Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Letter
  • Published:

Genetic control of seed shattering during African rice domestication

Abstract

Domestication represents a unique opportunity to study the evolutionary process. The elimination of seed dispersal traits was a key step in the evolution of cereal crops under domestication. Here, we show that ObSH3, a YABBY transcription factor, is required for the development of the seed abscission layer. Moreover, selecting a genomic segment deletion containing SH3 resulted in the loss of seed dispersal in populations of African cultivated rice (Oryza glaberrima Steud.). Functional characterization of SH3 and SH4 (another gene controlling seed shattering on chromosome 4) revealed that multiple genes can lead to a spectrum of non-shattering phenotypes, affecting other traits such as ease of threshing that may be important to tune across different agroecologies and postharvest practices. The molecular evolution analyses of SH3 and SH4 in a panel of 93 landraces provided unprecedented geographical detail of the domestication history of African rice, tracing multiple dispersals from a core heartland and introgression from local wild rice. The cloning of ObSH3 not only provides new insights into a critical crop domestication process but also adds to the body of knowledge on the molecular mechanism of seed dispersal.

This is a preview of subscription content, access via your institution

Access options

Rent or buy this article

Prices vary by article type

from$1.95

to$39.95

Prices may be subject to local taxes which are calculated during checkout

Fig. 1: Comparison of seed shattering and floral abscission zone morphologies between W1411 (O. barthii) and IRGC104165 (O. glaberrima).
Fig. 2: Map-based clone of ObSH3.
Fig. 3: Expression and subcellular localization of ObSH3.
Fig. 4: Additive effect of SH3 and SH4.
Fig. 5: Evolution of the non-shattering trait in African rice.

Similar content being viewed by others

References

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

    Article  PubMed  CAS  Google Scholar 

  2. Meyer, R. S. & Purugganan, M. D. Evolution of crop species: genetics of domestication and diversification. Nat. Rev. Genet. 14, 840–852 (2013).

    Article  PubMed  CAS  Google Scholar 

  3. Tan, L. et al. Control of a key transition from prostrate to erect growth in rice domestication. Nat. Genet. 40, 1360–1364 (2008).

    Article  PubMed  CAS  Google Scholar 

  4. Jin, J. et al. Genetic control of rice plant architecture under domestication. Nat. Genet. 40, 1365–1369 (2008).

    Article  PubMed  CAS  Google Scholar 

  5. Mao, H. et al. Linking differential domain functions of the GS3 protein to natural variation of grain size in rice. Proc. Natl Acad. Sci. USA 107, 19579–19584 (2010).

    Article  PubMed  PubMed Central  Google Scholar 

  6. Li, Y. et al. Natural variation in GS5 plays an important role in regulating grain size and yield in rice. Nat. Genet. 43, 1266–1269 (2011).

    Article  PubMed  CAS  Google Scholar 

  7. Che, R. et al. Control of grain size and rice yield by GL2-mediated brassinosteroid responses. Nat. Plants 2, 15195 (2015).

    Article  PubMed  CAS  Google Scholar 

  8. Duan, P. et al. Regulation of OsGRF4 by OsmiR396 controls grain size and yield in rice. Nat. Plants 2, 15203 (2015).

    Article  PubMed  CAS  Google Scholar 

  9. Wang, Y. et al. Copy number variation at the GL7 locus contributes to grain size diversity in rice. Nat. Genet. 47, 944–948 (2015).

    Article  PubMed  CAS  Google Scholar 

  10. Si, L. et al. OsSPL13 controls grain size in cultivated rice. Nat. Genet. 48, 447–456 (2016).

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  PubMed Central  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  14. Lin, Z. et al. Parallel domestication of the Shattering1 genes in cereals. Nat. Genet. 44, 720–724 (2012).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  15. Pourkheirandish, M. et al. Evolution of the grain dispersal system in barley. Cell 162, 527–539 (2015).

    Article  PubMed  CAS  Google Scholar 

  16. Meyer, R. S. et al. Domestication history and geographical adaptation inferred from a SNP map of African rice. Nat. Genet. 48, 1083–1088 (2016).

