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Multilevel Control of Organelle DNA Sequence Length in Plants

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Abstract

We have compared the length of noncoding organelle DNA spacers in a broad sample of plant species characterized by different life history traits to test hypotheses regarding the nature of the mechanisms driving changes in their size. We first demonstrate that the spacers do not evolve at random in size but have experienced directional evolutionary trends during plant diversification. We then study the relationships between spacer lengths and other molecular features and various species attributes by taking into account population genetic processes acting within cell lineages. Comparative techniques are used to test these relationships while controlling for species phylogenetic relatedness. The results indicate that spacer length depends on mode of organelle transmission, on population genetic structure, on nucleotide content, on rates of molecular evolution, and on life history traits, in conformity with predictions based on a model of intracellular competition among replicating organelle genomes.

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Acknowledgments

We are grateful to Jean Bousquet, Arndt Hampe, and Marc-André Selosse for their critical comments on an early version of the manuscript. We thank Béatrice Albert, Anne Atlan, Christian Biémont, Henri Caron, Manuela Casasoli, Deena Decker-Walters, François Delmotte, Claude dePamphilis, Laurent Duret, Joe Felsenstein, Jean-Marc Frigério, Theodore Garland Jr, Pauline Garnier-Géré, Berthold Heinze, Antoine Kremer, Emilia Martins, Brian Morton, Sophie Nadot, Carmen Palacios, David Pot, Jonathan Silvertown, and Dorothy Steane for discussions and help during this work. The research was supported by grants from the EC research program FAIR5-CT97–3795 and by the Bureau des Ressources Génétiques to R. J. Petit.

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Author notes

  1. Jérôme Duminil

    Present address: Laboratoire d’Eco-Ethologie Evolutive, Université Libre de Bruxelles, Bruxelles, Belgium

  2. Delphine Grivet

    Present address: Department of Forest Systems and Resources, Forest Research Institute, CIFOR-INIA, Madrid, 28040, Spain

  3. Sylvain Jeandroz

    Present address: UPSP PROXISS, ENESAD, Dijon, France

Authors and Affiliations

  1. INRA, UMR Biodiversité, Gènes & Communautés, 69 route d’Arcachon, Cestas, 33612, France

    Jérôme Duminil, Delphine Grivet & Rémy J. Petit

  2. Laboratoire de Biométrie et Biologie Evolutive, Université Lyon 1, UMR 5558, Lyon, France

    Sébastien Ollier

  3. Interactions Arbres/Micro-organismes, Université Nancy I, UMR 1136, Nancy, France

    Sylvain Jeandroz

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  1. Jérôme Duminil
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Correspondence to Rémy J. Petit.

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Duminil, J., Grivet, D., Ollier, S. et al. Multilevel Control of Organelle DNA Sequence Length in Plants. J Mol Evol 66, 405–415 (2008). https://doi.org/10.1007/s00239-008-9095-3

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