C4 photosynthesis and hydraulics in grasses

Abstract

• 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 (K_leaf). 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 (A_max) and K_leaf, decoupling a canonical relationship between hydraulics and photosynthesis generally observed in vascular plants. Evolutionarily young C₄ lineages have higher K_leaf, capacitance, turgor loss point, and lower stomatal conductance than their C₃ relatives. By contrast, species from older C₄ lineages show decreased K_leaf and capacitance. The decline of K_leaf 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.