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Accumulation of additive effects generates a strong photoperiod sensitivity in the extremely late-heading rice cultivar ‘Nona Bokra’

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Abstract

Many rice cultivars that originated from lower-latitude regions exhibit a strong photoperiod sensitivity (PS) and show extremely late heading under long-day conditions. Under natural day-length conditions during the cropping season in Japan, the indica rice cultivar ‘Nona Bokra’ from India showed extremely late heading (202 days to heading) compared to the japonica cultivar ‘Koshihikari’ (105 days), from Japan. To elucidate the genetic factors associated with such extremely late heading, we performed quantitative trait locus (QTL) analyses of heading date using an F2 population and seven advanced backcross progeny (one BC1F2 and six BC2F2) derived from a cross between ‘Nona Bokra’ and ‘Koshihikari’. The analyses revealed 12 QTLs on seven chromosomes. The ‘Nona Bokra’ alleles of all QTLs contributed to an increase in heading date. Digenic interactions were rarely observed between QTLs. Based on the genetic parameters of the QTLs, such as additive effects and percentage of phenotypic variance explained, these 12 QTLs are likely generate a large proportion of the phenotypic variation observed in the heading dates between ‘Nona Bokra’ and ‘Koshihikari’. Comparison of chromosomal locations between heading date QTLs detected in this study and QTLs previously identified in ‘Nipponbare’ × ‘Kasalath’ populations revealed that eight of the heading date QTLs were recognized nearby the Hd1, Hd2, Hd3a, Hd4, Hd5, Hd6, Hd9, and Hd13. These results suggest that the strong PS in ‘Nona Bokra’ was generated mainly by the accumulation of additive effects of particular alleles at previously identified QTLs.

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References

  • Basten CJ, Weir BS, Zeng ZB (1994) Zmap—a QTL cartographer. In: Smith C, Gavora JS, Chesnais BBJ, Fairfull W, Gibson JP, Kennedy BW, Burnside EB (eds) Proceedings of the 5th world congress on genetics applied to livestock production: computing strategies and software, Guelph, Ontario, Canada, vol 22. Organizing Committee, 5th World Congress on Genetics Applied to Livestock Production, pp. 65–66

  • Churchill GA, Doerge RW (1994) Empirical threshold values for quantitative trait mapping. Genetics 138:963–971

    PubMed  CAS  Google Scholar 

  • 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 18:926–936

    Article  PubMed  CAS  Google Scholar 

  • Ebitani T, Takeuchi Y, Nonoue Y, Yamamoto T, Takeuchi K, Yano M (2005) Construction and evaluation of chromosome segment substitution lines carrying overlapping chromosome segments of indica rice cultivar ‘Kasalath’ in a genetic background of japonica elite cultivar ‘Koshihikari’. Breed Sci 55:65–73

    Article  CAS  Google Scholar 

  • Fujino K, Sekiguchi H (2005a) Identification of QTLs conferring genetic variation for heading date among rice varieties at the northern-limit of rice cultivation. Breed Sci 55:141–146

    Article  CAS  Google Scholar 

  • Fujino K, Sekiguchi H (2005b) Mapping of QTLs conferring extremely early heading in rice (Oryza sativa L.). Theor Appl Genet 111:393–398

    Article  CAS  Google Scholar 

  • Harushima Y, Yano M, Shomura A, Sato M, Shimano T, Kuboki Y, Yamamoto T, Lin SY, Antonio BA, Parco A, Kajiya H, Huang N, Yamamoto K, Nagamura Y, Kurata N, Khush GS, Sasaki T (1998) A high-density rice genetic linkage map with 2275 markers using a single F2 population. Genetics 148:479–494

    PubMed  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(2):677–684

    Article  PubMed  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  PubMed  CAS  Google Scholar 

  • Hosoi N (1976) Studies on meteorological fluctuation on the growth of rice plants. I Varietal differences of the heading response to temperature in paddy rice plants ((Japonica). Jpn J Breed 26(4):328–338 (in Japanese)

    Google Scholar 

  • Izawa T, Takahashi Y, Yano M (2003) Comparative biology comes to bloom: genomic and genetic comparison of flowering pathways in rice and Arabidopsis. Curr Opin Plant Biol 6:113–120

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Lander ES, Green P, Abrahamson J, Barlow A, Daley MJ, Lincoln SE, Newburg L (1987) MAPMAKER: an interactive computer package for constructing primary genetic linkage maps of experimental and natural populations. Genomics 1:174–181

    Article  PubMed  CAS  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, Yano M (2000) Characterization and detection of epistatic interactions of 3 QTLs, Hd1, Hd2, Hd3, controlling heading date in rice using nearly isogenic lines. Theor Appl Genet 101:1021–1028

    Article  CAS  Google Scholar 

  • Lin HX, 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 52:35–41

    Article  CAS  Google Scholar 

  • Lin HX, Liang ZW, Sasaki T, Yano M (2003a) Fine mapping and characterization of quantitative trait loci Hd4 and Hd5 controlling heading date in rice. Breed Sci 53:51–59

    Article  CAS  Google Scholar 

  • Lin HX, Zhu MZ, Yano M, Gao JP, Liang ZW, Su WA, Hu XH, Ren ZH, Chao DY (2003b) QTL for Na+ and K+ uptake of the shoots and roots controlling rice salt tolerance. Theor Appl Genet 108(2):253–260

    Article  Google Scholar 

  • Lu C, Shen L, Tan Z, Xu Y, He P, Chen Y, Zhu L (1996) Comparative mapping of QTLs for agronomic traits of rice across environments using a doubled haploid population. Theor Appl Genet 93:1211–1217

