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Natural variation in Ghd7 is an important regulator of heading date and yield potential in rice

Abstract

Yield potential, plant height and heading date are three classes of traits that determine the productivity of many crop plants. Here we show that the quantitative trait locus (QTL) Ghd7, isolated from an elite rice hybrid and encoding a CCT domain protein, has major effects on an array of traits in rice, including number of grains per panicle, plant height and heading date. Enhanced expression of Ghd7 under long-day conditions delays heading and increases plant height and panicle size. Natural mutants with reduced function enable rice to be cultivated in temperate and cooler regions. Thus, Ghd7 has played crucial roles for increasing productivity and adaptability of rice globally.

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Figure 1: Performance of Zhenshan 97 and NIL(mh7) planted under natural long-day conditions.
Figure 2: Diurnal expression patterns of NIL(mh7) and NIL(zs7) as indicated by quantitative RT-PCR results.
Figure 3: Expression of Ghd7 in various tissues detected by in situ hybridization with an antisense probe using various tissues of Minghui 63.
Figure 4: Effects of Ghd7 on the stem.

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References

  1. Li, X. et al. Control of tillering in rice. Nature 422, 618–621 (2003).

    Article  CAS  Google Scholar 

  2. Ashikari, M. et al. Cytokinin oxidase regulates rice grain production. Science 309, 741–745 (2005).

    Article  CAS  Google Scholar 

  3. Fan, C. et al. GS3, a major QTL for grain length and weight and minor QTL for grain width and thickness in rice, encodes a putative transmembrane protein. Theor. Appl. Genet. 112, 1164–1171 (2006).

    Article  CAS  Google Scholar 

  4. Song, X.J., Huang, W., Shi, M., Zhu, M.Z. & Lin, H.X.A. QTL for rice grain width and weight encodes a previously unknown RING-type E3 ubiquitin ligase. Nat. Genet. 39, 623–630 (2007).

    Article  CAS  Google Scholar 

  5. Peng, J. et al. 'Green revolution' genes encode mutant gibberellin response modulators. Nature 400, 256–261 (1999).

    Article  CAS  Google Scholar 

  6. Ashikari, M., Wu, J., Yano, M., Sasaki, T. & Yoshimura, A. Rice gibberellin-insensitive dwarf mutant gene Dwarf 1 encodes the alpha-subunit of GTP-binding protein. Proc. Natl. Acad. Sci. USA 96, 10284–10289 (1999).

    Article  CAS  Google Scholar 

  7. Spielmeyer, W., Ellis, M.H. & Chandler, P.M. Semidwarf (sd-1), “green revolution” rice, contains a defective gibberellin 20-oxidase gene. Proc. Natl. Acad. Sci. USA 99, 9043–9048 (2002).

    Article  CAS  Google Scholar 

  8. Itoh, H. et al. A rice semi-dwarf gene, Tan-Ginbozu (D35), encodes the gibberellin biosynthesis enzyme, ent-kaurene oxidase. Plant Mol. Biol. 54, 533–547 (2004).

    Article  CAS  Google Scholar 

  9. Simpson, G.G. & Dean, C. Arabidopsis, the Rosetta stone of flowering time? Science 296, 285–289 (2002).

    Article  CAS  Google Scholar 

  10. Wigge, P.A. et al. Integration of spatial and temporal information during floral induction in Arabidopsis. Science 309, 1056–1059 (2005).

    Article  CAS  Google Scholar 

  11. Abe, M. et al. FD, a bZIP protein mediating signals from the floral pathway integrator FT at the shoot apex. Science 309, 1052–1056 (2005).

    Article  CAS  Google Scholar 

  12. Corbesier, L. et al. FT protein movement contributes to long-distance signalling in floral induction of Arabidopsis. Science 316, 1030–1033 (2007).

    Article  CAS  Google Scholar 

  13. Yano, M. et al. 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 (2000).

    Article  CAS  Google Scholar 

  14. Kojima, S. et al. 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 (2002).

    Article  CAS  Google Scholar 

  15. Hayama, R., Yokoi, S., Tamaki, S., Yano, M. & Shimamoto, K. Adaptation of photoperiodic control pathways produces short-day flowering in rice. Nature 422, 719–722 (2003).

