Rapid variation in leaf water status results in large reductions in photosynthesis due to reduced liquid phase diffusion of CO2 in the mesophyll

Background/Question/Methods

Until recently, stomatal conductance to CO₂ was considered to be the major limiting factor for photosynthesis, particularly under moderate drought conditions. As stomatal conductance relates to leaf water relations this forms an indirect link between photosynthesis and plant water status. Recently, mesophyll conductance to CO₂ has also been shown to be limiting to photosynthesis, and vary rapidly in response to light and CO₂ concentration. While current data suggests that mesophyll conductance is reduced by drought, to date there is no mechanism for this effect. Indeed, the nature of CO₂ transport across mesophyll cell plasma membranes and chloroplast membranes remains poorly understood. The most provocative explanation of membrane permeability to CO₂ has been the demonstration that membrane CO₂ permeability is associated with aquaporin function. Therefore, we aim to: further investigate the nature of CO₂ diffusion within the leaf, and determine if there are direct links between leaf water status and photosynthesis.  

Results/Conclusions

When transpiring leaves were allowed to rehydrate, by cutting petioles under water, a fast reduction in photosynthesis occurred within a couple of minutes (from 0 to 80% reduction). This effect was only present in leaves that initially had considerably negative leaf water potentials, resulting in large (>1bar) changes in turgor. Fluorescence based estimates of mesophyll conductance demonstrated that the observed reductions in photosynthesis were due to combined changes in stomatal and mesophyll conductance, and that the rapid change was mainly due to reductions in mesophyll conductance. Further experiments using low O₂, high CO₂, CO₂ response curve analysis, and a novel light perturbation approach confirmed that the turgor related photosynthetic reduction was likely to be due changes in mesophyll conductance, and not other photosynthetic parameters. This provides the first evidence of a direct effect of leaf water relations on mesophyll conductance to CO₂. This mesophyll conductance effect neatly coincides with the gating effect of turgor on the water transport function of aquaporins, although this novel hypothesis requires further corroboration. This turgor effect indicates that transpiring leaves have more complex regulation of photosynthesis by leaf water relations than the indirect effects of water status on stomata.