Simultaneous changes in seed size, oil content and protein content driven by selection of SWEET 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 if these effects were due to selective pressure on a single gene or multiple genes. Here, resequencing data from over 800 genotypes revealed a strong selection during soybean domestication on GmSWEET10a. The selection of GmSWEET10a conferred simultaneous increases in soybean seed size and oil content as well as reduction in protein content. The result was validated using both near-isogenic lines carrying substitution of haplotype chromosomal segments and transgenic soybeans. Moreover, GmSWEET10b was found to be functionally redundant with its homologue GmSWEET10a and to be undergoing selection in current breeding, leading the elite allele GmSWEET10b 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 GmSWEET10a alleles drove the initial domestication of multiple soybean seed traits, and that targeted selection of the elite allele GmSWEET10b may further improve the yield and seed quality of modern soybean cultivars.

Selection of GmSWEET39 for oil and protein improvement in soybean

“…It should also be noted that, at the early maturation stage, GmSWEET39 exhibited decreasing gradients in expression in three connected layers of tissues, from the parenchyma (seed coat) to abaxial epidermis (cotyledon) and to aleurone ( Fig 2J and 2K ), which was coincident with the possible path of sugar flux from maternal seed coat to filial cotyledon [ 13 , 34 ]. Interestingly, we observed that the truncated GmSWEET39 (CC-) had a higher level of oil content, as evidenced by the H1 vs H2 comparison ( Fig 4A and 4B ) and supported by recent reports that overexpression of the truncated GmSWEET39 increased oil in seeds [ 28 , 29 ]. Previous studies have shown that replacing or removing the C-terminal peptide of sugar transporters significantly increased the transport activity by increasing the affinity for the substrates [ 35 , 36 ].…”

“…Here, we revealed that the complex and highly correlated protein and oil traits were controlled by a single gene GmSWEET39 with two major types of alleles carrying CC- and CC+ that were highly associated with high oil and high protein, respectively. Differing from the two contemporary studies locating GmSWEET39 using genetic sweep-inferred approach followed by functional validation [ 28 , 29 ], we identified GmSWEET39 and its causative allele (CC Indel) underlying the long-pursued chr15 QTL using the classic genetics and high-resolution GWAS followed by uncovering its dual role for oil and protein improvement. Uncovering the causative gene and alleles for the long-pursued chr15 QTL and the dual functions of the GmSWEET39 alleles allows us to associate it tightly with soybean decades’ breeding practices and highlight its importance in increasing oil or protein during soybean domestication and improvement.…”

“…Previous studies have shown that replacing or removing the C-terminal peptide of sugar transporters significantly increased the transport activity by increasing the affinity for the substrates [ 35 , 36 ]. GmSWEET39 has ability to transport sugar [ 29 ], and our protein structural analysis predicted that C-terminal truncation changed its cytoplasmic domain structure. It will be interesting to experimentally test if C terminus truncated GmSWEET39 can facilitate the sugar transport across the membrane.…”

Transcriptome Profiling Reveals Spatial-temporal Dynamics of Gene Expression Essential for Soybean Seed Development

“…Accordingly, the numbers of the expressed genes that fell in the majority of those enriched terms were approximately doubled or tripled, such as hexose metabolic process (8 to 22), glycolysis (7 to 18) cellular nitrogen compound metabolic process (18 to 36), cellular amino acid biosynthetic process (15 to 32), Ribosomal proteins (47 to 132). It should be noted that no change in the numbers of the genes with the terms related to monolayer-surrounded lipid storage body (7), nutrient reservoir activity (11), and sulfur amino acid metabolic process (6 to 7) was observed, suggesting the importance of maintaining high transcript abundance of these genes for seed lling. Additional enriched GO terms for the 1,343 genes were identi ed, protein localization, glutamine family amino acid biosynthetic process, intracellular transport, gene silencing by RNA, vesicle-related components (COP-II-, COP-I, coated vesicle, transport vesicle, ER to Golgi transport vesicle, membrane-bounded vesicle).…”

“…Thus far, several genes involved in seed nutrient accumulation such as bZIP123 involved lipid accumulation and GA20OX-associated seed weight and oil accumulation [8][9][10][11] and genes associated with seed development [12] have been identi ed. The conservation in some regulatory processes of seed development between soybean and model plant Arabidopsis was revealed [7,13].…”