Deletion in a gene associated with grain size increased yields during rice domestication

Nature Genetics volume 40, pages1023–1028(2008)Cite this article

Abstract

The domestication of crops involves a complex process of selection in plant evolution and is associated with changes in the DNA regulating agronomically important traits. Here we report the cloning of a newly identified QTL, qSW5 (QTL for seed width on chromosome 5), involved in the determination of grain width in rice. Through fine mapping, complementation testing and association analysis, we found that a deletion in qSW5 resulted in a significant increase in sink size owing to an increase in cell number in the outer glume of the rice flower; this trait might have been selected by ancient humans to increase yield of rice grains. In addition, we mapped two other defective functional nucleotide polymorphisms of rice domestication-related genes with genome-wide RFLP polymorphisms of various rice landraces. These analyses show that the qSW5 deletion had an important historical role in artificial selection, propagation of cultivation and natural crossings in rice domestication, and shed light on how the rice genome was domesticated.

Rent or Buy article

Get time limited or full article access on ReadCube.

from$8.99

Rent or Buy

All prices are NET prices.

Figure 1: Characterization of qSW5.
Figure 2: Mapping and cloning of qSW5.
Figure 3: Genome dynamics during rice domestication.

References

  1. 1

    Darwin, C. The Variations of Animals and Plants under Domestication (D. Appleton, New York, 1857).

    Google Scholar 

  2. 2

    Wright, S.I. et al. The effects of artificial selection on the maize genome. Science 308, 1310–1314 (2005).

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  3. 3

    Doebley, J.F., Gaut, B.S. & Smith, B.D. The molecular genetics of crop domestication. Cell 127, 1309–1321 (2006).

    CAS  Article  Google Scholar 

  4. 4

    Roos-Ibarra, J., Morell, P.L. & Gaut, B.S. Plant domestication, a unique opportunity to identify the genetic basis of adaptation. Proc. Natl. Acad. Sci. USA 104, 8641–8648 (2007).

    Article  Google Scholar 

  5. 5

    Dubcovsky, J. & Dvorak, J. Genome plasticity: a key factor in the success of polyploidy wheat under domestication. Science 316, 1862–1866 (2007).

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  6. 6

    Sang, T. & Ge, S. The puzzle of rice domestication. J. Integr. Plant Biol. 49, 760–768 (2007).

    CAS  Article  Google Scholar 

  7. 7

    Sweeney, M. & McCouch, S. The complex history of the domestication of rice. Ann. Bot. (Lond.) 100, 951–957 (2007).

    Article  Google Scholar 

  8. 8

    Doebley, J., Stec, A. & Hubbard, L. The evolution of apical dominance in maize. Nature 386, 485–488 (1997).

    CAS  Article  Google Scholar 

  9. 9

    Wang, H. et al. The origin of the naked grains of maize. Nature 436, 714–719 (2005).

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  10. 10

    Simons, K.J. et al. Molecular characterization of the major wheat domestication gene Q. Genetics 172, 547–555 (2006).

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  11. 11

    Komatsuda, T. et al. Six-rowed barley originated from a mutation in a homeodomain-leucine zipper I-class homeobox gene. Proc. Natl. Acad. Sci. USA 104, 1424–1429 (2007).

    CAS  Article  Google Scholar 

  12. 12

    Li, C., Zhou, A. & Sang, T. Rice domestication by reducing shattering. Science 311, 1936–1939 (2006).

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  13. 13

    Konishi, S. et al. An SNP caused loss of seed shattering during rice domestication. Science 312, 1392–1396 (2006).

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  14. 14

    Hong, S.K., Kitano, H., Satoh, H. & Nagato, Y. How is embryo size genetically regulated in rice? Development 122, 2051–2058 (1996).

    CAS  PubMed  Google Scholar 

  15. 15

    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).

    CAS  Article  PubMed  Google Scholar 

  16. 16

    Isshiki, M. et al. Naturally occurring functional allele of the rice waxy locus has a GT to TT mutation at the 5′ splice site of the first intron. Plant J. 15, 133–138 (1998).

    CAS  Article  PubMed  Google Scholar 

  17. 17

    Olesen, K.M. & Purugganan, M.D. Molecular evidence on the origin and evolution of glutinous rice. Genetics 162, 941–950 (2002).

