Integrated omics revealed regulatory mechanisms governing potato (Solanum tuberosum L.) seedling growth during shade avoidance syndrome

Potato (Solanum tuberosum L.) is the fourth largest food crop worldwide with significant economic value and importance for food security. Shade avoidance syndrome (SAS) considerably affects crop architecture and productivity in high-density planting systems; however, its molecular mechanisms in potato remain poorly understood. Potato seedlings were subjected to four light treatments: white light (control, WL), low blue light (LBL, simulating blue light attenuation by plant canopies), low red: far-red ratio (WL + FR, simulating far-red reflection from neighboring plants), and their combination (LBL + FR, simulating complete plant shade environment). An integrated analysis including morphological characterization, leaf anatomical observations, hormone quantification, transcriptome sequencing, and metabolite profiling was performed to investigate plant responses to these conditions. Morphological analysis revealed that WL + FR primarily induced internode elongation (+ 20.0%) and leaf hyponasty, while LBL promoted stem elongation through increased node production (+ 36.3%). When combined, these signals (LBL + FR) synergistically enhanced stem elongation by 79.3%. Anatomical examination showed that LBL-treated leaves formed thickened palisade tissue layers (176.34 μm) with 6–7 layers of spongy tissue, whereas WL + FR resulted in thinner leaves (151.22 μm). Hormone profiling revealed that LBL increased gibberellic acid 3 (GA₃) and indole-3-acetic acid (IAA) levels, while WL + FR further elevated IAA. LBL + FR markedly increased zeatin riboside (ZR) level, highlighting intricate hormonal crosstalk underlying shade-avoidance responses. Transcriptomic analysis identified 6,057 differentially expressed genes enriched in photosynthesis, hormone signaling, and carbohydrate metabolism pathways. A total of 1,168 differentially accumulated metabolites were detected across treatments, particularly organic acids and lipids associated with TCA (tricarboxylic acid) cycle and starch-sucrose metabolism. Weighted gene co-expression network analysis (WGCNA) identified PHYTOCHROME A (PHYA) as the central hub gene coordinating SAS responses under combined light stress, contrasting with the PHYB-centric model established in Arabidopsis. These findings provide comprehensive insights into potato-specific SAS regulatory networks and contribute to understanding crop-specific light sensing strategies, with potential applications for breeding shade-tolerant varieties and applications for optimizing plant architecture in high-density planting systems.