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Genomic variation in weedy and cultivated broomcorn millet accessions uncovers the genetic architecture of agronomic traits

Nature Genetics (2024)Cite this article

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Abstract

Large-scale genomic variations are fundamental resources for crop genetics and breeding. Here we sequenced 1,904 genomes of broomcorn millet to an average of 40× sequencing depth and constructed a comprehensive variation map of weedy and cultivated accessions. Being one of the oldest cultivated crops, broomcorn millet has extremely low nucleotide diversity and remarkably rapid decay of linkage disequilibrium. Genome-wide association studies identified 186 loci for 12 agronomic traits. Many causative candidate genes, such as PmGW8 for grain size and PmLG1 for panicle shape, showed strong selection signatures during domestication. Weedy accessions contained many beneficial variations for the grain traits that are largely lost in cultivated accessions. Weedy and cultivated broomcorn millet have adopted different loci controlling flowering time for regional adaptation in parallel. Our study uncovers the unique population genomic features of broomcorn millet and provides an agronomically important resource for cereal crops.

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Fig. 1: Geographical distribution and phylogeny of 1,904 broomcorn millet accessions.
Fig. 2: Evolution and divergence of weedy and cultivated broomcorn millet.
Fig. 3: SVs in weedy and cultivated broomcorn millet.
Fig. 4: Genome-wide analysis of selected sweeps.
Fig. 5: GWAS for GS and HD, and identification of candidate genes.
Fig. 6: GWAS for PH and functional validation of candidate causal gene.
Fig. 7: GWAS of weedy and cultivated populations.
Fig. 8: Distribution of qHD2 and qHD5 haplotypes in weedy and cultivated broomcorn millet.

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Data availability

The raw sequencing data of 1,904 diversity accessions was deposited with the NCBI genome database under project no. PRJNA917713 (SRR23330656–SRR23330837, SRR23330861–SRR23331110, SRR23331663–SRR23332055, SRR23332224–SRR23332338, SRR23332341–SRR23332395, SRR23338406–SRR23338647, SRR23344772–SRR23345046, SRR23366736–SRR23366900, SRR23378377–SRR23378603). The Longmi4 reference genome sequences were obtained from the NCBI GenBank assembly (www.ncbi.nlm.nih.gov/datasets/genome; GCA_002895445.2). The SNPs, indels and SVs, and the details of each phenotypic information, are available at Zenodo88 (https://doi.org/10.5281/zenodo.10783997). Data availability has no restrictions. Source data are provided with this paper.

Code availability

The custom code used in this study is available at Zenodo88 (https://doi.org/10.5281/zenodo.10783997). The code can be freely used and redistributed without any restrictions.

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Acknowledgements

We thank C. J. Yang (Scotland’s Rural College) and W. Xue (Agronomy College of Shenyang Agricultural University) for their valuable suggestions and comments. We thank the Tongzhou Yujiawu International Seed Industry Park and the Yujiawu Professor Workstation for providing the space that facilitated collaboration. We thank the High-performance Computing (HPC) Platform of China Agricultural University for its support of large-scale computation. We thank Beijing PARATERA Tech (https://paratera.com/) for providing the HPC resources that have contributed to the research results reported in this study. This work was supported by the National Key R&D Program of China (no. 2021YFD1200700 to W.S.), the National Natural Science Foundation of China (no. 32271541 to W.S., no. 32272143 to H.M.Z. and no. 62031003 to B.X.), the Science and Technology Innovation (STI) 2030 (no. 2022ZD04020 to H.M.Z.), a key project of maize germplasm improvement (no. 2022010202 to W. S. and no. B21HJ0509 to J.L.), the Chinese Universities Scientific Fund (no. 2023TC019 to H.N.Z.) and the STI 2030-Major Projects (no. 2023ZD04074 to H.N.Z.).

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Author notes

  1. These authors contributed equally: Qiong Lu, Hainan Zhao, Zhengquan Zhang, Yuhe Bai, Haiming Zhao, Guoqing Liu.

Authors and Affiliations

  1. State Key Laboratory of Maize Bio-breeding, National Maize Improvement Center, China Agricultural University, Beijing, People’s Republic of China

    Qiong Lu, Hainan Zhao, Zhengquan Zhang, Yuhe Bai, Haiming Zhao, Yunxiao Zheng, Haiyue Zhao, Huihui Gong, Lingwei Chen, Xizhen Deng, Xiangde Hong, Tianxiang Liu, Baichuan Li, Yan Bai, Beibei Xin, Jian Chen, Lizhu E., Jinsheng Lai & Weibin Song

  2. Frontiers Science Center for Molecular Design Breeding (Ministry of Education), China Agricultural University, Beijing, People’s Republic of China

    Hainan Zhao, Jinsheng Lai & Weibin Song

  3. Institute of Millet Crops, Hebei Academy of Agriculture and Forestry Sciences, Shijiazhuang, People’s Republic of China

    Guoqing Liu & Haiquan Li

  4. Institute of Crop Sciences, Chinese Academy of Agricultural Sciences, Beijing, People’s Republic of China

    Minxuan Liu & Ping Lu

  5. Tongliao Agricultural and Animal Husbandry Research Institute, Tongliao, People’s Republic of China

    Feng Wen

  6. Center for Agricultural Genetic Resources Research, Shanxi Agricultural University, Taiyuan, People’s Republic of China

    Lun Wang

  7. Institute of Crop Resources Research, Heilongjiang Academy of Agricultural Sciences, Harbin, People’s Republic of China

    Zhijiang Li

  8. High Latitude Crops Institute, Shanxi Agricultural University, Datong, People’s Republic of China

    Hai Li

  9. National Agricultural Technology Extension & Service Center, Beijing, People’s Republic of China

    Like Zhang, Wenhui Ma, Chunqing Liu & Yan Bai

  10. Center for Crop Functional Genomics and Molecular Breeding, China Agricultural University, Beijing, People’s Republic of China

    Jinsheng Lai & Weibin Song

  11. Sanya Institute of China Agricultural University, Sanya, People’s Republic of China

    Jinsheng Lai & Weibin Song

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  1. Qiong Lu
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  2. Hainan Zhao
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W.S. and J.L. conceived the research. Q.L., Y.Z., H.G., X.D., L.C., Y.H.B., B.L. and X.H. conducted the experiments. Q.L. and T.L. extracted the DNA. Q.L., H.N.Z. and Z.Z. performed the data analyses. G.L., H.Q.L., P.L., M.L., F.W., L.W., Z.L. and H.L. provided the cultivated broomcorn millet accessions. W.S. and H.Y.Z. collected the weedy broomcorn millet. L.Z., W.M., C.L., Y.B., B.X., J.C., H.M.Z. and L.E. contributed to the discussion. H.N.Z., Q.L., Z.Z., H.M.Z. and W.S. wrote the paper. B.X. and J.C. revised the paper.

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Correspondence to Weibin Song.

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Nature Genetics thanks Aureliano Bombarely and the other anonymous reviewer(s) for their contribution to the peer review of this work. Peer reviewer reports are available.

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Lu, Q., Zhao, H., Zhang, Z. et al. Genomic variation in weedy and cultivated broomcorn millet accessions uncovers the genetic architecture of agronomic traits. Nat Genet (2024). https://doi.org/10.1038/s41588-024-01718-6

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