    Article  PubMed  CAS  Google Scholar 

  17. Agnoun, Y. et al. The African rice Oryza glaberrima Steud: knowledge distribution and prospects. Int. J. Biol. 4, 158–180 (2012).

    Google Scholar 

  18. Linares, O. F. African rice (Oryza glaberrima): history and future potential. Proc. Natl Acad. Sci. USA 99, 16360–16365 (2002).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  19. Rhodes, E. R., Jalloh, A. & Diouf, A. Review of Research and Policy for Climate Change Adaptation in the Agriculture Sector of West Africa (AfricaInteract, 2014).

  20. Jones, M. P., Dingkuhn, M., Aluko, G. K. & Semon, M. Interspecific Oryza sativa L. X O. glaberrima Steud. progenies in upland rice improvement. Euphytica 94, 237–246 (1997).

    Article  Google Scholar 

  21. Li, X. M. et al. Natural alleles of a proteasome alpha2 subunit gene contribute to thermotolerance and adaptation of African rice. Nat. Genet. 47, 827–833 (2015).

    Article  PubMed  CAS  Google Scholar 

  22. Wang, M. et al. The genome sequence of African rice (Oryza glaberrima) and evidence for independent domestication. Nat. Genet. 46, 982–988 (2014).

    Article  PubMed  CAS  Google Scholar 

  23. Carney, J. A. Black Rice: the African Origins of Rice Cultivation in the Americas (Harvard Univ. Press, Cambridge, MA, 2001).

  24. Vydrin, V. On the problem of the Proto-Mande homeland. J. Lang. Relat. 1, 107–142 (2009).

    Google Scholar 

  25. Wu, W. et al. A single-nucleotide polymorphism causes smaller grain size and loss of seed shattering during African rice domestication. Nat. Plants 3, 17064 (2017).

    Article  PubMed  CAS  Google Scholar 

  26. Cong, B., Barrero, L. S. & Tanksley, S. D. Regulatory change in YABBY-like transcription factor led to evolution of extreme fruit size during tomato domestication. Nat. Genet. 40, 800–804 (2008).

    Article  PubMed  CAS  Google Scholar 

  27. Siegfried, K. R. et al. Members of the YABBY gene family specify abaxial cell fate in Arabidopsis. Development 126, 4117–4128 (1999).

    PubMed  CAS  Google Scholar 

  28. Yamaguchi, T. et al. The YABBY gene DROOPING LEAF regulates carpel specification and midrib development in Oryza sativa. Plant Cell 16, 500–509 (2004).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  29. Portères, R. in Papers in African Prehistory (eds Fage, J. D. & Oliver, R. A.) 43–58 (Cambridge Univ. Press, Cambridge, 1970).

  30. Portères, R. in Origins of African Plant Domestication (eds Harlan, J. R., De Wet, J. M. & Stemler, A. B.) 409–452 (De Gruyter Mouton, Berlin, 1976).

  31. Barrett, R. D. & Schluter, D. Adaptation from standing genetic variation. Trends Ecol. Evol. 23, 38–44 (2008).

    Article  PubMed  Google Scholar 

  32. Stetter, M. G., Gates, D. J., Mei, W. B. & Ross-Ibarra, J. How to make a domesticate. Curr. Biol. 27, R896–R900 (2017).

    Article  PubMed  CAS  Google Scholar 

  33. Studer, A., Zhao, Q., Ross-Ibarra, J. & Doebley, J. Identification of a functional transposon insertion in the maize domestication gene tb1. Nat. Genet. 43, 1160–1163 (2011).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  34. Hammer, K. Das Domestikationssyndrom. Kulturpflanze 32, 11–34 (1984).

    Article  Google Scholar 

  35. Mercuri, A. M., Fornaciari, R., Gallinaro, M., Vanin, S. & di Lernia, S. Plant behaviour from human imprints and the cultivation of wild cereals in Holocene Sahara. Nat. Plants 4, 71–81 (2018).

    Article  PubMed  Google Scholar 

  36. Stein, J. C. et al. Genomes of 13 domesticated and wild rice relatives highlight genetic conservation, turnover and innovation across the genus Oryza. Nat. Genet. 50, 285–296 (2018).

