Simultaneous changes in seed size, oil content and protein content driven by selection of <i>SWEET</i> homologues during soybean domestication

Abstract

Soybean accounts for more than half of the global production of oilseed and more than a quarter of the protein used globally for human food and animal feed. Soybean domestication involved parallel increases in seed size and oil content, and a concomitant decrease in protein content. However, science has not yet discovered whether these effects were due to selective pressure on a single gene or multiple genes. Here, re-sequencing data from >800 genotypes revealed a strong selection during soybean domestication on <i>GmSWEET10a</i>. The selection of <i>GmSWEET10a</i> conferred simultaneous increases in soybean-seed size and oil content as well as a reduction in the protein content. The result was validated using both near-isogenic lines carrying substitution of haplotype chromosomal segments and transgenic soybeans. Moreover, <i>GmSWEET10b</i> was found to be functionally redundant with its homologue <i>GmSWEET10a</i> and to be undergoing selection in current breeding, leading the the elite allele <i>GmSWEET10b</i>, a potential target for present-day soybean breeding. Both GmSWEET10a and GmSWEET10b were shown to transport sucrose and hexose, contributing to sugar allocation from seed coat to embryo, which consequently determines oil and protein contents and seed size in soybean. We conclude that past selection of optimal <i>GmSWEET10a</i> alleles drove the initial domestication of multiple soybean-seed traits and that targeted selection of the elite allele <i>GmSWEET10b</i> may further improve the yield and seed quality of modern soybean cultivars.