How are leaf carbon- and water-related traits coordinated acclimation to elevated CO2 by its anatomy? A case study in tomato

Abstract

A fundamental behavior for plants will be to minimize transpirational water loss whilst maximize photosynthesis in order to acclimate complex growth conditions. However, elevated CO 2 is expected to result in photosynthesis acclimation, the primary limitations and mechanisms underlying the concerted changes of leaf photosynthesis and hydraulic conductance are not fully understood. To test the acclimation of photosynthetic carbon gain and transpirational water loss to elevated CO 2 concentration, we conducted a study in cherry tomatoes grown under two CO 2 levels with different water and fertilizer management. Leaf anatomical traits associated with photosynthesis and hydraulics were also measured. Tomato plants showed greater photosynthesis and lower hydraulic conductance under high CO 2 conditions. However, as durative high concentration of CO 2 injection, photosynthetic rate and hydraulic conductance significantly decreased in both high- and low-water treatments, yet the decrease could be mitigated by conducting fertilizer. Further quantitative analysis showed that mesophyll limitation (ML) and outside-xylem hydraulic resistance (R ox ) were the major contributors to photosynthetic and hydraulic acclimation under durative elevated CO 2 exposure. High water and fertilization treatments decreased the ML and R ox , which supported the higher photosynthetic rate and hydraulic conductance of plants grown under extended elevated CO 2 condition. The acclimation to durative elevated CO 2 concentration is partly attributed to the modification of leaf anatomy. The lower leaf vein length per area (VLA) or the mesophyll cell to cell connectivity (f cm ) which supported lower water transport conductivity of xylem and outside-xylem in elevated CO 2 and low-water treatments. Additionally, a reduction of mesophyll (S m ) and/or chloroplast (S c ) surface area adjacent to intercellular space in CO 2 gas-phase paths with the time of high CO 2 injection was also observed, which may responsible for lower g m , thus photosynthesis acclimation. Coordination of leaf photosynthesis and hydraulics was changed under durative elevated CO 2 condition. Only g m and K ox , the main contributor of photosynthesis and hydraulics, existed a coordinated relationship by modifying their common structural basis, as the volume fraction of the intercellular air space (f ias ) and mesophyll surface area adjacent to intercellular space (S m ). These results will be helpful for better understanding of plants acclimate to future CO 2 enriched condition and are of significance to agricultural management. • Tomato showed a lower hydraulic cost of photosynthesis under elevated CO 2 . • Coordination of leaf photosynthesis and hydraulics was changed under durative elevated CO 2 condition. • The coordination of g m and K ox influenced the photosynthetic carbon gain and hydraulics of tomatoes grown under elevated CO 2 . • Leaf morpho-anatomical traits drive the long-term acclimation to elevated CO 2 concentration.