Analysis and Simulation of Circadian Multi-Oscillator Systems in a Crassulacean Acid Metabolism Plant

Crassulacean acid metabolism (CAM) is an adaptation of photosynthetic organisms to drought stress: improved water-use efficiency is achieved by an optimized temporal arrangement of photosynthetic subprocesses, which are driven by an endogenous pacemaker, i.e. a circadian clock. The present work deals with the hypothesis that the circadian rhythm of gas-exchange of entire leaves of the CAM plant Kalanchoë daigremontiana has to be understood as the collective signal of the population of cells in the leaf. In this multi-oscillator picture, certain features of the whole-leaf rhythm can be understood as a desynchronization of the population due to noise and synchronization due to common environmental stimuli, respectively. This hypothesis is checked by comparison of numerical simulations of uncoupled populations of two different phenomenological models of circadian rhythms to experimental data obtained from monitoring the spatio-temporal metabolic dynamics in the leaf by means of chlorophyll-fluorescence imaging. The comparison shows that the features of the whole-leaf rhythm are also exhibited by each individual cell, hence the predicted emergence of new effects at the population level cannot be confirmed. Further spatio-temporal analyses and simulations suggest that pattern formation and the appearance of synchronized clusters in the leaf are induced by spatially heterogeneous fluctuations of environmental parameters. A further focus of interest is on the analysis of multi-variate time-series of whole-leaf gas exchange. Comparison of numerical simulations based on a physiological model of CAM to experimental data suggests that circadian rhythm generation cannot be understood by considering a single pacemaker situated at the metabolic level. Rather, evidence is presented that the observable rhythms are the output of a functional network of multiple original oscillators, situated at multiple levels from gene expression to stomatal guard cells. Future work, both experimental and numerical, is proposed to address questions of pattern formation by spatial heterogeneity, as well as unraveling the network structure of circadian rhythm generation in CAM