Originally published as Genetics Published Articles Ahead of Print on February 3, 2008.

Genetics, Vol. 178, 2373-2387, April 2008, Copyright © 2008
doi:10.1534/genetics.108.087205

Early Gene Duplication Within Chloroplastida and Its Correspondence With Relocation of Starch Metabolism to Chloroplasts

Philippe Deschamps^*, Hervé Moreau, Alexandra Z. Worden, David Dauvillée^* and Steven G. Ball^*,1

^* Unité de Glycobiologie Structurale et Fonctionnelle, UMR8576 CNRS/USTL, Université des Sciences et Technologies de Lille, 59655 Villeneuve d'Ascq, France, Observatoire Océanologique, Laboratoire Arago, UMR 7628 CNRS-Université Paris VI, 66651 Banyuls-sur-mer, France and Monterey Bay Aquarium Research Institute, Moss Landing, California 95039-9644

¹ Corresponding author: UMR8576 CNRS, Bât. C9, Cité Scientifique, Université des Sciences et Technologies de Lille, 59655 Villeneuve d'Ascq, Cedex France.
E-mail: steven.ball{at}univ-lille1.fr

The endosymbiosis event resulting in the plastid of photosynthetic eukaryotes was accompanied by the appearance of a novel form of storage polysaccharide in Rhodophyceae, Glaucophyta, and Chloroplastida. Previous analyses indicated that starch synthesis resulted from the merging of the cyanobacterial and the eukaryotic storage polysaccharide metabolism pathways. We performed a comparative bioinformatic analysis of six algal genome sequences to investigate this merger. Specifically, we analyzed two Chlorophyceae, Chlamydomonas reinhardtii and Volvox carterii, and four Prasinophytae, two Ostreococcus strains and two Micromonas pusilla strains. Our analyses revealed a complex metabolic pathway whose intricacies and function seem conserved throughout the green lineage. Comparison of this pathway to that recently proposed for the Rhodophyceae suggests that the complexity that we observed is unique to the green lineage and was generated when the latter diverged from the red algae. This finding corresponds well with the plastidial location of starch metabolism in Chloroplastidae. In contrast, Rhodophyceae and Glaucophyta produce and store starch in the cytoplasm and have a lower complexity pathway. Cytoplasmic starch synthesis is currently hypothesized to represent the ancestral state of storage polysaccharide metabolism in Archaeplastida. The retargeting of components of the cytoplasmic pathway to plastids likely required a complex stepwise process involving several rounds of gene duplications. We propose that this relocation of glucan synthesis to the plastid facilitated evolution of chlorophyll-containing light-harvesting complex antennae by playing a protective role within the chloroplast.

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