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Open Access Highly Accessed Research article

Molecular evolution accompanying functional divergence of duplicated genes along the plant starch biosynthesis pathway

Odrade Nougué123, Jonathan Corbi4, Steven G Ball5, Domenica Manicacci3* and Maud I Tenaillon26

Author Affiliations

1 Department of Evolutionary Ecology, CEFE-CNRS, UMR 5175, F-34293 Montpellier, Cedex 5, France

2 Department of Ecology and Evolutionary Biology, U.C. Irvine, Irvine, California, USA

3 University Paris-Sud, UMR 0320/UMR 8120 Génétique Végétale, Ferme du Moulon, F-91190 Gif-sur-Yvette, France

4 Department of Plant Biology, University of Georgia, Athens, Georgia, USA

5 Laboratoire de Glycobiologie Structurale et Fonctionnelle, UMR 8576, Université des Sciences et Technologies de Lille, F-59655 Villeneuve d’Ascq, Cedex, France

6 CNRS, UMR 0320/UMR 8120 Génétique Végétale, Ferme du Moulon, F-91109 Gif-sur-Yvette, France

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BMC Evolutionary Biology 2014, 14:103  doi:10.1186/1471-2148-14-103

Published: 15 May 2014

Abstract

Background

Starch is the main source of carbon storage in the Archaeplastida. The Starch Biosynthesis Pathway (SBP) emerged from cytosolic glycogen metabolism shortly after plastid endosymbiosis and was redirected to the plastid stroma during the green lineage divergence. The SBP is a complex network of genes, most of which are members of large multigene families. While some gene duplications occurred in the Archaeplastida ancestor, most were generated during the SBP redirection process, and the remaining few paralogs were generated through compartmentalization or tissue specialization during the evolution of the land plants. In the present study, we tested models of duplicated gene evolution in order to understand the evolutionary forces that have led to the development of SBP in angiosperms. We combined phylogenetic analyses and tests on the rates of evolution along branches emerging from major duplication events in six gene families encoding SBP enzymes.

Results

We found evidence of positive selection along branches following cytosolic or plastidial specialization in two starch phosphorylases and identified numerous residues that exhibited changes in volume, polarity or charge. Starch synthases, branching and debranching enzymes functional specializations were also accompanied by accelerated evolution. However, none of the sites targeted by selection corresponded to known functional domains, catalytic or regulatory. Interestingly, among the 13 duplications tested, 7 exhibited evidence of positive selection in both branches emerging from the duplication, 2 in only one branch, and 4 in none of the branches.

Conclusions

The majority of duplications were followed by accelerated evolution targeting specific residues along both branches. This pattern was consistent with the optimization of the two sub-functions originally fulfilled by the ancestral gene before duplication. Our results thereby provide strong support to the so-called “Escape from Adaptive Conflict” (EAC) model. Because none of the residues targeted by selection occurred in characterized functional domains, we propose that enzyme specialization has occurred through subtle changes in affinity, activity or interaction with other enzymes in complex formation, while the basic function defined by the catalytic domain has been maintained.

Keywords:
Starch enzymes; Angiosperms; Positive selection; Paralogous genes; Escape from Adaptive Conflict model; Protein sequence evolution; PAML