Key message. In droughted oak foliage, water shortage and carbon starvation caused structural injury varying in severity between cell types and indicative of adaptive reversible and degenerative irreversible processes.
Warmer temperatures as a consequence of climate change have already started to affect forest ecosystems, enhancing drought frequency and severity. Also depending on drought chronicity and ontological tissue development, tree foliage can respond to drought by enhancing structural acclimation and thus delay injury. More comprehensive characterization of micromorphological responses in foliage is needed for evaluating the tolerance of forest trees in the future. In the present study, structural reactions in foliage of three oak species exposed to acute summer drought were analyzed using transmitted light, fluorescence and electron microscopy. Oak leaves withstood drought stress for a considerable length of time before injury in the form of necrotic leaf margins appeared. In the leaf parts still asymptomatic, structural changes indicative of water stress and carbon starvation were observed. In the epidermis, autophagic processes–with exocytosis of degraded material–contributed to cell wall thickening. However, they also accelerated the degeneration of cell content whereas stomatal guard cells often remained unscathed. In mesophyll, the material in autolytic vesicles was internalized in vacuoles, which contributed to maintaining the cell turgescence. Plugging of xylem and phloem cells with polysaccharidic and proteinic material was mechanistically related to necrosis of leaf margins. These structural changes were indicative of reversible adaptive and irreversible degenerative processes. The functionality of upper mesophyll and stomata was prioritized, allowing foliage to resume gas exchange within hours of rewatering. Hence, extensive structural changes within still asymptomatic parts of the foliage were accountable in increasing the drought tolerance of the oaks.