Mechanistic roles of GmSWEET10a/b and GmSUT1 in the oil–protein balance in soybean mature seeds at transcriptional and metabolic levels

Previous investigations indicated that the soybean (Glycine max) SUGARS WILL EVENTUALLY BE EXPORTED TRANSPORTER10a/b (GmSWEET10a/b) genes promote oil accumulation, while inhibiting protein accumulation in seeds. To clarify the mechanisms modulated by GmSWEET10a/b in mediating the oil and protein accumulations in soybean seeds, an integrated comparative multiomics was conducted using the double gmsweet10a,b mutant and wild-type (WT) embryos. Spatial metabolomic analysis revealed that gmsweet10a,b embryos were surrounded by a sugar-reduced seed coat and experienced a sugar-starvation state in embryonic tissues in vivo. The decreased sugar content in the gmsweet10a,b embryos reduced the availability of carbon skeletons required for oil synthesis and was associated with decreased expression levels of genes involved in sucrose metabolism, fatty acid biosynthesis, and triacylglycerol assembly. Meanwhile, the expression of genes encoding storage protein was induced in gmsweet10a,b embryos, when compared with WT. These changes resulted in decreased oil content and increased protein content in gmsweet10a,b embryos versus WT. In vitro sugar-starvation assay also supported the suppression of fatty acid biosynthesis and the enhanced storage protein accumulation in developmental embryo under sugar-starved conditions. Furthermore, the knockout of SUCROSE TRANSPORTER 1 (GmSUT1), which was upregulated in gmsweet10a,b embryos, significantly decreased the sugar level, resulting in lower oil content but higher protein content in gmsut1 embryos than WT ones. Our findings provided a mechanistic understanding of the modulation of sugar transport between seed coat to embryo by both GmSWEET10a/b and GmSUT1, which plays a pivotal role in balancing oil and protein accumulations in soybean mature seeds.