Integrating omics approaches to discover and prioritize candidate genes involved in oil biosynthesis in soybean

Soybean is one of the major sources of edible protein and oil. Oil content is a quantitative trait that is significantly determined by genetic and environmental factors. Over the past 30 years, a large volume of soybean genetic, genomic, and transcriptomic data have been accumulated. Nevertheless, integrative analyses of such data remain scarce, in spite of their importance for crop improvement. We hypothesized that the co-occurrence of genomic regions for oil-related traits in different studies may reveal more stable regions encompassing important genetic determinants of oil content and quality in soybean. We integrated publicly available data, obtained with distinct techniques, to discover and prioritize candidate genes involved in oil biosynthesis and regulation in soybean. We detected key fatty acid biosynthesis genes (e.g., BCCP and ACCase, FADs, KAS family proteins) and several transcripton factors, which are likely regulators of oil biosynthesis. In addition, we identified new candidates for seed oil accumulation and quality, such as Glyma.03G213300 and Glyma.19G160700, which encode a translocator protein and a histone acetyltransferase, respectively. Further, oil and protein genomic hotspots are strongly associated with breeding and not with domestication, suggesting that soybean domestication prioritized other traits. The genes identified here are promising targets for breeding programs and for the development of soybean lines with increased oil content and quality.

Identification of Non-Pleiotropic Loci in Flowering and Maturity Control in Soybean

Pleiotropy is considered to have a significant impact on multi-trait evolution, but its roles in the evolution of domestication-related traits in crop species have been unclear. In soybean, several known quantitative trait loci (QTL) controlling maturity, called the maturity loci, are known to have major effects on both flowering and maturity in a highly correlated pleiotropic manner. Aiming at the identification of non-pleiotropic QTLs that independently control flowering and maturity and dissecting the effects of pleiotropy in these important agronomic traits, we conducted a QTL mapping experiment by creating a population from a cross between domesticated soybean G. max and its wild ancestor G. soja that underwent stringent selection for non-pleiotropy in flowering and maturity. Our QTL mapping analyses using the experimental population revealed novel loci that acted in a non-pleiotropic manner: R1-1 controlled primarily flowering and R8-1 and R8-2 controlled maturity, while R1-1 overlapped with QTL, affecting other agronomic traits. Our results suggest that pleiotropy in flowering and maturity can be genetically separated, while artificial selection during soybean domestication and diversification may have favored pleiotropic loci such as E loci that control both flowering and maturity. The non-pleiotropic loci identified in this study will help to identify valuable novel genes to optimize soybean’s life history traits and to improve soybean’s yield potential under diverse environments and cultivation schemes.

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

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 GmSWEET10a. The selection of GmSWEET10a 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, GmSWEET10b was found to be functionally redundant with its homologue GmSWEET10a and to be undergoing selection in current breeding, leading the 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.

Genetic Control and Geo-Climate Adaptation of Pod Dehiscence Provide Novel Insights into Soybean Domestication

Loss of pod dehiscence was a key step in soybean [Glycine max (L.) Merr.] domestication. Genome-wide association analysis for soybean shattering identified loci harboring Pdh1, NST1A and SHAT1-5. Pairwise epistatic interactions were observed, and the dehiscent Pdh1 overcomes resistance conferred by NST1A or SHAT1-5 locus. Further candidate gene association analysis identified a nonsense mutation in NST1A associated with pod dehiscence. Geographic analysis showed that in Northeast China (NEC), indehiscence at both Pdh1 and NST1A were required in cultivated soybean, while indehiscent Pdh1 alone is capable of preventing shattering in Huang-Huai-Hai (HHH) valleys. Indehiscent Pdh1 allele was only identified in wild soybean (Glycine soja L.) accession from HHH valleys suggesting that it may have originated in this region. No specific indehiscence was required in Southern China. Geo-climatic investigation revealed strong correlation between relative humidity and frequency of indehiscent Pdh1 across China. This study demonstrates that epistatic interaction between Pdh1 and NST1A fulfills a pivotal role in determining the level of resistance against pod dehiscence, and humidity shapes the distribution of indehiscent alleles. Our results give further evidence to the hypothesis that HHH valleys was at least one of the origin centers of cultivated soybean.