Parallel selection of distinct Tof5 alleles drove the adaptation of cultivated and wild soybean to high latitudes

• Published in: Molecular plant 2022-02, Vol.15 (2), p.308-321
• Main Authors: Dong, Lidong, Cheng, Qun, Fang, Chao, Kong, Lingping, Yang, Hui, Hou, Zhihong, Li, Yongli, Nan, Haiyang, Zhang, Yuhang, Chen, Qingshan, Zhang, Chunbao, Kou, Kun, Su, Tong, Wang, Lingshuang, Li, Shichen, Li, Haiyang, Lin, Xiaoya, Tang, Yang, Zhao, Xiaohui, Lu, Sijia, Liu, Baohui, Kong, Fanjiang
• Format: Article
• Language: English
• Subjects: Alleles; ancestry; Arabidopsis thaliana; artificially selection; domestication; flowering time; Flowers - metabolism; Gene Expression Regulation, Plant; genetically modified organisms; Genome-Wide Association Study; genomics; geographical distribution; Glycine max - metabolism; Glycine soja; latitude adaptation; loci; natural selection; Photoperiod; Plant Proteins - metabolism; soybean; soybeans; wild
• ISSN: 1674-2052; 1752-9867
• DOI: 10.1016/j.molp.2021.10.004

Photoperiod responsiveness is a key factor limiting the geographic distribution of cultivated soybean and its wild ancestor. In particular, the genetic basis of the adaptation in wild soybean remains poorly understood. In this study, by combining whole-genome resequencing and genome-wide association studies we identified a novel locus, Time of Flowering 5 (Tof5), which promotes flowering and enhances adaptation to high latitudes in both wild and cultivated soybean. By genomic, genetic and transgenic analyses we showed that Tof5 encodes a homolog of Arabidopsis thaliana FRUITFULL (FUL). Importantly, further analyses suggested that different alleles of Tof5 have undergone parallel selection. The Tof5H1 allele was strongly selected by humans after the early domestication of cultivated soybean, while Tof5H2 allele was naturally selected in wild soybean, and in each case facilitating adaptation to high latitudes. Moreover, we found that the key flowering repressor E1 suppresses the transcription of Tof5 by binding to its promoter. In turn, Tof5 physically associates with the promoters of two important FLOWERING LOCUS T (FT), FT2a and FT5a, to upregulate their transcription and promote flowering under long photoperiods. Collectively, our findings provide insights into how wild soybean adapted to high latitudes through natural selection and indicate that cultivated soybean underwent changes in the same gene but evolved a distinct allele that was artificially selected after domestication. This study reveals that different alleles of Tof5 have undergone parallel selection in wild and cultivated soybean. The transcription of Tof5 is directly regulated by soybean key flowering suppressor E1. In turn, Tof5 protein physically associates with the promoters of FT homologs to enhance their transcription and improve adaptation to high latitudes in both wild and cultivated soybean.