Quercus suber (cork oak) is a sustainably exploited forest resource, producing a unique renewable raw material known as cork. With drought events imposing a negative impact on tree vitality, further research is needed to enhance our understanding of the genetic and environmental factors regulating cork development, to foster the resilience of cork oak ecosystems. We focused on characterizing long-term drought-induced molecular adaptations occurring in stems, and identifying key genetic pathways regulating phellem development. One-year-old cork oak plants were grown for 6 months under well-watered, or water-deficit (WD) conditions and main stems were targeted for histological characterization and transcriptomic analysis. WD treatment reduced meristem activity at both vascular cambium and phellogen, impairing secondary growth. Transcriptional analysis revealed a global downregulation of genes related to cell division, differentiation, and cell wall biogenesis in phellem, inner bark, and xylem under WD conditions. Phellem and inner bark showed upregulation of photosynthesis-related genes, highlighting a determinant role of stem photosynthesis in the adaptation to long-term drought. We show that developing phellem cells contain chloroplasts and their abundance increases under WD. Lastly, we propose new candidate regulatory genes involved in regulating phellogen activity and demonstrate the role of phellem in drought-induced bark photosynthesis in young plants.
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