Seasonal adaptation strategies of heteroblastic foliage in Pinus massoniana seedlings: insights into sugar composition, osmotic regulation, and protective enzyme mechanisms

Pinus massoniana displays heteroblastic foliage during the first growing season, forming primary needle seedlings (PNS) and secondary needle seedlings (SNS). Significant differences exist between primary and secondary needles in morphology, seasonal photosynthetic physiology, and growth patterns. However, their responses to seasonal temperature variations remain poorly understood. We systematically compare seasonal physiological adjustments of the PNS and SNS, focusing on carbohydrate dynamics, osmotic regulation, and stress-responsive enzyme activities under natural temperature gradients. The progressive accumulation of malondialdehyde with declining temperatures, accompanied by rapid starch-to-sucrose conversion driven by elevated sucrose phosphate synthase activity, indicates that PNS is more sensitive to cold than SNS. This physiological shift results in increased sucrose and L-fucose concentrations, synergistically enhanced by proline accumulation and superoxide dismutase-mediated antioxidant defense. In contrast, SNS exhibits a distinct metabolic reprogramming characterized by amplified sucrose cleavage, leading to substantial accumulation of maltose, glucose, D-fructose, and inositol. Additionally, SNS prioritized osmotic homeostasis through soluble protein synthesis and peroxidase activation, thereby maintaining osmotic balance and protecting cellular integrity. Collectively, these findings reveal distinct physiological differences in the responses of PNS and SNS to seasonal temperature variations. As such, a theoretical framework is developed to better understand key traits that enable conifer species to adapt to environmental stressors associated with changing climates.