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

Background: 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. Methods: Potato seedlings were subjected to four light treatments simulating different shade signals: 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). We conducted a comprehensive study integrating morphological characterization, leaf anatomical analysis, hormone quantification, transcriptome sequencing, and metabolite profiling. Results: 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). 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, significantly diverging from the PHYB-centric model established in Arabidopsis. Overall design: The experiment utilized 20-day-old potato plants (Solanum tuberosum L. cv. Atlantic) provided by the Agricultural Biotechnology Research Center, Ningxia Academy of Agriculture and Forestry Sciences. This cultivar was selected for its vigorous growth and broad adaptability. Virus-free plantlets were obtained through tissue culture and subcultured for three generations before experiment. Only plants with uniform growth were selected and transferred to soil, where they were acclimated for 14 days under a 16-h light/8-h dark cycle at 60% relative humidity. The growth environment simulated artificial shading conditions, with temperature maintained at 23-25°C. The experiment was conducted with six plants per treatment group. Light treatments were implemented using combinations of different LED light sources, including white light, blue light (400-499 nm), red light (600-699 nm), and far-red light (700-750 nm). To establish low R:FR conditions, far-red light (peak wavelength 730 nm) was supplemented to white light. For low blue light conditions, white light was passed through two layers of yellow filter (#101, Lee Filters, CA, USA). Light quality and intensity were measured using a HiPoint HR-350 spectrometer (wavelength range: 380-780 nm, accuracy: ±2 nm), and R:FR ratios were calculated according to the method described by Lyu et al [30]. Four light treatments were established to assess plant responses under varying light conditions. The white light treatment (WL) applied full-spectrum white LEDs with peak wavelengths at 450 nm and 570 nm, simulating a daylight-like spectrum. In the low blue light treatment (LBL), white light filtered through yellow filters, reducing blue light intensity to 1.5 µmol·m?²·s?¹. For low R:FR treatment (WL+FR), far-red light was added to the white light, resulting in an R:FR ratio of 0.41. The fourth treatment combined WL+FR and LBL, and was referred to as LBL+FR. Photosynthetically active radiation (PAR) was maintained at 500 µmol m?²s?¹ to observe plant responses during the transition from etiolation to de-etiolation. Light quality parameters were monitored every 2 h throughout a 14-day treatment period, with detailed records of photon flux density (PPFD; 400-750 nm) under each treatment condition