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Genome Biology and Evolution Advance Access originally published online on July 20, 2009
Genome Biology and Evolution (2009) Vol. 2009:221; doi:10.1093/gbe/evp020 published on August 13, 2009
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© 2009 The Authors
This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/2.0/uk/) which permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited.

Evolutionary Insights on C4 Photosynthetic Subtypes in Grasses from Genomics and Phylogenetics

Pascal-Antoine Christin*, Emanuela Samaritani*,1, Blaise Petitpierre*, Nicolas Salamin*,{dagger} and Guillaume Besnard*,2

* Department of Ecology and Evolution, Biophore, University of Lausanne, Lausanne, Switzerland
{dagger} Swiss Institute of Bioinformatics, Génopode, Quartier-Sorge, 1015 Lausanne, Switzerland

E-mail: Pascal-Antoine.Christin{at}unil.ch.


   Abstract

In plants, an oligogene family encodes NADP-malic enzymes (NADP-me), which are responsible for various functions and exhibit different kinetics and expression patterns. In particular, a chloroplast isoform of NADP-me plays a key role in one of the three biochemical subtypes of C4 photosynthesis, an adaptation to warm environments that evolved several times independently during angiosperm diversification. By combining genomic and phylogenetic approaches, this study aimed at identifying the molecular mechanisms linked to the recurrent evolutions of C4-specific NADP-me in grasses (Poaceae). Genes encoding NADP-me (nadpme) were retrieved from genomes of model grasses and isolated from a large sample of C3 and C4 grasses. Genomic and phylogenetic analyses showed that 1) the grass nadpme gene family is composed of four main lineages, one of which is expressed in plastids (nadpme-IV), 2) C4-specific NADP-me evolved at least five times independently from nadpme-IV, and 3) some codons driven by positive selection underwent parallel changes during the multiple C4 origins. The C4 NADP-me being expressed in chloroplasts probably constrained its recurrent evolutions from the only plastid nadpme lineage and this common starting point limited the number of evolutionary paths toward a C4 optimized enzyme, resulting in genetic convergence. In light of the history of nadpme genes, an evolutionary scenario of the C4 phenotype using NADP-me is discussed.

Keywords: gene duplication, molecular convergence, evolutionary constraint, genetic adaptation, multiple origins

Accepted July 15, 2009


1 Present address: WSL, Wetlands Research Group, Station 2, 1015 Lausanne, Switzerland.

2 Imperial College, Silwood Park Campus, Buckhurst Road, Ascot, Berkshire SL5 7PY, UK.

William Martin, Associate Editor


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