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Published on July 14, 2006; 10.1104/pp.106.081885

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Received April 12, 2006
Accepted July 3, 2006

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

Jean-Philippe Ral , Christophe Colleoni , Fabrice Wattebled , David Dauvillée , Clément Nempont , Philippe Deschamps , Zhongyi Li , Matthew K. Morell , Ravindra Chibbar , Saul Purton , Christophe d'Hulst , and Steven G. Ball *

From the Unité de Glycobiologie Structurale et Fonctionnelle, UMR8576 CNRS/USTL, IFR 118, Université des Sciences et Technologies de Lille, 59655 Villeneuve d'Ascq, Cedex France
From the CSIRO Plant Industry, GPO Box 1600, Canberra, ACT 2601, Australia
From the Plant Biotechnology Institute, National Research Council of Canada, 110 Gymnasium Place, Saskatoon, Saskatchewan, Canada S7N 0W9
From the Department of Biology, University College London, Gower street WC1E 6BT, London, UK

* Corresponding author; email: steven.ball{at}univ-lille1.fr.

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 the ADP-glucose pyrophosphorylase activity. Persistence of this rhythm depends on the presence of either soluble starch synthase III (SSIII) 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 becomes required to obtain maximal polysaccharide contents and fully compensates for the loss of SSIII. A point mutation in GBSSI gene that prevents extension of amylopectin chains but retains the enzyme's normal ability to extend malto-oligosaccharides 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 arhythmic systems. The maintenance in higher plant leaves of circadian clock control of GBSSI transcription is discussed.




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