    Article  CAS  Google Scholar 

  16. Tamaki, S., Matsuo, S., Wong, H.L., Yokoi, S. & Shimamoto, K. Hd3a protein is a mobile flowering signal in rice. Science 316, 1033–1036 (2007).

    Article  CAS  Google Scholar 

  17. Takahashi, Y., Shomura, A., Sasaki, T. & Yano, M. 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 (2001).

    Article  CAS  Google Scholar 

  18. Doi, K. et al. 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 (2004).

    Article  CAS  Google Scholar 

  19. Yu, S.B. et al. Importance of epistasis as the genetic basis of heterosis in an elite rice hybrid. Proc. Natl. Acad. Sci. USA 94, 9226–9231 (1997).

    Article  CAS  Google Scholar 

  20. Yu, S.B. et al. Identification of quantitative trait loci and epistatic interactions for plant height and heading date in rice. Theor. Appl. Genet. 104, 619–625 (2002).

    Article  CAS  Google Scholar 

  21. Li, J.X. et al. Analyzing quantitative trait loci for yield using a vegetatively replicated F2 population from a cross between the parents of an elite rice hybrid. Theor. Appl. Genet. 101, 248–254 (2000).

    Article  CAS  Google Scholar 

  22. Xing, Y., Tan, Y.F., Xu, C.G., Hua, J.P. & Sun, X.L. Mapping and isolation of quantitative trait loci controlling plant height and heading date in rice. Acta Bot. Sin. 43, 721–746 (2001).

    CAS  Google Scholar 

  23. Xing, Z. et al. Characterization of the main effects, epistatic effects and their environmental interactions of QTLs on the genetic basis of yield traits in rice. Theor. Appl. Genet. 105, 248–257 (2002).

    Article  CAS  Google Scholar 

  24. Hua, J.P. et al. Genetic dissection of an elite rice hybrid revealed that heterozygotes are not always advantageous for performance. Genetics 162, 1885–1895 (2002).

    CAS  PubMed  PubMed Central  Google Scholar 

  25. International Rice Genome Sequencing Project. The map-based sequence of the rice genome. Nature 436, 793–800 (2005).

    Article  Google Scholar 

  26. Putterill, J., Robson, F., Lee, K., Simon, R. & Coupland, G. The CONSTANS gene of Arabidopsis promotes flowering and encodes a protein showing similarities to zinc finger transcription factors. Cell 80, 847–857 (1995).

    Article  CAS  Google Scholar 

  27. Strayer, C. et al. Cloning of the Arabidopsis clock gene TOC1, an autoregulatory response regulator homolog. Science 289, 768–771 (2000).

    Article  CAS  Google Scholar 

  28. Robson, F. et al. Functional importance of conserved domains in the flowering-time gene CONSTANS demonstrated by analysis of mutant alleles and transgenic plants. Plant J. 28, 619–631 (2001).

    Article  CAS  Google Scholar 

  29. Peng, K.M., Zhang, H.B. & Zhang, Q.A. BAC library constructed to the rice cultivar “Minghui 63” for cloning gene of agronomic importance. Acta Bot. Sin. 40, 1108–1114 (1998).

    CAS  Google Scholar 

  30. Turner, A., Beales, J., Faure, S., Dunford, R.P. & Laurie, D.A. The pseudo-response regulator Ppd-H1 provides adaptation to photoperiod in barley. Science 310, 1031–1034 (2005).

    Article  CAS  Google Scholar 

  31. Yan, L. et al. The wheat VRN2 gene is a flowering repressor down-regulated by vernalization. Science 303, 1640–1644 (2004).

    Article  CAS  Google Scholar 

  32. Salome, P.A., To, J.P., Kieber, J.J. & McClung, C.R. Arabidopsis response regulators ARR3 and ARR4 play cytokinin-independent roles in the control of circadian period. Plant Cell 18, 55–69 (2006).

