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MBE Advance Access published online on December 18, 2007
Molecular Biology and Evolution, 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 Article

Metabolic Symbiosis and the Birth of the Plant Kingdom

Philippe Deschamps1,{dagger}, Christophe Colleoni1,{dagger}, Yasunori Nakamura2, Eiji Suzuki2, Jean-Luc Putaux3, Alain Buléon4, Sophie Haebel5, Gerhard Ritte6, Martin Steup6, Luisa I. Falcón7, David Moreira8, Wolfgang Loffelhardt9, Jenifer Nirmal Raj1, Charlotte Plancke1, Christophe d'Hulst1, David Dauvillée1 and Steven Ball1

1 CNRS, UMR8576, Cité Scientifique, 59655 Villeneuve d'Ascq, France
2 Faculty of Bioresource Sciences, Akita Prefectural University, Shimoshinjo-Nakano, Akita 010-0195, Japan
3 Centre de Recherches sur les Macromolécules Végétales (CERMAV-CNRS), BP 53, F-38041 Grenoble cedex 9, France - affiliated with Université Joseph Fourier and member of the Institut de Chimie Moléculaire de Grenoble
4 Institut National de la Recherche Agronomique, Centre de Recherches Agroalimentaires, Rue de la Géraudière, BP71627, 44316 Nantes cedex 03, France
5 Center of Mass Spectrometry of Biopolymers of the University of Potsdam
6 Plant Physiology, Institute of Biochemistry and Biology, University of Potsdam, 14476 Golm, Germany
7 Departamento de Ecología Evolutiva, Instituto de Ecología, Universidad Nacional Autónoma de México, 04510, México
8 Unite d'Ecologie, Systematique et Evolution, UMR CNRS 8079, Universite Paris-Sud, batiment 360, 91405 Orsay Cedex, France
9 Max F. Perutz Laboratories, University of Vienna, Department of Biochemistry, Dr. Bohrgasse 9, 1030 Vienna, Austria

Corresponding author: Steven G. Ball, CNRS, UMR8576, Cité Scientifique, 59655 Villeneuve d'Ascq, France. Tel.: + 33 3 20436543 - Fax: + 33 3 20436555, Steven.ball{at}univ-lille1.fr

Received for publication September 28, 2007. Revision received November 22, 2007. 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 semi-crystalline 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 UDP-glucose-based pathway similar to that characterized in amoebas. Because of the monophyletic origin of plants, we can define the genetic make-up 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 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.

{dagger} These authors contributed equally to this work


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