Photosynthetic Entrainment of the Circadian Clock Facilitates Plant Growth under Environmental Fluctuations: Perspectives from an Integrated Model of Phase Oscillator and Phloem Transportation

Abstract

Plants need to avoid carbon starvation and resultant growth inhibition under fluctuating light environments to ensure optimal growth and reproduction. As diel patterns of carbon metabolism are influenced by the circadian clock, appropriate regulation of the clock is essential for plants to properly manage their carbon resources. For proper adjustment of the circadian phase, higher plants utilize environmental signals such as light or temperature and metabolic signals such as photosynthetic products; the importance of the latter as phase regulators has been recently elucidated. A mutant of Arabidopsis thaliana that is deficient in phase response to sugar has been shown, under fluctuating light conditions, to be unable to adjust starch turnover and to realize carbon homeostasis. Whereas, the effects of light entrainment on growth and survival of higher plants are well studied, the impact of phase regulation by sugar remains unknown. Here we show that endogenous sugar entrainment facilitates plant growth. We integrated two mathematical models, one describing the dynamics of carbon metabolism in A. thaliana source leaves and the other growth of sink tissues dependent on sucrose translocation from the source. The integrated model predicted that sugar-sensitive plants grow faster than sugar-insensitive plants under constant as well as changing photoperiod conditions. We found that sugar entrainment enables efficient carbon investment for growth by stabilizing sucrose supply to sink tissues. Our results highlight the importance of clock entrainment by both exogenous and endogenous signals for optimizing growth and increasing fitness.

Plant behaviour: A mathematical approach for understanding intra-plant communication

“…• The starch degradation rate τ as is simpler respect to the definition provided 148 in [41] and [42], and it does not depend on a subjective dusk [44]. Even 149 considering the simplification adopted in this paper for starch degradation, its 150 dynamic remains correct (see file S1 in supporting information for demonstration); 151…”

“…As in [42], we assumed the respiration to be proportional to the sucrose content. The former has a frequency of r m = 0.79 1 h .…”

“…For instance, we tested the adaptation of the 334 model to different light periods. In [42], it is shown how plant changes its metabolism 335 and its sucrose content when day length changes from 8h to 16h ( Fig 5). [42].…”

“…In [42], it is shown how plant changes its metabolism 335 and its sucrose content when day length changes from 8h to 16h ( Fig 5). [42]. Dynamic of sucrose content in sinks in Arabidopsis when passing from 8h to 16h of light (in top left plot) and vice versa (in the top right plot).…”

“…In fact, our 339 model correctly predicts this dynamic as shown in Fig 6. Just like in [42], in the day when photoperiod changes, plant adapts its behaviour in 341 an intermediate way, to fix it during successive days.…”