Unveiling resilience mechanisms of Quercus ilex seedlings to severe water stress: Changes in non-structural carbohydrates, xylem hydraulic functionality and wood anatomy

Over the last few decades, extensive dieback and mortality episodes of Quercus ilex L. have been documented after severe drought events in many Mediterranean forests. However, the underlying physiological, anatomical, and biochemical mechanisms remain poorly understood. We investigated the physiological and biochemical processes linked to embolism formation and non-structural carbohydrates (NSCs) dynamics in Q. ilex seedlings exposed to severe water stress and rewatering. Measurements of leaf gas exchange, water relations, non-structural carbohydrates, drought-related gene expression, and anatomical changes in wood parenchyma were assessed. Under water stress, the midday stem water potential dropped below - 4.5 MPa corresponding to a ~ 50% loss of hydraulic conductivity. A 70% reduction in stomatal conductance led to a strong depletion of wood NSCs. Starch consumption, resulting from the upregulation of the β-amylase gene BAM3, together with the downregulation of glucose (GPT1) and sucrose (SUC27) transport genes, suggests glucose utilization to sustain cellular metabolism in the wood parenchyma. After rewatering, the presence of residual xylem embolism led to an incomplete recovery of leaf gas exchanges. However, the partial restoration of photosynthesis allowed the accumulation of new starch reserves in the wood parenchyma and the production of new narrower vessels. In addition, changes in the cell wall composition of the wood parenchyma fibres were observed. Our findings indicate that thirty days of rewatering were sufficient to restore the NSCs reserves and growth rates of Q. ilex seedlings and that the carryover effects of water stress were primarily caused by hydraulic dysfunction.