Circadian Clock Regulation of Starch Metabolism Establishes GBSSI as a Major Contributor to Amylopectin Synthesis in Chlamydomonas reinhardtii

Chlamydomonas reinhardtii displays a diurnal rhythm of starch content that peaks in the middle of the night phase if the algae are provided with acetate and CO₂ as a carbon source. We show that this rhythm is controlled by the circadian clock and is tightly correlated to ADP-glucose pyrophosphorylas...

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Published in:Plant physiology (Bethesda) 2006-09, Vol.142 (1), p.305-317
Main Authors: Ral, Jean-Philippe, Colleoni, Christophe, Wattebled, Fabrice, Dauvillée, David, Nempont, Clément, Deschamps, Philippe, Li, Zhongyi, Morell, Matthew K, Chibbar, Ravindra, Purton, Saul, d'Hulst, Christophe, Ball, Steven G
Format: Article
Language:English
Subjects:
Acetates
Algae
Amylopectin - biosynthesis
Animals
Biochemical Processes and Macromolecular Structures
Biochemistry
Biochemistry, Molecular Biology
Biological and medical sciences
Biological Clocks - physiology
Chlamydomonas reinhardtii
Chlamydomonas reinhardtii - genetics
Chlamydomonas reinhardtii - metabolism
Chlamydomonas reinhardtii - physiology
Circadian rhythm
Circadian Rhythm - physiology
Enzymes
Freshwater
Fundamental and applied biological sciences. Psychology
Gene expression regulation
Genes, Protozoan
Glucans
Glucose-1-Phosphate Adenylyltransferase - metabolism
Glucosyltransferases - genetics
Glucosyltransferases - metabolism
Life Sciences
Metabolism
Molecular Sequence Data
Photosynthesis, respiration. Anabolism, catabolism
Physiological regulation
Plant physiology and development
Plants
Starch Synthase - metabolism
Starches
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Summary:Chlamydomonas reinhardtii displays a diurnal rhythm of starch content that peaks in the middle of the night phase if the algae are provided with acetate and CO₂ as a carbon source. We show that this rhythm is controlled by the circadian clock and is tightly correlated to ADP-glucose pyrophosphorylase activity. Persistence of this rhythm depends on the presence of either soluble starch synthase III or granule-bound starch synthase I (GBSSI). We show that both enzymes play a similar function in synthesizing the long glucan fraction that interconnects the amylopectin clusters. We demonstrate that in log phase-oscillating cultures, GBSSI is required to obtain maximal polysaccharide content and fully compensates for the loss of soluble starch synthase III. A point mutation in the GBSSI gene that prevents extension of amylopectin chains, but retains the enzyme's normal ability to extend maltooligosaccharides, abolishes the function of GBSSI both in amylopectin and amylose synthesis and leads to a decrease in starch content in oscillating cultures. We propose that GBSSI has evolved as a major enzyme of amylopectin synthesis and that amylose synthesis comes as a secondary consequence of prolonged synthesis by GBSSI in arrhythmic systems. Maintenance in higher plant leaves of circadian clock control of GBSSI transcription is discussed.
ISSN:0032-0889
1532-2548
1532-2548
DOI:10.1104/pp.106.081885