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

Abstract 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.