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MBE Advance Access published online on August 11, 2008

Molecular Biology and Evolution, doi:10.1093/molbev/msn178
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© The Author 2008. 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

Evolutionary switch and genetic convergence on rbcL following the evolution of C4 photosynthesis

Pascal-Antoine Christin1, Nicolas Salamin1, A. Muthama Muasya2, Eric H. Roalson3, Flavien Russier1 and Guillaume Besnard1

1 Department of Ecology and Evolution, University of Lausanne, 1015 Lausanne, Switzerland
2 Botany Department, University of Cape Town, Private Bag X3, Rondebosch 7701, South Africa
3 School of Biological Sciences and Center for Integrated Biotechnology, Washington State University, Pullman, Washington 99164-4236, USA

Corresponding author Pascal-Antoine Christin, Department of Ecology and Evolution, Biophore, Quartier Sorge, 1015 Lausanne, Switzerland, Phone number: +41216924279, Fax number: +41216924165, pascal-antoine.christin{at}unil.ch

Received for publication June 30, 2008. Revision received July 31, 2008. Accepted for publication August 6, 2008.

Rubisco is responsible for the fixation of CO2 into organic compounds through photosynthesis and has thus a great agronomic importance. It is well established that this enzyme suffers from a slow catalysis, and its low specificity results into photorespiration, which is considered as an energy waste for the plant. However, natural variations exist and some Rubisco lineages, such as in C4 plants, exhibit higher catalytic efficiencies coupled to lower specificities. These C4 kinetics could have evolved as an adaptation to the higher CO2 concentration present in C4 photosynthetic cells. In this study, using phylogenetic analyses on a large dataset of C3 and C4 monocots, we showed that the rbcL gene, which encodes the large subunit of Rubisco, evolved under positive selection in independent C4 lineages. This confirms that selective pressures on Rubisco have been switched in C4 plants by the high CO2 environment prevailing in their photosynthetic cells. Eight rbcL codons evolving under positive selection in C4 clades were involved in parallel changes among the 23 independent monocot C4 lineages included in this study. These amino acids are potentially responsible for the C4 kinetics and their identification opens new roads for human-directed Rubisco engineering. The introgression of C4-like high efficiency Rubisco would strongly enhance C3 crop yields in the future CO2 enriched atmosphere.

Key Words: Rubisco • Molecular evolution • Positive selection • C4 photosynthesis • convergence • monocots


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