C4 photosynthesis and hydraulics in grasses

Abstract

Summary The anatomical reorganization required for C4 photosynthesis should also impact plant hydraulics. Most C4 plants possess large bundle sheath cells and high vein density, which should also lead to higher leaf capacitance and hydraulic conductance (Kleaf). Paradoxically, the C4 pathway reduces water demand and increases water use efficiency, creating a potential mismatch between supply capacity and demand in C4 plant water relations. Here, we use phylogenetic analyses, physiological measurements, and models to examine the reorganization of hydraulics in closely related C4 and C3 grasses. The evolution of C4 disrupts the expected positive correlation between maximal assimilation rate (Amax) and Kleaf, decoupling a canonical relationship between hydraulics and photosynthesis generally observed in vascular plants. Evolutionarily young C4 lineages have higher Kleaf, capacitance, turgor loss point, and lower stomatal conductance than their C3 relatives. By contrast, species from older C4 lineages show decreased Kleaf and capacitance. The decline of Kleaf through the evolution of C4 lineages was likely controlled by the reduction in outside‐xylem hydraulic conductance, for example the reorganization of leaf intercellular airspace. These results indicate that, over time, C4 plants have evolved to optimize hydraulic investments while maintaining the anatomical requirements for the C4 carbon‐concentrating mechanism.