Heat-Stress Memory Modulates Antioxidant Metabolism and Increases Senecionine Biosynthesis Across Developmental Stages of Senecio madagascariensis

Temperature stress strongly affects plant metabolism, and recurrent heat exposure can modify physiological responses depending on developmental stage. This study examined the biochemical and physiological adjustments of Senecio madagascariensis subjected to single (naïve) or repeated (primed) heat stress at 40 °C during vegetative and reproductive stages. Sampling was conducted after the second heat stress and after the subsequent recovery period. Principal component analyses (PCAs) revealed marked stage-specific contrasts. In the vegetative stage, PCA1 and PCA2 explained 75.7% of total variance, clearly separating treatments: naïve plants were associated with elevated proline, soluble sugars, phenolics, glycine betaine, hydrogen peroxide (H2O2) and lipid peroxidation, whereas primed plants were linked to enhanced superoxide dismutase (SOD) and ascorbate peroxidase (APX) activities and reduced oxidative markers. Under stress, naïve plants showed substantial increases in soluble sugars (+198%) and proline (+66.9%), whereas primed plants exhibited attenuated oxidative responses and reduce phenolic accumulation. After recovery, primed plants exhibited markedly reduced H2O2 levels (−57.5%) and lipid peroxidation, alongside higher SOD activity. In the reproductive stage, PCA indicated more subtle priming effects, with overlapping clusters among treatments. Primed plants accumulated the highest soluble sugar levels under stress (+276.5%), while naïve plants showed higher proline and glycine betaine levels. Following recovery, osmolyte levels were similar among groups. Senecionine remained unchanged during the vegetative stage but increased in both naïve (+21.4%) and primed (+19.1%) plants during the reproductive stage after recovery. Oxidative markers revealed contrasting patterns, with primed reproductive plants showed the lowest superoxide under stress but the highest H2O2 and lipid peroxidation at both time points. Overall, the findings demonstrate that heat-stress responses in S. madagascariensis are developmentally regulated, with stronger priming effects during vegetative growth and phenology-dependent metabolic adjustments during reproduction. All results are directly supported by the measured biochemical and physiological data.