Leaf anatomical adaptations have central roles in photosynthetic acclimation to humidity

Rates of photosynthesis can be lower in plants grown under conditions of high leaf-to-air vapour pressure difference (VPD) than under low VPD. Leaf phenotype plasticity is a primary factor determining photosynthetic responses to environmental stimuli. However, it remains unclear how changes in leaf anatomical traits drive photosynthetic acclimation to high VPD. Here, we examined the role of leaf anatomy in the differing photosynthetic responses of two tomato cultivars (Jinpeng and Zhongza) to long-term growth under high and low VPD. Photosynthesis was not affected by VPD in Jinpeng. This was attributed to homeostasis in stomatal conductance (gs) and, to a lesser extent, mesophyll conductance (gm). Disruption of synchronized changes to cell size in the epidermis and mesophyll meant that growth under high VPD reduced stomatal density in Jinpeng, but minor vein density remained unchanged. Thus, water supplied by the veins could support the increased transpirational demand, preventing stomatal closure. Variation in VPD did not affect mesophyll cell structures, and therefore gm, in Jinpeng. By contrast, photosynthesis in Zhongza was reduced under high VPD, which was primarily attributed to decreased gs and gm. The former was mainly induced by decreased stomatal aperture. Thus, transpirational demand exceeded water supply in Zhongza. This was likely due to coordinated decreases in stomatal and minor vein density driven by synchronized increases in epidermal and mesophyll cell size under high VPD. Liquid-phase limitation was primarily responsible for the reduced gm in Zhongza under high VPD. High VPD induced an increase in liquid-phase resistance by reducing the mesophyll surface area exposed to intercellular air spaces and increasing cytosolic resistance. These results suggest that plasticity in epidermal and mesophyll cell size provides an efficient means of regulating photosynthesis during acclimation to long-term high VPD.