Spatiotemporal variation of metabolism in a plant circadian rhythm: The biological clock as an assembly of coupled individual oscillators

The complex dynamic properties of biological timing in organisms remain a c entral enigma in biology despite the increasingly precise genetic character ization of oscillating units and their components. Although attempts to obt ain the time constants from oscillations of gene activity and biochemical u nits have led to substantial progress, we are still far from a full molecul ar understanding of endogenous rhythmicity and the physiological manifestat ions of biological clocks. Applications of nonlinear dynamics have revoluti onized thinking in physics and in biomedical and life sciences research, an d spatiotemporal considerations are now advancing our understanding of deve lopment and rhythmicity. Here we show that the well known circadian rhythm of a metabolic cycle in a higher plant, namely the crassulacean acid metabo lism mode of photosynthesis, is expressed as dynamic patterns of independen tly initiated variations in photosynthetic efficiency (phi (PSII)) over a s ingle leaf. Noninvasive highly sensitive chlorophyll fluorescence imaging r eveals randomly initiated patches of varying phi (PSII) that are propagated within minutes to hours in wave fronts, forming dynamically expanding and contracting clusters and clearly dephased regions of phi (PSII). Thus, this biological clock is a spatiotemporal product of many weakly coupled indivi dual oscillators, defined by the metabolic constraints of crassulacean acid metabolism. The oscillators operate independently in space and time as a c onsequence of the dynamics of metabolic pools and limitations of CO2 diffus ion between tightly packed cells.