Nature of the Periplastidial Pathway of Starch Synthesis in the Cryptophyte Guillardia theta

doi:10.1128/EC.00380-05

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Nature of the Periplastidial Pathway of Starch Synthesis in the Cryptophyte Guillardia theta

Philippe Deschamps,¹ Ilka Haferkamp,² David Dauvillée,¹ Sophie Haebel,³ Martin Steup,⁴ Alain Buléon,⁵ Jean-Luc Putaux,⁶ Christophe Colleoni,¹ Christophe d'Hulst,¹ Charlotte Plancke,¹ Sven Gould,⁷ Uwe Maier,⁷ H. Ekkehard Neuhaus,² and Steven Ball¹^*

CNRS, UMR8576, Cité Scientifique, 59655 Villeneuve d'Ascq, France,¹ Pflanzenphysiologie, Fachbereich Biologie, Technische Universität Kaiserslautern, D-67663 Kaiserslautern, Germany,² Center of Mass Spectrometry of Biopolymers,³ Plant Physiology, Institute of Biochemistry and Biology, University of Potsdam, 14476 Golm, Germany,⁴ Institut National de la Recherche Agronomique, Centre de Recherches Agroalimentaires, Rue de la Géraudière, BP 71627, 44316 Nantes Cedex 03, France,⁵ Centre de Recherches sur les Macromolécules Végétales, ICMG-CNRS, BP 53, F-38041 Grenoble Cedex 9, France,⁶ Philipps-Universität Marburg, Zellbiologie, Karl von Frisch-Strasse, D-35032 Marburg, Germany⁷

Received 22 December 2005/ Accepted 10 March 2006

The nature of the periplastidial pathway of starch biosynthesiswas investigated with the model cryptophyte Guillardia theta.The storage polysaccharide granules were shown to be composedof both amylose and amylopectin fractions with a chain lengthdistribution and crystalline organization very similar to thoseof starch from green algae and land plants. Most starch granulesdisplayed a shape consistent with biosynthesis occurring aroundthe pyrenoid through the rhodoplast membranes. A protein withsignificant similarity to the amylose-synthesizing granule-boundstarch synthase 1 from green plants was found as the major polypeptidebound to the polysaccharide matrix. N-terminal sequencing ofthe mature protein proved that the precursor protein carriesa nonfunctional transit peptide in its bipartite topogenic signalsequence which is cleaved without yielding transport of theenzyme across the two inner plastid membranes. The enzyme wasshown to display similar affinities for ADP and UDP-glucose,while the V_max measured with UDP-glucose was twofold higher.The granule-bound starch synthase from Guillardia theta wasdemonstrated to be responsible for the synthesis of long glucanchains and therefore to be the functional equivalent of theamylose-synthesizing enzyme of green plants. Preliminary characterizationof the starch pathway suggests that Guillardia theta utilizesa UDP-glucose-based pathway to synthesize starch.

* Corresponding author. Mailing address: CNRS, UMR8576, USTL, Bâtiment C9, Cité Scientifique, 59655 Villeneuve d'Ascq, France. Phone: 33 3 2043 6543. Fax: 33 3 2043 6555. E-mail: steven.ball{at}univ-lille1.fr.

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