Potassium mediates coordination of leaf photosynthesis and hydraulic conductance by modifications of leaf anatomy

Typical symptoms of potassium deficiency, characterized as chlorosis or withered necrosis, occur concomitantly with downregulated photosynthesis and impaired leaf water transport. However, the prominent limitations and mechanisms underlying the concerted decreases of leaf photosynthesis and hydraulic conductance are poorly understood. Monocots and dicots were investigated based on responses of photosynthesis and hydraulic conductance and their components and the correlated anatomical determinants to potassium deficiency. We found a conserved pattern in which leaf photosynthesis and hydraulic conductance concurrently decreased under potassium starvation. However, monocots and dicots showed two different hydraulic-redesign strategies: Dicots tended to show a decreased minor vein density, whereas monocots reduced the size of the bundle sheath and its extensions, rather than the minor vein density; both of these strategies may restrain xylem and outside-xylem hydraulic conductance. Additionally, potassium-deprived leaves developed with fewer mesophyll cell-to-cell connections, leading to a reduced area being available for liquid-phase flow. Further quantitative analysis revealed that mesophyll conductance to CO2 and outside-xylem hydraulic resistance were the major contributors to photosynthetic limitation and increased hydraulic resistance, at more than 50% and 60%, respectively. These results emphasize the importance of potassium in the coordinated regulation of leaf photosynthesis and hydraulic conductance through modifications of leaf anatomy.