Impact of heat priming on heat shock responses in Origanum vulgare: Enhanced foliage photosynthetic tolerance and biphasic emissions of volatiles

Climate change enhances the frequency of heatwaves that negatively affect photosynthesis and can alter constitutive volatile emissions and elicit emissions of stress volatiles, but how pre-exposure to mildly warmer temperatures affects plant physiological responses to subsequent severe heat episodes remains unclear, especially for aromatic plants with high and complex volatile defenses. We studied the impact of heat shock (45 °C/5 min) applied alone and after exposure to moderate heat stress (35 °C/1 h, priming) on foliage photosynthesis and volatile emissions in the aromatic plant Origanum vulgare through 72 h recovery period. Heat stress decreased photosynthesis rates and stomatal conductance, whereas the reductions in photosynthesis were primarily due to non-stomatal factors. In non-primed plants, heat shock-induced reductions in photosynthetic activity were the greatest, but photosynthetic activity completely recovered by the end of the experiment. In primed plants, a certain inhibition of photosynthetic activity remained, suggesting a sustained priming effect. Heat shock enhanced the emissions of volatiles including lipoxygenase pathway volatiles, long-chained fatty acid-derived compounds, mono- and sesquiterpenes, geranylgeranyl diphosphate pathway volatiles, and benzenoids, whereas different heat treatments resulted in unique emission blends. In non-primed plants, stress-elicited emissions recovered at 72 h. In primed plants, volatile emissions were multiphasic, the first phase, between 0.5 and 10 h, reflected the primary stress response, whereas the secondary rise, between 24 and 72 h, indicated activations of different defense metabolic pathways. Our results demonstrate that exposure to mild heat leads to a sustained physiological stress memory that enhances plant resistance to subsequent severe heat stress episodes. •Heat stress decreased leaf photosynthesis via non-stomatal factors.•Photosynthetic reductions were lower in plants pre-exposed to mild heat (priming).•Heat stress enhanced volatile emissions differently in primed and non-primed plants.•Volatile emissions recovered earlier in primed plants but later rose again.•Priming improves resistance and acclimation during subsequent severe heat stress.