    Article  PubMed  CAS  Google Scholar 

  37. Avni, R. et al. Wild emmer genome architecture and diversity elucidate wheat evolution and domestication. Science 357, 93–97 (2017).

    Article  PubMed  CAS  Google Scholar 

  38. Murray, M. G. & Thompson, W. F. Rapid isolation of high molecular weight plant DNA. Nucleic Acids Res. 8, 4321–4325 (1980).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  39. Ma, X. et al. A robust CRISPR/Cas9 system for convenient, high-efficiency multiplex genome editing in monocot and dicot plants. Mol. Plant 8, 1274–1284 (2015).

    Article  PubMed  CAS  Google Scholar 

  40. Li, H. & Durbin, R. Fast and accurate long-read alignment with Burrows–Wheeler transform. Bioinformatics 26, 589–595 (2010).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  41. Hu, Z. et al. EUPAN enables pan-genome studies of a large number of eukaryotic genomes. Bioinformatics 33, 2408–2409 (2017).

    Article  PubMed  Google Scholar 

  42. Thorvaldsdottir, H., Robinson, J. T. & Mesirov, J. P. Integrative Genomics Viewer (IGV): high-performance genomics data visualization and exploration. Brief. Bioinform. 14, 178–192 (2013).

    Article  PubMed  CAS  Google Scholar 

  43. DePristo, M. A. et al. A framework for variation discovery and genotyping using next-generation DNA sequencing data. Nat. Genet. 43, 491–498 (2011).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  44. Price, M. N., Dehal, P. S. & Arkin, A. P.FastTree 2 — approximately maximum-likelihood trees for large alignments. PLoS ONE 5, e9490 (2010).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  45. Letunic, I. & Bork, P. Interactive tree of life (iTOL)v3: an online tool for the display and annotation of phylogenetic and other trees. Nucleic Acids Res. 44, W242–W245 (2016).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  46. Alexander, D. H., Novembre, J. & Lange, K. Fast model-based estimation of ancestry in unrelated individuals. Genome Res. 19, 1655–1664 (2009).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  47. Purcell, S. et al. PLINK: a tool set for whole-genome association and population-based linkage analyses. Am. J. Hum. Genet. 81, 559–575 (2007).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  48. Patterson, N., Price, A. L. & Reich, D. Population structure and eigenanalysis. PLoS Genet. 2, e190 (2006).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

Download references

Acknowledgements

We thank the International Rice Research Institute for providing the wild rice and cultivated rice samples. This research was supported by the Ministry of Agriculture of China (2016ZX08009-003) and the National Key R&D Program for Crop Breeding (2016YFD0100901). The funders had no role in the study design, data collection and analyses, decision to publish, or preparation of the manuscript.

Author information

Authors and Affiliations

Authors

Contributions

Z.Z. designed and supervised this study. S.L. conducted the map-based cloning, genetic transformation and gene expression analyses. S.L., W.W. and H.Z. conducted the histological analyses of the seed abscission layers. M.W. performed the evolutionary analysis and R.S.M assisted in analysing the results. M.-N.N., L.T., H.C., Y.F., J.Z. and C.S. conducted the collection of rice germplasm and phenotypic data. Z.Z., R.S.M. M.W. and R.A.W. wrote the manuscript.

Corresponding author

Correspondence to Zuofeng Zhu.

Ethics declarations

Competing interests

The authors declare no competing interests.

Additional information

Publisher’s note: Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary information

Supplementary Information

Supplementary Figures 1–12

Reporting Summary

Supplementary Table 1

Geographical distribution of position in O. glaberrima and O. barthii

Supplementary Table 2

Primers used in this study

Supplementary Table 3

The ancestry of each population

Supplementary Table 4

PCA analysis of O. glaberrima and O. barthii individuals

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Lv, S., Wu, W., Wang, M. et al. Genetic control of seed shattering during African rice domestication. Nature Plants 4, 331–337 (2018). https://doi.org/10.1038/s41477-018-0164-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/s41477-018-0164-3

This article is cited by

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