Integrated transcriptome and metabolome analysis reveals molecular networks underlying soybean responses to shade stress

Intercropping and high-density planting are effective ways to increase soybean yield but may trigger shade avoidance syndrome (SAS), a response that causes excessive stem elongation and lodging and significantly reduces productivity. To elucidate the molecular mechanisms governing this adaptation, integrated transcriptomic and metabolomic analyses were conducted by using two contrasting varieties: the highly shade-tolerant Guixiadou 105 (GX) and the sensitive Zhizidou (ZZ). Our findings demonstrate that these varieties utilize divergent strategies to manage shade. RNA-seq analyses revealed numerous SAS-related differentially expressed genes (SAS_DEGs) enriched in plant hormone signaling, flavonoid/isoflavonoid biosynthesis, carbon fixation, photosynthesis, and MAPK signaling. The sensitive ZZ variety adopts a costly "escape" strategy, doubling plant height through massive accumulation of auxin (IAA) and the activation of key genes such as GA20OX2, PIF4A and GASAs , but reduction of gibberellin (GA) content. In contrast, the tolerant GX maintains structural and metabolic stability by restraining elongation and uniquely accumulating flavonoids and organic acids, which are hypothesized to serve as biochemical buffers against light-induced stress. By constructing a putative transcriptional regulatory and gene-metabolite (TRN–GMP) network, we identified candidate transcription factor hubs from the AP2/ERF, MYB , and bHLH families that associate environmental perception with hormonal metabolic outputs. These molecular networks suggest that shade tolerance is associated with a coordinated balance between growth reinforcement and metabolic homeostasis rather than a single pathway. Collectively, our results highlight a coordinated hormonal crosstalk where IAA accumulation in the shoot apex concurs with GA-responsive pathways to activate shade-induced elongation, even in the absence of elevated GA levels. The shade-sensitive ZZ prioritizes rapid escape through this integrated hormonal response, whereas the shade-tolerant GX prioritizes metabolic stability. These mechanistic insights provide valuable targets for genetic studies of SAS and breeding shade-resilient cultivars in soybean.