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Starch Granule Initiation in Arabidopsis Requires the Presence of Either Class IV or Class III Starch Synthases^[W]

^a Unité de Glycobiologie Structurale et Fonctionnelle, Unité Mixte de Recherche 8576, Centre National de la Recherche Scientifique, Université des Sciences et Technologies de Lille, 59655 Villeneuve d'Ascq Cedex, France
^b Instituto de Bioquímica Vegetal y Fotosíntesis, Consejo Superior de Investigaciones Científicas-Universidad de Sevilla, Isla de la Cartuja, 41092-Sevilla, Spain
^c Instituto de Recursos Naturales, Centro de Ciencias Medioambientales, Consejo Superior de Investigaciones Científicas, 28006-Madrid, Spain
^d Instituto de Agrobiotecnología (Consejo Superior de Investigaciones Científicas, Universidad Pública de Navarra, Gobierno de Navarra), 31192 Mutiloabeti, Nafarroa, Spain
^e Institute of Botany, Slovak Academy of Sciences, SK-84523 Bratislava, Slovakia
^f Unité de Recherche Biopolymères, Assemblages et Interactions, Centre Institut National de la Recherche Agronomique de Nantes, 44316 Nantes Cedex 3, France

² Address correspondence to angel{at}ibvf.csic.es.

The mechanisms underlying starch granule initiation remain unknown. We have recently reported that mutation of soluble starch synthase IV (SSIV) in Arabidopsis thaliana results in restriction of the number of starch granules to a single, large, particle per plastid, thereby defining an important component of the starch priming machinery. In this work, we provide further evidence for the function of SSIV in the priming process of starch granule formation and show that SSIV is necessary and sufficient to establish the correct number of starch granules observed in wild-type chloroplasts. The role of SSIV in granule seeding can be replaced, in part, by the phylogenetically related SSIII. Indeed, the simultaneous elimination of both proteins prevents Arabidopsis from synthesizing starch, thus demonstrating that other starch synthases cannot support starch synthesis despite remaining enzymatically active. Herein, we describe the substrate specificity and kinetic properties of SSIV and its subchloroplastic localization in specific regions associated with the edges of starch granules. The data presented in this work point to a complex mechanism for starch granule formation and to the different abilities of SSIV and SSIII to support this process in Arabidopsis leaves.