Circadian Regulation Does Not Optimize Stomatal Behaviour.

Víctor Resco De Dios,Ximeng Li,Damien Landais,Yinan Yao,David T Tissue,Michael Bahn,Alexandru Milcu,Rachael H Nolan,Arthur Gessler,William R.L Anderegg,Jacques Roy

doi:10.3390/plants9091091

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.

Highlights

Circadian rhythms regulate the temporal pattern of the transcription of ~30% of the plant genome [1]
We modelled temporal patterns in gas exchange using Generalized Additive Models (GAM)
We observed that the oscillation of gs could not be predicted by current optimization models, suggesting that, contrary to conventional wisdom, circadian regulation does not directly lead to optimal stomatal behaviour or, alternately, that circadian regulation may provide benefits but current optimization models may not account for a key mechanism or cost to capture this behaviour

Summary

Introduction

Circadian rhythms regulate the temporal pattern of the transcription of ~30% of the plant genome [1]. Diurnal variation in photosynthesis and stomatal conductance, among other processes such as growth [2] and respiration [3], is affected by circadian regulation. Resonance between circadian rhythms in gas exchange and environmental cues has been documented to increase plant growth [5,6,7,8,9] because circadian regulation underlies the temporal partitioning and synchronization of different processes associated with carbon metabolism. Circadian regulation affects stomatal behaviour and the proportion of the diurnal oscillation in stomatal conductance (gs ) that is currently attributed to the clock, amounting to 30–35% of the total daytime variation [4,11], is larger than the previously clock-attributed variation in photosynthesis

Methods

Results

Conclusion