Tansley Review No. 37 Circadian rhythms: their origin and control.

This article reviews the circadian rhythm of carbon dioxide metabolism in leaves of the Crassulacean plant Bryophyllum (Kalanchoë) fedtsckenkoi which persists both in continuous darkness and a CO -free atmosphere, and in continuous light and normal air. Under both conditions the rhythm is due to the periodic activity of the enzyme phosphoenolpyruvate carboxylase (PEPc). The physiological characteristics of the rhythm are described in detail and, from these characteristics, hypotheses are advanced to account for both the generation of the rhythm and the regulation of its phase and period by environmental factors. The periodic activity of PEPc is ascribed to the periodic accumulation of an allosteric inhibitor, malate, in the cytoplasm and its subsequent removal either to the vacuole in continuous darkness, or by metabolism in continuous light. Also involved in the generation of the rhythm is a periodic change in the sensitivity of PEPc to malate inhibition due to the periodic phosphorylation and dephosphorylation of PEPc which changes its K by a factor of 10 from 30 to 0.3 mM and vice versa. This periodic phosphorylation of PEPc is apparently achieved by the periodic synthesis and breakdown of a PEPc kinase which phosphorylates the enzyme on a serine residue; dephosphorylation is achieved by a type 2A phosphatase which shows no rhythmic variation. The induction of phase shifts in the rhythm in continuous darkness and CO -free air has been explained in terms of light and high-temperature activated gates or channels in the tonoplast which, when open, allow malate to diffuse between the vacuole and cytoplasm. For the rhythm in continuous light and normal air phase, control by environmental signals can be attributed to changes in the malate levels in critical cell compartments, or in particular cell populations such as the stomatal guard cells, due to regulation of the malate synthesizing enzyme system involving PEPc, and malic enzyme which is responsible for malate metabolism. The role of the stomata in the generation of the rhythm is also discussed. The biochemical events which appear to give rise to the well-studied circadian rhythms in leaf movement in Samanea and Albizza, in luminescence in Gonyaulax polyedra and in the synthesis of the chlorophyll a/b binding protein are also reviewed in an attempt to identify similarities between these events and those involved in the Bryophyllum rhythm. Finally, the somewhat similar nature of the genes apparently responsible for circadian rhythmicity in Neurospora and Drosophila are discussed, and suggestions made for utilizing anti-sense nucleic acid technology in the further elucidation of the critical biochemical events involved in the basic, temperature-compensated circadian oscillator in living organisms. CONTENTS Summary 347 I. Introduction 348 II. Occurrence of circadian rhythms 348 III. Physiological characteristics of circadian rhythms 349 IV. Biochemical and molecular events involved in the circadian rhythm in Bryophyllum leaves 362 V. Biochemical and molecular events involved in the origin and control of circadian rhythmicity in other organisms 366 VI. Genetic studies 370 VII. Conclusion 371 References 372.