Mono- and sesquiterpene release from tomato (Solanum lycopersicum) leaves upon mild and severe heat stress and through recovery: From gene expression to emission responses

• Mild heat stress did not affect foliage photosynthetic characteristics but severe heat stress lead to irreversible photosynthetic reductions.
• Severe heat stress resulted in changes in emissions of mono- and sesquiterpenes immediately after heat stress and during recovery.
• Heat stress lead to a sharp decline in the expression of β-phellandrene and (E)-β-caryophyllene/α-humulene synthase activity followed by a full recovery in leaves treated by mild heat stress.

Plants frequently experience heat ramps of various severities, but how and to what degree plant metabolic activity recovers from mild and severe heat stress is poorly understood. In this study, we exposed the constitutive terpene emitter, Solanum. lycopersicum leaves to mild (37 and 41 °C), moderate (46 °C) and severe (49 °C) heat ramps of 5 min and monitored foliage photosynthetic activity, lipoxygenase pathway volatile (LOX), and mono- and sesquiterpene emissions and expression of two terpene synthase genes, β-phellandrene synthase and (E)-β-caryophyllene/α-humulene synthase, through a 24 h recovery period upon return to pre-stress conditions. Leaf monoterpene emissions were dominated by β-phellandrene and sesquiterpene emissions by (E)-β-caryophyllene, and thus, these two terpene synthase genes were representative for the two volatile terpene classes. Photosynthetic characteristics partly recovered under moderate heat stress, and very limited recovery was observed under severe stress. All stress treatments resulted in elicitation of LOX emissions that declined during recovery. Enhanced mono- and sesquiterpene emissions were observed immediately after the heat treatment, but the emissions decreased even to below the control treatment during recovery between 2 and 10 h, and raised again by 24 h. The expression of β-phellandrene and (E)-β-caryophyllene synthase genes decreased between 2 and 10 h after heat stress, and recovered to pre-stress level in mild heat stress treatment by 24 h. Overall, this study demonstrates a highly sensitive heat response of terpenoid synthesis that is mainly controlled by gene level responses under mild stress, while severe stress leads to non-recoverable declines in foliage physiological and gene expression activities.