Population genomic analysis reveals domestication of cultivated rye from weedy rye

• Published in: Molecular plant 2022-03, Vol.15 (3), p.552-561
• Main Authors: Sun, Yanqing, Shen, Enhui, Hu, Yiyu, Wu, Dongya, Feng, Yu, Lao, Sangting, Dong, Chenfeng, Du, Tianyu, Hua, Wei, Ye, Chu-Yu, Zhu, Jinhuan, Zhu, Qian-Hao, Cai, Daguang, Skuza, Lidia, Qiu, Jie, Fan, Longjiang
• Format: Article
• Language: English
• Subjects: Domestication; Evolution, Molecular; Genetic Variation; Genome, Plant - genetics; introgression; Metagenomics; Plant Breeding; Secale - genetics; Secale cereale; Triticum - genetics; Vavilovian hypothesis; weedy rye
• ISSN: 1674-2052; 1752-9867
• DOI: 10.1016/j.molp.2021.12.015

Rye (Secale cereale) is an important crop with multiple uses and a valuable genetic resource for wheat breeding. However, due to its complex genome and outcrossing nature, the origin of cultivated rye remains elusive. The geneticist N.I. Vavilov proposed that cultivated rye had been domesticated from weedy rye, rather than directly from wild species like other crops. Unraveling the domestication history of rye will extend our understanding of crop evolution and upend our inherent understanding of agricultural weeds. To this end, in this study we generated the 8.5 Tb of whole-genome resequencing data from 116 worldwide accessions of wild, weedy, and cultivated rye, and demonstrated that cultivated rye was domesticated directly from weedy relatives with a similar but enhanced genomic selection by humans. We found that a repertoire of genes that experienced artificial selection is associated with important agronomic traits, including shattering, grain yield, and disease resistance. Furthermore, we identified a composite introgression in cultivated rye from the wild perennial Secale strictum and detected a 2-Mb introgressed fragment containing a candidate ammonium transporter gene with potential effect on the grain yield and plant growth of rye. Taken together, our findings unravel the domestication history of cultivated rye, suggest that interspecific introgression serves as one of the likely causes of obscure species taxonomy of the genus Secale, and provide an important resource for future rye and wheat breeding. This study provides insight into genetic underpinning of the domestication of rye, a secondary domesticate (Vavilovian hypothesis) directly from weedy rye, based on genome resequencing data of 116 Secale accessions. A repertoire of domestication genes and a 2-Mb introgressed fragment from Secale strictum associated with important traits were identified, providing an important resource for future rye and wheat breeding.