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Theoretical and Applied Genetics

, Volume 120, Issue 5, pp 895–908 | Cite as

Dissection of a QTL reveals an adaptive, interacting gene complex associated with transgressive variation for flowering time in rice

  • Luis F. Maas
  • Anna McClung
  • Susan McCouch
Original Paper

Abstract

A days to heading QTL (dth1.1) located on the short arm of rice chromosome 1 was sub-divided into eight sub-introgression lines (SILs) to analyze the genetic basis of transgressive variation for flowering time. Each SIL contained one or more introgression(s) from O. rufipogon in the genetic background of the elite Oryza sativa cultivar, Jefferson. Each introgression was defined at high resolution using molecular markers and those in the dth1.1 region were associated with the presence of one or more flowering time genes (GI, SOC1, FT-L8, EMF1, and PNZIP). SILs and controls were evaluated for flowering time under both short- and long-day growing conditions. Under short-day lengths, lines with introgressions carrying combinations of linked flowering time genes (GI/SOC1, SOC1/FT-L8, GI/SOC1/FT-L8 and EMF1/PNZIP) from the late parent, O. rufipogon, flowered earlier than the recurrent parent, Jefferson, while recombinant lines carrying smaller introgressions marked by the presence of GI, SOC1, EMF1 or PNZIP alone no longer flowered early. Under long-day length, lines carrying SOC1/FT-L8, SOC1 or PNZIP flowered early, while those carrying GI or EMF1 delayed flowering. Across all experiments and in the field, only SIL_SOC1/FT-L8 was consistently early. A preliminary yield evaluation indicated that the transgressive early flowering observed in several of the SILs was also associated with a measurable and positive effect on yield. These SILs represent a new source of variation that can be used in breeding programs to manipulate flowering time in rice cultivars without the reduction in yield that is often associated with early maturing phenotypes.

Keywords

Flowering Time Early Flowering Photoperiod Sensitivity Ratoon Crop Tropical Japonica 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Notes

Acknowledgments

We would like to thank Mrs. Marie Lavallard and the Department of Plant Breeding and Genetics for financial support for the PhD program of LFM (via a Frank T. Rhodes Fellowship), the National Science Foundation (Grant DBI #0606461 to SMc) for research funding, Lisa Polewczak for assistance with the field work in the Dale Bumpers National Rice Research Center in Stuttgart, AR and the USDA-ARS Rice Research Unit in Beaumont, TX. We express our gratitude to Michael Thomson and Jeremy Edwards for seeds from the parental pre-SILs provided for this study, and to Michael Gore and Walter de Jong for constructive comments and suggestions during manuscript preparation. We gratefully acknowledge Lois Swales for her assistance in preparing the figures and for formatting the manuscript.

Supplementary material

122_2009_1219_MOESM1_ESM.pdf (383 kb)
Supplementary Fig. 1. Genomic distribution of homologous flowering time genes in Arabidopsis and O. sativa. (PDF 383 kb)
122_2009_1219_MOESM2_ESM.xls (40 kb)
Supplementary Table 1. List of indel and SSR markers, chromosomal locations, primer sequences and expected size (bp) in cv Nipponbare. (XLS 40 kb)
122_2009_1219_MOESM3_ESM.xls (18 kb)
Supplementary Table 2. Summary of agronomic trait means in SILs and parental lines. (XLS 18 kb)