    Article  CAS  Google Scholar 

  • Monna L, Lin HX, 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 104:772–778

    Article  PubMed  CAS  Google Scholar 

  • Murray MG, Thompson WF (1980) Rapid isolation of high molecular weight plant DNA. Nucleic Acids Res 8:4321–4325

    Article  PubMed  CAS  Google Scholar 

  • Oka HI (1958) Photoperiodic adaptation to latitude in rice varieties. Phyton 11(2):153–160

    Google Scholar 

  • Septiningsih EM, Prasetiyono J, Lubis E, Tai TH, Tjubaryat T, Moeljopawiro S, McCouch SR (2003) Identification of quantitative trait loci for yield and yield components in an advanced backcross population derived from the Oryza sativa variety IR64 and the wild relative O. rufipogon. Theor Appl Genet 107:1419–1432

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Takeuchi Y, Lin SY, Sasaki T, Yano M (2003) Fine linkage mapping enables dissection of closely linked quantitative trait loci for seed dormancy and heading in rice. Theor Appl Genet 107:1174–1180

    Article  PubMed  CAS  Google Scholar 

  • Tanksley SD (1993) Mapping polygenes. Annu Rev Genet 27:205–233

    Article  PubMed  CAS  Google Scholar 

  • Thomson MJ, Tai TH, McClung AM, Lai XH, Hinga ME, Lobos KB, Xu Y, Martinez CP, McCouch SR (2003) Mapping quantitative trait loci for yield, yield components and morphological traits in an advanced backcross population between Oryza rufipogon and the Oryza sativa cultivar Jefferson. Theor Appl Genet 107:479–493

    Article  PubMed  CAS  Google Scholar 

  • Wu J, Maehara T, Shimokawa T, Yamamoto S, Harada C, Takazaki Y, Ono N, Mukai Y, Koike K, Yazaki J, Fujii F, Shomura A, Ando T, Kono I, Waki K, Yamamoto K, Yano M, Matsumoto T, Sasaki T (2002) A comprehensive rice transcript map containing 6591 EST sites. Plant Cell 14:525–535

    Article  PubMed  CAS  Google Scholar 

  • Xiao J, Li J, Yuan L, Tanksley SD (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  Google Scholar 

  • Yamamoto T, Kuboki Y, Lin SY, Sasaki T, Yano M (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 HX, Sasaki T, Yano M (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

    PubMed  CAS  Google Scholar 

  • Yamamoto T, Taguchi-Shiobara F, Ukai Y, Sasaki T, Yano M (2001) Mapping quantitative trait loci for days-to-heading, and culm, panicle and internode lengths in a BC1F3 population using an elite rice variety, Koshihikari, as the recurrent parent. Breed Sci 51:63–71

    Article  CAS  Google Scholar 

  • Yano M, Sasaki T (1997) Genetic and molecular dissection of quantitative traits in rice. Plant Mol Biol 35:145–153

    Article  PubMed  CAS  Google Scholar 

  • Yano M, Harushima Y, Nagamura Y, Kurata N, Minobe Y, Sasaki T (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, Yamanouchi U, Monna L, Fuse T, Baba T, Yamamoto K, Umehara Y, Ngamura 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 12:2473–2484

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Yokoo M, Kikuchi F, Nakane A, Fujimaki H (1980) Genetical analysis of heading time by aid of close linkage with blast resistance in rice (in Japanese). Bull Natl Inst Agric Sci Ser D31:95–126

    Google Scholar 

  • Yu SB, Li JX, Xu CG, Tan YF, Li XH, Zhang Q (2002) Identification of quantitative trait loci and epistatic interactions for plant height and heading date in rice. Theor Appl Genet 104:619–625

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

We thank Dr. T. Hayashi for his statistical advice in the QTL analyses. This work was supported by a grant from the Bio-oriented Technology Research Advancement Institution and the Ministry of Agriculture, Forestry and Fisheries (Green Technology Project IP-1001).

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Author notes

  1. Z. W. Liang

    Present address: Northeast Institute of Geography and Agricultural Ecology, Chinese Academy of Science, Changchun, 130012, People’s Republic of China

  2. H. X. Lin

    Present address: Shanghai Institute of Plant Physiology and Ecology, Chinese Academy of Science, Shanghai, 200032, People’s Republic of China

Authors and Affiliations

  1. National Institute of Agrobiological Sciences, 2-1-2 Kannondai, Tsukuba, Ibaraki, 305-8602, Japan

    Y. Uga, Z. W. Liang, H. X. Lin, S. Yamamoto, U. Yamanouchi & M. Yano

  2. Institute of the Society for Techno-innovation of Agriculture, Forestry and Fisheries, Tsukuba, Ibaraki, 305-0854, Japan

    Y. Nonoue

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  1. Y. Uga
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  2. Y. Nonoue
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  3. Z. W. Liang
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  4. H. X. Lin
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  5. S. Yamamoto
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  6. U. Yamanouchi
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Correspondence to M. Yano.

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Communicated by C. Hackett.

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Uga, Y., Nonoue, Y., Liang, Z.W. et al. Accumulation of additive effects generates a strong photoperiod sensitivity in the extremely late-heading rice cultivar ‘Nona Bokra’. Theor Appl Genet 114, 1457–1466 (2007). https://doi.org/10.1007/s00122-007-0534-0

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  • DOI: https://doi.org/10.1007/s00122-007-0534-0

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