From cellular micro-compartmentation to inter-organ communications : the kinetic basis for molecular controls in photoperiodism

Abstract

An autonomous self-sustained ~24 h oscillation of metabolic activity functions as a physiological clock to allow living systems seasonal adaptation of behaviour, like flowering or hibernation. Until recently circadian rhythms were considered to be a characteristic of eukaryotic cells despite a very early report by Halberg on the observation of a circadian rhythm in E. coli. With the detection of circadian oscillations of metabolic activity in Synechococcus, circadian rhythmicity has proven to exist on all levels of biological organisation from prokaryotic cells to unicellular eukaryotes to higher plants, animals and man. Circadian rhythmicity is an in viva feature of living cells and cannot be observed in vitro. Higher frequency oscillations, however, can be found in many biochemical reactions in vitro as well as in viva. This overview on rhythmic organisation of metabolism in living systems will discuss how macro-parameters like pH, ionic balances (osmos), redox state and phosphorylation potential or hydrophobicity control metabolic functions like photosynthesis, respiration, nitrogen fixation. The temporal control of metabolic pathways involves oscillatory networks in transcription, translation or posttranslational modulation of protein structure and function. Changes in macroparameter status are due to precise feedback networks in basic metabolism leading to a circadian rhythm in overall energy metabolism and thus in metabolic control of timing. Multifactorial changes in environmental conditions like light intensity and -quality, temperature, water status, ionic balances, pressure, etc. are transduced into a network of intracellular signal processing leading to a combinatorial interaction of transcription factors and outputs with cell-, tissue- and organ-specific response-patterns. Compartmentation is coupled to vectorial metabolism and electron transport and the involvement of membrane pores and ion channels. The generation of specific changes in membrane potential can be expected. The physical state of membranes is involved in the transduction of temperature signals and the control of expression of nuclear, mitochondrial and plastid genes which also can be modulated by photoreceptors like the red / far red reversible phytochromes, the blue / UV-A and the UV-B photoreceptors and the feeding of sugars. Membrane-bound processes are controlling and vice versa are controlled by voltage gated ion channels and pores, giving rise to an overall electro-chemical-hydraulic integration of organs and the whole organism on the basis of Mitchell's chemiosmotic theory of energy transduction. The electrophysiological integration offers the possibility for characterisation of cells, organs and organisms by electrophysiogrammes as a means for non-invasive continuous in vivo monitoring of physiology and behaviour