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

Abstract

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.

Linking water relations and hydraulics with photosynthesis

“…Interestingly, recent modeling and experimental studies found S m , T cw and membrane permeability also influence the water transport efficiency through mesophyll tissues (Xiong et al, 2017). However, Lu et al (2019) did not find such relationships; in fact, they observed intraspecific relationships between the fraction of the mesophyll cell wall adjoining other cell walls (f cm ) and K ox among four crop species subjected to different K supplies. This result would suggest a major role of cell connectivity across tissues in the apoplastic pathway, contrasting with the greater vapor phase that could be associated with S m , which reflects cell exposure to intercellular spaces and thus increased surface for water evaporation along the water pathway.…”

“…Recently, the coordination of K leaf and mesophyll conductance to CO 2 (g m ), another major photosynthetic limitation factor (for review, see Flexas et al, 2012), across species and/or genotypes was suggested by several studies (Flexas et al, 2013;Xiong et al, 2017Xiong et al, , 2018Lu et al, 2019; Figure 2c). The g m accounts for the apparent diffusion efficiency of CO 2 from substomatal cavity through mesophyll cell components into the chloroplasts where biochemical assimilation occurs.…”

“…A , photosynthetic rate, g s , stomatal conductance, g m , mesophyll conductance, and K leaf , leaf hydraulic conductance. Gas exchange and K leaf data collected across different species (Xiong et al ., ; Lu et al ., ) and a wide range of environmental conditions, including high temperature (Huang et al ., ), light intensities (Loucos et al ., ), long‐term drought (Theroux‐Rancourt et al ., ) and potassium application (Lu et al ., ).…”

“…Hence, here we consider the coordination of g m and K leaf rather than K ox under dynamic conditions. The responses of g m and K leaf 0 10 20 30 40 50 Huang et al, 2017Loucos et al, 2017Lu et al 2019 Theroux Figure 2. The correlation between gas exchange parameters and leaf hydraulic conductance.…”

Temperature responses of photosynthesis and leaf hydraulic conductance in rice and wheat

“…They are suggested to be correlated across different plant species (Flexas et al, ) and across different genotypes within a single plant species (Xiong et al, ). Their coordination is also present when plants are subjected to drought stress (Wang et al, ), and potassium deficit (Lu et al, ). The coordination between g m and K leaf is important to the balance of plant carbon gain and water loss.…”