J Integr Plant Biol. ›› 2023, Vol. 65 ›› Issue (11): 2469-2489.DOI: 10.1111/jipb.13559

• Functional Omics and Systems Biology • Previous Articles     Next Articles

A loss-of-function mutant allele of a glycosyl hydrolase gene has been co-opted for seed weight control during soybean domestication

Siming Wei1,2,3, Bin Yong1,2,3, Hongwei Jiang4,5, Zhenghong An1,2,3, Yan Wang1,2, Bingbing Li1,2,3, Ce Yang1,2,3, Weiwei Zhu1,2,3, Qingshan Chen4* and Chaoying He1,2,3,6*   

  1. 1. State Key Laboratory of Plant Diversity and Specialty Crops/State Key Laboratory of Systematic and Evolutionary Botany, Institute of Botany, the Chinese Academy of Sciences, Beijing 100093, China;
    2. China National Botanical Garden, Beijing 100093, China;
    3. College of Life Sciences, University of Chinese Academy of Sciences, Beijing 100049, China;
    4. College of Agriculture, Northeast Agricultural University, Harbin 150030, China;
    5. Jilin Academy of Agricultural Sciences, Changchun 130022, China;
    6. The Innovative Academy of Seed Design, the Chinese Academy of Sciences, Beijing 100101, China
    *Correspondences:Qingshan Chen(qshchen@126.com);Chaoying He(chaoying@ibcas.ac.cn, Dr. He is fully responsible for the distributions of all materials associated with this article)
  • Received:2023-08-15 Accepted:2023-08-28 Online:2023-08-28 Published:2023-11-01

Abstract: The resultant DNA from loss-of-function mutation can be recruited in biological evolution and development. Here, we present such a rare and potential case of “to gain by loss” as a neomorphic mutation during soybean domestication for increasing seed weight. Using a population derived from a chromosome segment substitution line of Glycine max (SN14) and Glycine soja (ZYD06), a quantitative trait locus (QTL) of 100-seed weight (qHSW) was mapped on chromosome 11, corresponding to a truncated β-1, 3-glucosidase (βGlu) gene. The novel gene hsw results from a 14-bp deletion, causing a frameshift mutation and a premature stop codon in the βGlu. In contrast to HSW, the hsw completely lost βGlu activity and function but acquired a novel function to promote cell expansion, thus increasing seed weight. Overexpressing hsw instead of HSW produced large soybean seeds, and surprisingly, truncating hsw via gene editing further increased the seed size. We further found that the core 21-aa peptide of hsw and its variants acted as a promoter of seed size. Transcriptomic variation in these transgenic soybean lines substantiated the integration hsw into cell and seed size control. Moreover, the hsw allele underwent selection and expansion during soybean domestication and improvement. Our work cloned a likely domesticated QTL controlling soybean seed weight, revealed a novel genetic variation and mechanism in soybean domestication, and provided new insight into crop domestication and breeding, and plant evolution.

Key words: domestication, frameshift mutation, QTL, seed weight, soybean, to gain by loss

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