Light and nutrient stress interactively regulate phenylpropanoid metabolism via substrate competition and ROS/RNS signaling

Plants allocate fixed carbon between growth and defense based on environmental constraints, yet how light and nutrient interactively regulate this trade-off remains unclear. Here we demonstrate that high-light/low-nutrient combination synergistically enhances phenylpropanoid synthesis in Agastache rugosa via ROS/RNS signaling and substrate competition cascades. Plants were grown under factorial light (0% and 50% shade) and nutrient (40–160 mg kg−1) levels in a nested design. Path analysis revealed that nutrient supply strongly promotes free amino acid accumulation (β = 0.789), which negatively regulates chalcone synthase activity (β = −0.412), confirming substrate competition between protein synthesis and phenylpropanoid production. Simultaneously, high-light increases hydrogen peroxide and inhibits nitric oxide levels (β = −0.811), yet these ROS/RNS molecules function as complementary signaling mediators that positively regulate shikimic acid synthesis and phenylalanine ammonia-lyase activity (β = 0.789). This dual regulatory mechanism increased shikimic acid and chalcone synthase activity under high-light/low-nutrient conditions by 6-fold and 5-fold, respectively, than low-light/low-nutrient treatment, resulting in increases in flavonoid and ascorbic acid content. Principal component analysis confirmed light conditions explain 52.5% of metabolic variance, with nutrient availability modulating response magnitude. These findings establish that environmental stress combinations elicit non-additive metabolic responses through integrated substrate competition and ROS/RNS signaling networks, providing a mechanistic framework for optimizing bioactive compound production in medicinal plants.

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