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Differential selection of yield and quality traits has shaped genomic signatures of cowpea domestication and improvement

Nature Genetics (2024)Cite this article

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Abstract

Cowpeas (tropical legumes) are important in ensuring food and nutritional security in developing countries, especially in sub-Saharan Africa. Herein, we report two high-quality genome assemblies of grain and vegetable cowpeas and we re-sequenced 344 accessions to characterize the genomic variations landscape. We identified 39 loci for ten important agronomic traits and more than 541 potential loci that underwent selection during cowpea domestication and improvement. In particular, the synchronous selections of the pod-shattering loci and their neighboring stress-relevant loci probably led to the enhancement of pod-shattering resistance and the compromise of stress resistance during the domestication from grain to vegetable cowpeas. Moreover, differential selections on multiple loci associated with pod length, grain number per pod, seed weight, pod and seed soluble sugars, and seed crude proteins shaped the yield and quality diversity in cowpeas. Our findings provide genomic insights into cowpea domestication and improvement footprints, enabling further genome-informed cultivar improvement of cowpeas.

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Fig. 1: High-quality genome assembly of vegetable cowpea G98 and grain cowpea G323.
Fig. 2: Phylogenetic analysis and genome structure variations of cowpeas.
Fig. 3: Population structure and genomic diversity of 344 cowpea accessions.
Fig. 4: Genome-wide distribution of selective sweeps in cowpea and GWAS for four different traits.
Fig. 5: Identification of PS-related genes in cowpeas.
Fig. 6: Yield traits-related gene mining in cowpea.
Fig. 7: Quality traits-related gene mining in cowpea.
Fig. 8: Proposed model of cowpea domestication and improvement.

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Data availability

The genome assemblies of G98 (accession number JBALLC000000000) and G323 (accession number JAZDUG000000000) and the re-sequencing data of 344 accessions have been deposited in the NCBI Sequence Read Archive under the BioProject accession number PRJNA889224; the RNA-seq data for gene annotation have been deposited in the NCBI Sequence Read Archive under BioProject accession number PRJNA954189; the transcriptome data of three cowpea accessions have been deposited in the NCBI Sequence Read Archive under BioProject accession number PRJNA970477. The genotype and phenotype data can be accessed in figshare (https://doi.org/10.6084/m9.figshare.21646556)141.

Code availability

All codes and tools used in this study are described in Methods and Reporting Summary.

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Acknowledgements

We thank J. Yang from Zhejiang University for valuable comments on the paper. This work was supported by the Key R&D Program of Zhejiang Province (2022C02016 to Xinyi Wu), the Major Science and Technology Project of Plant Breeding in Zhejiang Province (2021C02065 to B.W.), Key R&D Program of Guangdong Province (2020B020220002 to Xinyi Wu), the Crop Germplasm Identification Project of General Seed Management Station of Agriculture and Rural Affairs Department in Zhejiang Province (2022R23T60D01 to Xinyi Wu), the Fundamental Research Funds for the Central Universities (+226-2022-00100 to M.Z.) and Biological Breeding Project of ZAAS Program for Transdisciplinary Research (to Xinyi Wu).

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  1. These authors contributed equally: Xinyi Wu, Zhongyuan Hu.

Authors and Affiliations

  1. State Key Laboratory for Managing Biotic and Chemical Threats to the Quality and Safety of Agro-products, Institute of Vegetables, Zhejiang Academy of Agricultural Sciences, Hangzhou, P. R. China

    Xinyi Wu, Mao Li, Junyang Dong, Baogen Wang, Jian Wu, Xiaohua Wu, Ying Wang, Jian Wang, Zhongfu Lu, Yuyan Sun, Wenqi Dong & Guojing Li

  2. Laboratory of Vegetable Germplasm Innovation and Molecular Breeding, College of Agriculture and Biotechnology, Zhejiang University, Hangzhou, P. R. China

    Zhongyuan Hu, Nanqiao Liao & Mingfang Zhang

  3. Guangdong Key Laboratory for New Technology Research of Vegetables, Vegetable Research Institute, Guangdong Academy of Agricultural Sciences, Guangzhou, P. R. China

    Yan Zhang & Yi Yang

  4. Key Laboratory of Vegetable Legumes Germplasm Enhancement and Molecular Breeding in Southern China (Co-construction by Ministry and Province), Ministry of Agriculture and Rural Affairs, Zhejiang Academy of Agricultural Sciences, Hangzhou, P. R. China

    Mao Li, Junyang Dong, Baogen Wang, Jian Wu, Xiaohua Wu, Ying Wang, Jian Wang, Zhongfu Lu, Yuyan Sun, Wenqi Dong & Guojing Li

  5. Hainan Institute of Zhejiang University, Yazhou Bay Science and Technology City, Sanya, P. R. China

    Mingfang Zhang

  6. Key Laboratory of Horticultural Plant Growth and Development, Ministry of Agriculture and Rural Affairs, Hangzhou, P. R. China

    Mingfang Zhang

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Contributions

Xinyi Wu, M.Z. and G.L. conceived and designed the project. Xinyi Wu, Z.H. and N.L. performed genome assembly and assessment, comparative genome analysis and other bioinformatic analyses. Xinyi Wu, B.W., Xiaohua Wu, Y.W., J.W., Z.L., Y.S. and W.D. performed field cultivation and phenotype investigation in Hangzhou, and Y.Z. and Y.Y. performed field cultivation and phenotype investigation in Guangzhou. M.L., J.D. and J.W. worked on quality testing and GWAS data analysis. J.D. performed gene expression analysis and gene function validation on the bi-parental population. Xinyi Wu and Z.H. wrote the paper, M.Z. revised the paper and all authors read and approved the paper.

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Correspondence to Mingfang Zhang or Guojing Li.

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Wu, X., Hu, Z., Zhang, Y. et al. Differential selection of yield and quality traits has shaped genomic signatures of cowpea domestication and improvement. Nat Genet (2024). https://doi.org/10.1038/s41588-024-01722-w

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