Photosynthesis is led by stomatal circadian rhythm and not by starch depletion after a long period of darkness

The circadian rhythm is an endogenous rhythm, defined by repeated metabolic oscillations every 24 hours under constant parameters. In plants, the circadian rhythm regulates the growth through photosynthesis and the management of carbohydrates. In indoor farming, the photoperiod is independent from the sunlight and is of interest to increase energy savings. In this work, we studied the effects of modifications of photoperiods on indoor-grown lettuces (L. sativa), which were then not tuned with the circadian rhythm. The pattern of photoperiods applied was: 16/12-16/8-16/8. A mutant-free study was carried out to avoid genes shutdown unintended side effects and to evaluate the impact of the circadian rhythm under marketable production conditions. We observed that the circadian regulation of the stomatal conductance was the main limiting factor of net photosynthesis when the photoperiod is exceptionally not tuned with the circadian rhythm. In our experiment, the disruption of the circadian rhythm decreased the photosynthetic activity by 6.2% throughout the light period, with no alteration of the yield, morphology or light and water use efficiencies. Furthermore, starch depletion induced by the changes in the photoperiod could not explain variations of the net photosynthetic activity during the following light period. Interestingly, disrupting the circadian rhythm saved 5% of lighting time compared to the control, which can be converted into energy savings. Consequently, the circadian rhythm can be defined as a limiting factor for reducing energy consumption in indoor farming. Further characterization of the links between the photosynthesis-carbohydrates-growth continuum and the circadian rhythm is thus required.