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MBE Advance Access originally published online on December 18, 2007
Molecular Biology and Evolution 2008 25(3):536-548; doi:10.1093/molbev/msm280
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© The Author 2007. Published by Oxford University Press on behalf of the Society for Molecular Biology and Evolution. All rights reserved. For permissions, please e-mail: journals.permissions@oxfordjournals.org

Research Articles

Metabolic Symbiosis and the Birth of the Plant Kingdom

Philippe Deschamps*,1, Christophe Colleoni*,1, Yasunori Nakamura{dagger}, Eiji Suzuki{dagger}, Jean-Luc Putaux{ddagger}, Alain Buléon§, Sophie Haebel||, Gerhard Ritte, Martin Steup, Luisa I. Falcón#, David Moreira**, Wolfgang Löffelhardt{dagger}{dagger}, Jenifer Nirmal Raj*, Charlotte Plancke*, Christophe d'Hulst*, David Dauvillée* and Steven Ball*

* Université des Sciences et Technologies de Lille, Unité Mixte de Recherches 8576 du Centre National de la Recherche Scientifique, Cité Scientifique, Villeneuve d'Ascq, France
{dagger} Faculty of Bioresource Sciences, Akita Prefectural University, Shimoshinjo-Nakano, Akita, Japan
{ddagger} Centre de Recherches sur les Macromolécules Végétales (CERMAV-CNRS), Grenoble, France—; Center of Mass Spectrometry of Biopolymers of the University of Potsdam, Golm, Germany
§ Institut National de la Recherche Agronomique, Centre de Recherches Agroalimentaires, Rue de la Géraudière, Nantes, France
|| Center of Mass Spectrometry of Biopolymers of the University of Potsdam
Plant Physiology, Institute of Biochemistry and Biology, University of Potsdam, Golm, Germany
# Departamento de Ecología Evolutiva, Instituto de Ecología, Universidad Nacional Autónoma de México, México
** Unite d'Ecologie, Systematique et Evolution, UMR CNRS 8079, Universite Paris-Sud, Orsay, France
{dagger}{dagger} Max F. Perutz Laboratories, Department of Biochemistry, University of Vienna, Vienna, Austria

E-mail: steven.ball{at}univ-lille1.fr.

Accepted for publication December 13, 2007.

Eukaryotic cells are composed of a variety of membrane-bound organelles that are thought to derive from symbiotic associations involving bacteria, archaea, or other eukaryotes. In addition to acquiring the plastid, all Archaeplastida and some of their endosymbiotic derivatives can be distinguished from other organisms by the fact that they accumulate starch, a semicrystalline-storage polysaccharide distantly related to glycogen and never found elsewhere. We now provide the first evidence for the existence of starch in a particular species of single-cell diazotrophic cyanobacterium. We provide evidence for the existence in the eukaryotic host cell at the time of primary endosymbiosis of an uridine diphosphoglucose (UDP-glucose)–based pathway similar to that characterized in amoebas. Because of the monophyletic origin of plants, we can define the genetic makeup of the Archaeplastida ancestor with respect to storage polysaccharide metabolism. The most likely enzyme-partitioning scenario between the plastid's ancestor and its eukaryotic host immediately suggests the precise nature of the ancient metabolic symbiotic relationship. The latter consisted in the export of adenosine diphosphoglucose (ADP-glucose) from the cyanobiont in exchange for the import of reduced nitrogen from the host. We further speculate that the monophyletic origin of plastids may lie in an organism with close relatedness to present-day group V cyanobacteria.

Key Words: Endosymbiosis • starch • plastid • glycogen


1 These authors contributed equally to this work.

William Martin, Associate Editor


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