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BIOCHEMICAL PROCESSES AND MACROMOLECULAR STRUCTURES

Circadian Clock Regulation of Starch Metabolism Establishes GBSSI as a Major Contributor to Amylopectin Synthesis in Chlamydomonas reinhardtii^1,[W],[OA]

Unité de Glycobiologie Structurale et Fonctionnelle, Unité Mixte de Recherche 8576, Centre National de la Recherche Scientifique, Université des Sciences et Technologies de Lille, Institut Fédératif de Recherche, 59655 Villeneuve d'Ascq cedex, France (J.-P.R., C.C., F.W., D.D., C.N., P.D., C.d.H., S.G.B.); CSIRO Plant Industry, Canberra, Australian Capital Territory 2601, Australia (Z.L., M.K.M.); Plant Biotechnology Institute, National Research Council of Canada, Saskatoon, Saskatchewan, Canada S7N 0W9 (R.C.); and Department of Biology, University College London, London WC1E 6BT, United Kingdom (S.P.)

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.

² These authors contributed equally to the paper.

³ Present address: CSIRO Plant Industry, GPO Box 1600, Canberra, ACT 2601, Australia.

The author responsible for distribution of materials integral to the findings presented in this article in accordance with the policy described in the Instructions for Authors (www.plantphysiol.org) is: Steven G. Ball (steven.ball{at}univ-lille1.fr).

^[W] The online version of this article contains Web-only data.

^[OA] Open Access articles can be viewed online without a subscription.

www.plantphysiol.org/cgi/doi/10.1104/pp.106.081885

^* Corresponding author; e-mail steven.ball{at}univ-lille1.fr; fax 33–3–20–43–65–55.

Received April 12, 2006; accepted July 3, 2006.

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