Transient photoinhibition and photo-oxidative stress as an integral part of stress acclimation and plant development in a dioecious tree adapted to Mediterranean ecosystems

Mastic trees (Pistacia lentiscus L.) are dioecious perennial plants that are highly adapted to Mediterranean climates but display a high sensitivity to winter periods. In order to understand how sex, leaf phenology and ecological context could condition sensitivity to winter and associated mechanisms to acclimate to these conditions, photoinhibition and photo-oxidative stress markers were examined in mastic trees (P. lentiscus) from a natural population growing in the Garraf Natural Park for a consecutive 12-month period (seasonal study), as well as in three populations naturally growing in the Montseny Natural Park, including the highest altitudes described for this species, during winter (altitudinal study). Results from these studies indicate that both the winter period and higher elevation influenced the degree of photoinhibition, but this was not conditioned by sex. In fact, winter photoinhibition occurred transiently even though it was accompanied by chlorophyll loss and malondialdehyde contents. Stress acclimation was achieved through biochemical adjustments in chloroplasts, characterized by anthocyanin shielding, increased de-epoxidation state of the xanthophyll cycle as well as tocopherol accumulation, and phenological adaptations, the latter allowing a complete resetting of the physiological performance of leaves. Moreover, although females showed higher lipid peroxidation than males during the coldest winter months, at the highest elevation and during flowering in spring, this oxidative stress was mild and transient with no negative consequences for the physiology of plants. It is concluded that evergreen mastic trees acclimate to winter conditions and higher elevations by activation of antioxidant defenses together with phenological adjustments, altogether playing a crucial role in plant survival. Sexual dimorphism in mastic trees appears as a relevant factor when considering sensitivity to photo-oxidative stress in winter and altitudinal conditions.