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MBE Advance Access originally published online on May 21, 2009
Molecular Biology and Evolution 2009 26(8):1909-1919; doi:10.1093/molbev/msp103
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© The Author 2009. 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

Phylogenomics of C4 Photosynthesis in Sedges (Cyperaceae): Multiple Appearances and Genetic Convergence

Guillaume Besnard*,1, A. Muthama Muasya{dagger}, Flavien Russier*, Eric H. Roalson{ddagger}, Nicolas Salamin*,§ and Pascal-Antoine Christin*

* Department of Ecology and Evolution, University of Lausanne, Lausanne, Switzerland
{dagger} Botany Department, University of Cape Town, Private Bag X3, Rondebosch, South Africa
{ddagger} School of Biological Sciences and Center for Integrated Biotechnology, Washington State University, Pullman, USA
§ Swiss Institute of Bioinformatics, Genopode, Lausanne, Switzerland

E-mail: g.besnard{at}imperial.ac.uk.

Accepted for publication May 5, 2009.

C4 photosynthesis is an adaptive trait conferring an advantage in warm and open habitats. It originated multiple times and is currently reported in 18 plant families. It has been recently shown that phosphoenolpyruvate carboxylase (PEPC), a key enzyme of the C4 pathway, evolved through numerous independent but convergent genetic changes in grasses (Poaceae). To compare the genetics of multiple C4 origins on a broader scale, we reconstructed the evolutionary history of the C4 pathway in sedges (Cyperaceae), the second most species-rich C4 family. A sedge phylogeny based on two plastome genes (rbcL and ndhF) has previously identified six fully C4 clades. Here, a relaxed molecular clock was used to calibrate this tree and showed that the first C4 acquisition occurred in this family between 19.6 and 10.1 Ma. According to analyses of PEPC-encoding genes (ppc), at least five distinct C4 origins are present in sedges. Two C4 Eleocharis species, which were unrelated in the plastid phylogeny, acquired their C4-specific PEPC genes from a single source, probably through reticulate evolution or a horizontal transfer event. Acquisitions of C4 PEPC in sedges have been driven by positive selection on at least 16 codons (3.5% of the studied gene segment). These sites underwent parallel genetic changes across the five sedge C4 origins. Five of these sites underwent identical changes also in grass and eudicot C4 lineages, indicating that genetic convergence is most important within families but that identical genetic changes occurred even among distantly related taxa. These lines of evidence give new insights into the constraints that govern molecular evolution.

Key Words: C4 photosynthesis • convergence • Cyperaceae • molecular dating • phosphoenolpyruvate carboxylase • positive selection


1 Present address: Imperial College London, Silwood Park Campus, Ascot, Berkshire, United Kingdom.

David Irwin, Associate Editor


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