar 

  • Tamura K, Nomura K, Oshima I et al (1998) Identification of restriction fragment length polymorphism markers tightly linked to a major photoperiod sensitivity gene, Se1, and to a blast resistance gene, Piz-t, in rice. SABRAO J Breed Genet 30:61–67

    Google Scholar 

  • Tan J, Jin M, Wang J et al (2016) OsCOL10, a CONSTANS-like gene, functions as a flowering time repressor downstream of Ghd7 in rice. Plant Cell Physiol 57:798–812

    Article  CAS  PubMed  Google Scholar 

  • Thomas B, Vince-Pure D (1997) Photoperiodism in plants, 2nd edn. Academic Press, San Diego

    Google Scholar 

  • Tsai KH (1976) Studies on earliness genes in rice, with special reference to analysis of isoalleles at the E locus. Jpn J Genet 51:115–128

    Article  Google Scholar 

  • Tsai KH (1991) Genes for late heading and their interaction in the background of Taichung 65. In: Rice Genetics II, Proceedings of International Rice Genetics Symposium, IRRI, Manila, pp 211–215

  • Tsai KH (1995) Genetic analysis for heading time in wild rice strains. Jpn J Genet 70:555–562

    Article  Google Scholar 

  • Tsai KH (1999) Genetic analysis for heading time in tropical rice strains. Rice Genet Newslett 16:55–57

    Google Scholar 

  • Tsai KH, Oka HI (1966) Genetic study of yielding capacity and adaptability in crop plants. 2. Analysis of genes controlling heading time in Taichung 65 and other rice varieties. Bot Bull Acad Sin 7:54–70

    Google Scholar 

  • Uwatoko N, Onishi A, Ikeda Y et al (2008) Epistasis among the three major flowering time genes in rice: coordinate changes of photoperiod sensitivity, basic vegetative growth and optimum photoperiod. Euphytica 163:167–175

    Article  CAS  Google Scholar 

  • Vergara BS, Chang TT (1985) The flowering response of the rice plant to photoperiod, 4th edn. IRRI, Manila

    Google Scholar 

  • Wei X, Xu J, Guo H et al (2010) DTH8 suppresses flowering in rice, influencing plant height and yield potential simultaneously. Plant Physiol 153:1747–1758

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wu W, Zheng XM, Lu G et al (2013) Association of functional nucleotide polymorphisms at DTH2 with the northward expansion of rice cultivation in Asia. Proc Natl Acad Sci USA 110:2775–2780

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Xiao J, Li J, Yuan L et al (1996) Identification of QTLs affecting traits of agronomic importance in a recombinant inbred population derived from a subspecific rice cross. Theor Appl Genet 92:230–244

    Article  CAS  PubMed  Google Scholar 

  • Xue W, Xing Y, Weng X et al (2008) Natural variation in Ghd7 is an important regulator of heading date and yield potential in rice. Nat Genet 40:761–767

    Article  CAS  PubMed  Google Scholar 

  • Yamagata H, Okumoto Y, Tanisaka T (1986) Analysis of genes controlling heading time in Japanese rice. In: Rice Genetics, Proceedings of International Rice Genetics Symposium, IRRI, Manila, pp 351–359

  • Yamamoto T, Kuboki Y, Lin SY et al (1998) Fine mapping of quantitative trait loci Hd-1, Hd-2 and Hd-3, controlling heading date of rice, as single Mendelian factors. Theor Appl Genet 97:37–44

    Article  CAS  Google Scholar 

  • Yamamoto T, Lin H, Sasaki T et al (2000) Identification of heading date quantitative trait locus Hd6 and characterization of its epistatic interactions with Hd2 in rice using advanced backcross progeny. Genetics 154:885–891

    CAS  PubMed  PubMed Central  Google Scholar 

  • Yamamoto E, Yonemaru J, Yamamoto T et al (2012) OGRO: the overview of functionally characterized genes in rice online database. Rice 5:26

    Article  PubMed  Google Scholar 

  • Yan WH, Wang P, Chen HX et al (2011) A major QTL, Ghd8, plays pleiotropic roles in regulating grain productivity, plant height, and heading date in rice. Mol Plant 4:319–330

    Article  CAS  PubMed  Google Scholar 

  • Yang J, Lee S, Hang R et al (2013) OsVIL2 functions with PRC2 to induce flowering by repressing OsLFL1 in rice. Plant J 73:566–578

