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.

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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

Author notes

    • Muhua Wang

    Present address: Friedrich Miescher Laboratory of the Max Planck Society, Tübingen, Germany

  1. These authors contributed equally: Shuwei Lv, Wenguang Wu, Muhua Wang and Rachel S. Meyer.

Affiliations

  1. MOE Key Laboratory of Crop Heterosis and Utilization, National Center for Evaluation of Agricultural Wild Plants (Rice), Department of Plant Genetics and Breeding, China Agricultural University, Beijing, China

    • Shuwei Lv
    • , Wenguang Wu
    • , Lubin Tan
    • , Haiying Zhou
    • , Yongcai Fu
    • , Hongwei Cai
    •  & Zuofeng Zhu
  2. Arizona Genomics Institute, School of Plant Sciences, University of Arizona, Tucson, AZ, USA

    • Muhua Wang
    • , Jianwei Zhang
    •  & Rod A. Wing
  3. Department of Ecology and Evolutionary Biology, University of California Los Angeles, Los Angeles, CA, USA

    • Rachel S. Meyer
  4. Africa Rice Center, Cotonou, Benin

    • Marie-Noelle Ndjiondjop
  5. State Key Laboratory of Plant Physiology and Biochemistry, China Agricultural University, Beijing, China

    • Chuanqing Sun

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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.

Competing interests

The authors declare no competing interests.

Corresponding author

Correspondence to Zuofeng Zhu.

Supplementary information

  1. Supplementary Information

    Supplementary Figures 1–12

  2. Reporting Summary

  3. Supplementary Table 1

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

  4. Supplementary Table 2

    Primers used in this study

  5. Supplementary Table 3

    The ancestry of each population

  6. Supplementary Table 4

    PCA analysis of O. glaberrima and O. barthii individuals

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DOI

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