Circadian Regulation Does Not Optimize Stomatal Behaviour

Abstract

The circadian clock is a molecular timer of metabolism that affects the diurnal pattern of stomatal conductance (gs), amongst other processes, in a broad array of plant species. The function of circadian gs regulation remains unknown and here, we test whether circadian regulation helps to optimize diurnal variations in stomatal conductance. We subjected bean (Phaseolus vulgaris) and cotton (Gossypium hirsutum) canopies to fixed, continuous environmental conditions of photosynthetically active radiation, temperature, and vapour pressure deficit (free-running conditions) over 48 h. We modelled gs variations in free-running conditions to test for two possible optimizations of stomatal behaviour under circadian regulation: (i) that stomata operate to maintain constant marginal water use efficiency; or (ii) that stomata maximize C net gain minus the costs or risks of hydraulic damage. We observed that both optimization models predicted gs poorly under free-running conditions, indicating that circadian regulation does not directly lead to stomatal optimization. We also demonstrate that failure to account for circadian variation in gs could potentially lead to biased parameter estimates during calibrations of stomatal models. More broadly, our results add to the emerging field of plant circadian ecology, where circadian controls may partially explain leaf-level patterns observed in the field.

Midday water use efficiency in sorghum is linked to faster stomatal closure rate, lower stomatal aperture and higher stomatal density

“…Similar results were also shown in field-grown sorghum under mild water stress and high temperatures (Pan et al, 2022), compared with the wellwatered, controlled conditions of this study. This suggests that mechanisms other than gas exchange optimisation are regulating iWUE in sorghum leaves, as was also observed for other C 4 species (Meinzer & Grantz, 1990) and C 3 crops (Eyland et al, 2021;Resco de Dios et al, 2020). Over a wide range of conditions, the relationship between A n and g s in C 4 leaves is curvilinear (Gilbert et al, 2011;Li et al, 2017).…”

Role of Circadian Rhythms in Major Plant Metabolic and Signaling Pathways

“…The regulation of this oscillator affects the diurnal fluctuation in the stomatal conductance and photosynthesis process and various processes, such as respiration and growth. Even the behavior of stomata gets affected by circadian regulation ( de Dios et al, 2020 ). The fraction of the diurnal pattern of variation in the stomatal conductance, which is allocated to the clock, is higher in amount during the changes in the daytime than in the changes allocated to the clock by photosynthesis.…”

Short‐term variation in leaf‐level water use efficiency in a tropical forest

“…This behavior, in systems with a fixed photoperiod, is thought to be adaptive as a means of maximizing carbon assimilation (Resco de Dios et al ., 2016). Higher than optimal morning g s would lead to elevated estimates of g 1 , which is consistent with previous findings that suggest circadian regulation fails to help to optimize diurnal variations in stomatal conductance (Resco de Dios et al ., 2020).…”

“…Other research has focused on the temporal consistency of stomatal parameters (Resco de Dios et al ., 2020), or the conditions in which the g s response should be optimized (Katul et al ., 2010). Plants may optimize their stomatal operation across a variety of time scales, from near instantaneous response to stimuli such as sunflecks (Way & Pearcy, 2012; Campany et al ., 2016), diurnal responses such as those to drying soil (Knapp, 1993; Zhang et al ., 2018), and long‐term responses such as those which optimize water and nutrient uptake by roots (Franklin, 2007).…”