References

  1. Altschul SF, Gish W, Miller W, Myer EW, Lipman DJ (1990) Basic local alignment search tool. Mol Biol 215:403–410Google Scholar
  2. Blazquez MA (2000) Flower development pathways. J Cell Sci 113:3547–3548PubMedGoogle Scholar
  3. Cai H, Morishima H (2002) QTL clusters reflect character associations in wild and cultivated rice. Theor Appl Genet 104:1217–1228CrossRefPubMedGoogle Scholar
  4. Chardon F, Damerval C (2005) Phylogenomic analysis of the PEBP gene family in cereals. J Mol Evol 61:579–590CrossRefPubMedGoogle Scholar
  5. Doi K, Yoshimura A, Iwata N (1998) RFLP mapping and QTL analysis of heading date and pollen sterility using backcross populations between Oryza sativa L. and Oryza glaberrima Steud. Breed Sci 48:395–399Google Scholar
  6. 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 18:926–936CrossRefPubMedGoogle Scholar
  7. Garner WW, Allard HA (1920) Effect of the relative length of day and night and other factors of the environment on growth and reproduction in plants. J Agric Res 18:553–606Google Scholar
  8. Han B, Xue Y (2003) Genome-wide intraspecific DNA-sequence variations in rice. Curr Opin Plant Biol 6:134–138CrossRefPubMedGoogle Scholar
  9. Hayama R, Coupland G (2004) The molecular basis of diversity in the photoperiodic flowering responses of Arabidopsis and rice. Plant Physiol 135:677–684CrossRefPubMedGoogle Scholar
  10. Hayama R, Yokoi S, Tamaki S, Yano M, Shimamoto K (2003) Adaptation of photoperiodic control pathways produces short-day flowering in rice. Nature 422:719–722CrossRefPubMedGoogle Scholar
  11. Huang X, Lu G, Zhao Q, Liu X, Han B (2008) Genome-wide analysis of transposon insertion polymorphisms reveals intraspecific variation in cultivated rice. Plant Physiol 48:25–40CrossRefGoogle Scholar
  12. Izawa T, Oikawa T, Sugiyama N, Tanisaka T, Yano M, Shimamoto K (2002) Phytochrome mediates the external light signal to repress FT orthologs in photoperiodic flowering of rice. Genes Dev 16:2006–2020CrossRefPubMedGoogle Scholar
  13. 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 6:113–120CrossRefPubMedGoogle Scholar
  14. 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 145:1484–1494CrossRefPubMedGoogle Scholar
  15. Kohn JR, Leyva N, Dossey R, Sobral B, Morishima H (1997) Quantitative trait locus analysis of trait variation among annual and perennial ecotypes of Oryza rufipogon. Int Rice Res Notes 22:4–5Google Scholar
  16. 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 43:1096–1105CrossRefPubMedGoogle Scholar
  17. Komiya R, Ikegami A, Tamaki S, Yokoi S, Shimamoto K (2008) HD3A and RFT1 are essential for flowering in rice. Development 135:767–774CrossRefPubMedGoogle Scholar
  18. Matsubara K, Yamanouchi U, Wang Z-X, Minobe Y, Izawa T, Yano M (2008) EHD2, a rice ortholog of the maize INDETERMINATE1 gene, promotes flowering by up regulating EHD1. Plant Physiol 148:1425–1435CrossRefPubMedGoogle Scholar
  19. Panaud O, Chen X, McCouch S (1996) Development of microsatellite markers and characterization of simple sequence length polymorphism (SSLP) in rice (Oryza sativa L.). Mol Gen Genet 252:597–607PubMedGoogle Scholar
  20. Paris M, Carter M (2000) Cereal DNA: a rapid high-throughput extraction method for marker assisted selection. Plant Mol Biol Report 18:357–360CrossRefGoogle Scholar
  21. 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 285:1579–1582CrossRefPubMedGoogle Scholar
  22. Paterson AH, Bowers JE, Feltus FA, Tang H, Lin L, Wang X (2009) Comparative genomics of grasses promises a bountiful harvest. Plant Physiol 149:125–131CrossRefPubMedGoogle Scholar
  23. Putterill J, Laurie R, Macknight R (2004) It’s time to flower: the genetic control of flowering time. Bioessays 26:363–373CrossRefPubMedGoogle Scholar
  24. Salse J, Piegu B, Cooke R, Delseny M (2002) Synteny between Arabidopsis thaliana and rice at the genome level: a tool to identify conservation in the ongoing rice genome sequencing project. Nucleic Acids Res 30:2316–2328CrossRefPubMedGoogle Scholar
  25. Takahashi Y, Teshima KM, Yokoi S, Innan H, Shimamoto K (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 106:4555–4560CrossRefPubMedGoogle Scholar
  26. 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 107:479–493CrossRefPubMedGoogle Scholar
  27. Thomson MJ, Edwards JD, Septiningsih EM, Harrington SE, McCouch SR (2006) Substitution mapping of dth1.1, a flowering-time quantitative trait locus (QTL) associated with transgressive variation in rice, reveals multiple sub-QTL. Genetics 172:2501–2514CrossRefPubMedGoogle Scholar
  28. Tsuji H, Tamaki S, Komiya R, Shimamoto K (2008) Florigen and the photoperiodic control of flowering in rice. Rice 1:25–35CrossRefGoogle Scholar
  29. Turck F, Fornara F, Coupland G (2008) Regulation and identity of florigen: FLOWERING LOCUS T moves center stage. Annl Rev Plant Biol 59:573CrossRefGoogle Scholar
  30. Vitte C, Panaud O, Quesneville H (2007) LTR retrotransposons in rice (Oryza sativa L.): recent burst amplifications followed by rapid DNA loss. BMC Genomics 8:218–233CrossRefPubMedGoogle Scholar
  31. Xiao J, Li J, Grandillo S, Ahn SN, Yuan L, Tanksley SD, McCouch SR (1998) Identification of trait-improving quantitative trait loci alleles from a wild rice relative, Oryza rufipogon. Genetics 150:899–909PubMedGoogle Scholar
  32. 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 40:761–767CrossRefPubMedGoogle Scholar
  33. Yamamoto T, Yonemaru J, Yano M (2009) Towards the understanding of complex traits in rice: substantially or superficially? DNA Res 16:141–154CrossRefPubMedGoogle Scholar
  34. 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 12:2473–2484CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag 2009

Authors and Affiliations

  1. 1.Department of Plant Breeding and GeneticsCornell UniversityIthacaUSA
  2. 2.USDA-ARS, Dale Bumpers National Rice Research CenterStuttgartUSA

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