Hyper-efficient water transport enables the high photosynthetic performance of C4 grasses

Background/Question/Methods

Grasses dominate ≈40% of the Earth’s land surface, accounting for > 25% of terrestrial primary productivity, largely due to the abundance of species using C₄ photosynthesis. The C₄ photosynthesis syndrome is defined by a CO₂ concentrating mechanism and associated specialized leaf anatomy that drive high photosynthetic rate and water use efficiency especially under high temperatures or low CO₂ . C₄ is thus a model for the repeated evolution of a suite of traits that are of tremendous ecological importance. In experiments and comparative analyses on 28 grass species we determined for the first time the differences in hydraulic design between C₃ and C₄ grasses, and its relationships with stomatal conductance, photosynthetic rate, vein and mesophyll anatomy and climate of origin.

Results/Conclusions

C₄ grasses possess a specialized leaf hydraulic design. For C₃ grasses, as shown previously across diverse C₃ species, the leaf hydraulic conductance (K_leaf) was proportional to stomatal conductance (g_s). By contrast, for C₄ grasses, K_leaf was disproportionately high, independently of g_s. The high K_leaf/g_s for C₄ grasses was related to differences in leaf cell, tissue, vein and xylem traits. Physiological modeling showed that high K_leaf/g_s is critical to the success of C₄ grasses; without it, stomatal closure during typical transpiration would eliminate their photosynthetic advantage. Thus,  this “hyper-efficient” water transport as important an adaptation as C₄ biochemistry, enabling the photosynthetic advantage of C₄ over C₃ grasses both in moist soil and moderate drought. This integrated hydraulic-photosynthetic syndrome in C₄ grasses allows them to perform competitively under moist and drying conditions, and further explains the decoupling of photosynthetic gas exchange from mean annual rainfall for C₄ grasses across native ranges. These findings also support the expectation of a C₄ advantage in drying climates under rising CO₂ concentrations and temperatures.