    Article  CAS  Google Scholar 

  33. Kaczorowski, K.A. & Quail, P.H. Arabidopsis PSEUDO-RESPONSE REGULATOR7 is a signalling intermediate in phytochrome-regulated seedling deetiolation and phasing of the circadian clock. Plant Cell 15, 2654–2665 (2003).

    Article  CAS  Google Scholar 

  34. Griffiths, S., Dunford, R.P., Coupland, G. & Laurie, D.A. The evolution of CONSTANS-like gene families in barley, rice, and Arabidopsis. Plant Physiol. 131, 1855–1867 (2003).

    Article  CAS  Google Scholar 

  35. Wenkel, S. et al. CONSTANS and the CCAAT box binding complex share a functionally important domain and interact to regulate flowering of Arabidopsis. Plant Cell 18, 2971–2984 (2006).

    Article  CAS  Google Scholar 

  36. Murakami, M., Tago, Y., Yamashino, T. & Mizuno, T. Comparative overviews of clock-associated genes of Arabidopsis thaliana and Oryza sativa. Plant Cell Physiol. 48, 110–121 (2007).

    Article  CAS  Google Scholar 

  37. Dubcovsky, J. et al. Effect of photoperiod on the regulation of wheat vernalization genes VRN1 and VRN2. Plant Mol. Biol. 60, 469–480 (2006).

    Article  CAS  Google Scholar 

  38. Trevaskis, B., Hemming, M.N., Peacock, W.J. & Dennis, E.S. HvVRN2 responds to daylength, whereas HvVRN1 is regulated by vernalization and developmental status. Plant Physiol. 140, 1397–1405 (2006).

    Article  CAS  Google Scholar 

  39. Oka, H.I. Origin of Cultivated Rice (Japan Scientific Soc. Press, Tokyo, 1988).

    Google Scholar 

  40. Hua, J. et al. Single-locus heterotic effects and dominance by dominance interactions can adequately explain the genetic basis of heterosis in an elite rice hybrid. Proc. Natl. Acad. Sci. USA 100, 2574–2579 (2003).

    Article  CAS  Google Scholar 

  41. Hajdukiewicz, P., Svab, Z. & Maliga, P. The small, versatile pPZP family of Agrobacterium binary vectors for plant transformation. Plant Mol. Biol. 25, 989–994 (1994).

    Article  CAS  Google Scholar 

  42. Hiei, Y., Ohta, S., Komari, T. & Kumashiro, T. Efficient transformation of rice (Oryza sativa L.) mediated by Agrobacterium and sequence analysis of the boundaries of the T-DNA. Plant J. 6, 271–282 (1994).

    Article  CAS  Google Scholar 

  43. De Block, M. & Debrouwer, D. RNA-RNA in situ hybridization using digoxigenin-labelled probes: the use of high-molecular-weight polyvinyl alcohol in the alkaline phosphatase indoxyl-nitroblue tetrazolium reaction. Anal. Biochem. 215, 86–89 (1993).

    Article  CAS  Google Scholar 

  44. Livak, K.J. & Schmittgen, T.D. Analysis of relative gene expression data using real-time quantitative PCR and the 2-ΔΔCT method. Methods 25, 402–408 (2001).

    Article  CAS  Google Scholar 

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Acknowledgements

We thank N. Chua and M. Matsuoka (Nagoya University) for helpful comments on a previous version of the manuscript, and J.B. Wang for field management. This work was supported by the Ministry of Science and Technology and the National Natural Science Foundation of China.

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Contributions

W.X., Y.X., W.T., C.X. and X.L. conducted genetic mapping, gene cloning and data collection; X.W. and L.W. conducted expression analysis; Y.Z. conducted the in situ hybridization; H.Z. and S.Y. conducted NIL development; Y.X. and Q.Z. designed and supervised the study; and Q.Z. analyzed the data and wrote the paper. All the authors discussed the results and commented on the manuscript.

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Correspondence to Qifa Zhang.

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Xue, W., Xing, Y., Weng, X. et al. Natural variation in Ghd7 is an important regulator of heading date and yield potential in rice. Nat Genet 40, 761–767 (2008). https://doi.org/10.1038/ng.143

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