    Google Scholar 

  18. 18

    Olsen, K.M. et al. Selection under domestication: evidence for a sweep in the rice Waxy genomic region. Genetics 173, 975–983 (2006).

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  19. 19

    Kojima, Y., Ebana, K., Fukuoka, S., Nagamine, T. & Kawase, M. Development of an RFLP-based rice diversity research set of germplasm. Breed. Sci. 55, 431–440 (2005).

    CAS  Article  Google Scholar 

  20. 20

    Cheng, C. et al. Polyphyletic origin of cultivated rice: based on the interspersion pattern of SINEs. Mol. Biol. Evol. 20, 67–75 (2003).

    CAS  Article  PubMed  Google Scholar 

  21. 21

    Ma, J. & Bennetzen, J.L. Rapid recent growth and divergence of rice nuclear genomes. Proc. Natl. Acad. Sci. USA 101, 12404–12410 (2004).

    CAS  Article  Google Scholar 

  22. 22

    Vitte, C., Ishii, T., Lamy, F., Brar, D. & Panaud, O. Genomic paleontology provides evidence for two distinct origins of Asian rice (Oryza sativa L.). Mol. Gen. Genet. 272, 504–511 (2004).

    CAS  Article  Google Scholar 

  23. 23

    Ehrenreich, I.M. & Purugganan, M.D. The molecular genetic basis of plant adaptation. Am. J. Bot. 93, 953–962 (2006).

    CAS  Article  PubMed  Google Scholar 

Download references

Acknowledgements

We thank H. Kanamori of Institute of the Society for Techno-Innovation of Agriculture, Forestry and Fisheries and T. Matsumoto of National Institute of Agrobiological Sciences for genomic sequencing of the qSW5 region of Kasalath, Y. Kojima for RFLP data production, and K. Ono for Kasalath transformation. M.Y. was supported by MP1113 (Integrated research project for plant, insect and animal using genome technology) and T.I. has been supported by GD2008 (Integrated research project for plant, insect and animal using genome technology) and QTL5001 (Genomics for Agricultural Innovation) of the Ministry of Agriculture, Forestry and Fisheries of Japan.

Author information

Author notes

  1. Ayahiko Shomura and Takeshi Izawa: These authors contributed equally to this work.

Affiliations

  1. Institute of the Society for Techno-Innovation of Agriculture, Forestry, and Fisheries, 446-1 Ippaizuka, Kamiyokoba, Tsukuba, 305-0854, Ibaraki, Japan

    Ayahiko Shomura

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

    Takeshi Izawa & Saeko Konishi

  3. QTL Genomics Research Center, National Institute of Agrobiological Sciences, 2-1-2 Kannondai, Tsukuba, 305-8602, Ibaraki, Japan

    Kaworu Ebana, Hiromi Kanegae & Masahiro Yano

  4. Toyama Agricultural Research Center, 1124-1, Yoshioka, 939-8153, Toyama, Japan

    Takeshi Ebitani

Authors
  1. Ayahiko Shomura
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Takeshi Izawa
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Kaworu Ebana
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Takeshi Ebitani
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Hiromi Kanegae
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Saeko Konishi
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Masahiro Yano
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

A.S. performed most of the experiments. S.K. helped A.S. with the experiments and carried out qRT-PCR expression analysis. H.K. performed the original QTL analysis with the F2 population. T.E. field-tested NIL(qSW5). K.E. provided genome-wide RFLP data on rice landraces. M.Y. directed the QTL analysis, material production and fine mapping of qSW5. T.I. directed the research, designed the experiments for all the other parts and analyzed the FNPs with genome data, and wrote the manuscript. All authors contributed to improve the manuscript.

Corresponding author

Correspondence to Takeshi Izawa.

Supplementary information

Supplementary Text and Figures

Supplementary Note, Supplementary Figures 1–7, Supplementary Tables 1–3 (PDF 1930 kb)

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Shomura, A., Izawa, T., Ebana, K. et al. Deletion in a gene associated with grain size increased yields during rice domestication. Nat Genet 40, 1023–1028 (2008). https://doi.org/10.1038/ng.169

Download citation

Further reading

Search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing