Spatio-temporal variation of photosynthetic activity during the endogenous circadian CAM rhythm of Kalanchoë daigremontiana: the biological clock as an assembly of coupled nonlinear oscillators

The complex dynamical properties of biological timing in organisms could never be fully accounted for, not even by increasingly precise characterization of oscillating units and their components. The circadian rhythm of CO2 exchange of the crassulacean acid metabolism plant Kalanchoe daigremontiana is regarded as a generic model system for exploration of endogenous rhythmicity in a well understood metabolic pathway. While the CAM-rhythm so far was thought to be solely time-dependent, we show here for the first time that the circadian rhythm of a metabolic cycle in a higher plant is expressed as independently initiated variations in photosynthetic efficiency (f PSII) over a single leaf. Non-invasive, highly sensitive chlorophyll fluorescence imaging under well controlled external conditions reveals dynamic clusters, moving wave fronts and clearly dephased regions of f PSII. This is the first demonstration that this biological clock is a spatio-temporal product of many weakly coupled oscillators. These oscillators are defined by the metabolic constraints of CAM but operate independently in space and time as a consequence of the dynamics of metabolic pools and limitations of CO2 diffusion between tightly packed cells. Several, especially long term aspects of this biological clock are strongly related to the self-organization of the interacting oscillators in space. We propose that synchronization of these individual oscillators is essential for the functioning of the biological clock.