Cell-level anatomy explains leaf age-dependent declines in mesophyll conductance and photosynthetic capacity in the evergreen Mediterranean oak Quercus ilex subsp. rotundifolia

David Alonso-Forn, José Javier Peguero-Pina, Juan Pedro Ferrio, José Ignacio García-Plazaola, Rubén Martín-Sánchez, Ülo Niinemets, Domingo Sancho-Knapik, Eustaquio Gil-Pelegrín, Cell-level anatomy explains leaf age-dependent declines in mesophyll conductance and photosynthetic capacity in the evergreen Mediterranean oak Quercus ilex subsp. rotundifolia, Tree Physiology, 2022;, tpac049, https://doi.org/10.1093/treephys/tpac049

Leaves of Mediterranean evergreen tree species experience a reduction in net CO2 assimilation (AN) and mesophyll conductance to CO2 (gm) during aging and senescence, which would be influenced by changes in leaf anatomical traits at cell level. Anatomical modifications can be accompanied by the dismantling of photosynthetic apparatus associated to leaf senescence, manifested through changes at biochemical level (i.e., lower nitrogen investment in photosynthetic machinery). However, the role of changes in leaf anatomy at cell level and nitrogen content in gm and AN decline experienced by old non-senescent leaves of evergreen trees with long leaf lifespan is far from being elucidated. We evaluated age-dependent changes in morphological, anatomical, chemical and photosynthetic traits in Quercus ilex subsp. rotundifolia Lam., an evergreen oak with high leaf longevity. All photosynthetic traits decreased with increasing leaf age. The relative change in cell wall thickness (Tcw) was less than in chloroplast surface area exposed to intercellular air space (Sc/S), and Sc/S was a key anatomical trait explaining variations in gm and AN among different age classes. The reduction of Sc/S were related to ultrastructural changes in chloroplasts associated to leaf aging, with a concomitant reduction in cytoplasmic nitrogen. Changes in leaf anatomy and biochemistry were responsible for the age-dependent modifications in gm and AN. These findings revealed a gradual physiological deterioration related to the dismantling of the photosynthetic apparatus in older leaves of Q. ilex subsp. rotundifolia.

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