Transcriptomic signatures of developing soybean seeds reveal the molecular mechanisms of oil accumulation during domestication

Seed oil content, a crucial nutritional trait in soybean, has been reshaped by domestication; however, the transcriptomic mechanisms underlying this change remain incompletely understood. Here, we sequenced seed transcriptomes from six soybean accessions - four cultivated (two high-oil, two medium-oil) and two wild (low-oil) - across four developmental stages (S1-S4). To identify transcriptional drivers of oil enhancement during domestication, we integrated differential expression, weighted gene co-expression network, core network, domestication signature and regulator target enrichment analyses across three comparisons: cultivated high-oil versus wild, cultivated medium-oil versus wild and all cultivated versus wild. Differences in oil accumulation were associated with two module classes: cultivated/wild-specific (cultivated-positive, wild-negative) and S1/S4 stage-specific (cultivated S1-positive, wild S4-negative). The cultivated/wild-specific modules were enriched for lipid storage, lipid localization and carbohydrate metabolism. Core network analysis identified two oil biosynthetic pathways - a lipid regulatory axis (BCCP2-SAD-FAD2-OBO/FA9) and a PLIP1-dependent pathway - both coupled to glycolysis (GPT2-GAPDH-PK). The S1/S4 stage-specific modules were enriched for carbohydrate and lipid metabolism. Their core networks highlighted a GmLEC1a-GmWRI1a/GmWRI1b cascade that coordinates cell wall metabolism, glycolysis, fatty acid synthesis and sterol biosynthesis. Furthermore, the S1/S4 stage-specific modules were enriched for domestication signatures, and the co-expression of oil content and seed-size genes suggests co-domestication of these traits. Thus, soybean domestication enhanced seed oil content by rewiring early (S1) transcriptional networks through a GmLEC1a-GmWRI1b cascade that directs carbon flux into fatty acid synthesis and triacylglycerol biosynthesis. We prioritized 15 synergistic targets - four transcription factors (GmLEC1a, GmWRI1a, GmWRI1b, ICE1) and 11 metabolic/structural genes (e.g. SAD.3, β-PDH.2, BC, LIL3:1) - for precision breeding to improve seed oil content.