    Article  CAS  PubMed  Google Scholar 

  • Yano M, Harushima Y, Nagamura Y et al (1997) Identification of quantitative trait loci controlling heading date in rice using a high-density linkage map. Theor Appl Genet 95:1025–1032

    Article  CAS  Google Scholar 

  • Yano M, Katayose Y, Ashikari M et al (2000) Hd1, a major photoperiod sensitivity quantitative trait locus in rice, is closely related to the Arabidopsis flowering time gene CONSTANS. Plant Cell 12:2473–2484

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yano M, Kojima S, Takahashi Y et al (2001) Genetic control of flowering time in rice, a short day plant. Plant Physiol 127:1425–1429

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yokoo M, Fujimaki H (1971) Tight linkage of blast-resistance with late maturity observed in different indica varieties of rice. Jpn J Breed 23:35–39 (in Japanese with English summary)

    Article  Google Scholar 

  • Yokoo M, Kikuchi F (1977) Multiple allelism of the locus controlling heading time of rice, detected using linkage with blast-resistance. Japan J Breed 27:123–130

    Article  Google Scholar 

  • Yokoo M, Okuno K (1993) Genetic analysis of earliness mutations induced in the rice variety Norin 8. Japan J Breed 43:1–11

    Article  Google Scholar 

  • Yokoo M, Kikuchi F, Nakane A et al (1980) Genetical analysis of heading time by aid of close linkage with blast resistance. Bull Nat Inst Agric Sci Ser D 31:95–126 (in Japanese with English summary)

    Google Scholar 

  • Yokoo T, Saito H, Yoshitake Y et al (2014) Se14, encoding a JmjC domain-containing protein, plays key roles in long-day suppression of rice flowering through the demethylation of H3K4me3 of RFT1. PLoS ONE 9:1–9

    Article  CAS  Google Scholar 

  • Yonemaru J, Yamamoto T, Fukuoka S et al (2010) Q-TARO: QTL annotation rice online database. Rice 3:194–203

    Article  Google Scholar 

  • Yoshitake Y, Yokoo T, Saito H et al (2015) The effects of phytochrome-mediated light signals on the developmental acquisition of photoperiod sensitivity in rice. Sci Rep 5:7709

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Youens-Clark K, Buckler E, Casstevens T et al (2011) Gramene database in 2010: updates and extensions. Nucleic Acids Res 39:D1085–D1094

    Article  CAS  PubMed  Google Scholar 

  • Yu CJ, Yao YT (1968) Genetische Studien beim Reis. II. Die Koppelung des Langhüllspelzengens mit dem Photoperiodizitätsgen. Bot Bull Acad Sin 9:34–35

    Google Scholar 

  • Yuan Q, Saito H, Okumoto Y et al (2009) Identification of a novel gene ef7 conferring an extremely long basic vegetative growth phase in rice. Theor Appl Genet 119:675–684.Zhao J, Huang X, Ouyang X et al (2012) OsELF3-1, an ortholog of Arabidopsis EARLY FLOWERING 3, regulates rice circadian rhythm and photoperiodic flowering. PLoS One 7:e43705

  • Zhao K, Tung CW, Eizenga GC et al (2011) Genome-wide association mapping reveals a rich genetic architecture of complex traits in Oryza sativa. Nat Commun 2:467

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Zheng XM, Feng L, Wang J et al (2015) Nonfunctional alleles of long-day suppressor genes independently regulate flowering time. J Integr Plant Biol. doi:10.1111/jipb.12383

    Google Scholar 

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Acknowledgments

The research activities at the Institute of Crop Science, NARO (formally National Institute of Agrobiological Sciences), have been supported mainly by the Ministry of Agriculture, Forestry and Fisheries of Japan and the Program for the Promotion of Basic Research Activities for Innovative Biosciences, and partly by the Ministry of Education, Culture, Sports, Science and Technology of Japan.

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Correspondence to Masahiro Yano.

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Communicated by H. Bürstmayr and J. Vollmann.

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Hori, K., Matsubara, K. & Yano, M. Genetic control of flowering time in rice: integration of Mendelian genetics and genomics. Theor Appl Genet 129, 2241–2252 (2016). https://doi.org/10.1007/s00122-016-2773-4

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  • DOI: https://doi.org/10.1007/s00122-016-2773-4

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