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MBE Advance Access published online on February 2, 2009
Molecular Biology and Evolution, doi:10.1093/molbev/msp021
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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 Article

The correlation of evolutionary rate with pathway position in plant terpenoid biosynthesis

Heather Ramsay1,2, Loren H. Rieseberg2 and Kermit Ritland1

1 Faculty of Forestry, University of British Columbia, Vancouver, British Columbia, V6T 1Z4 Canada
2 Department of Botany, University of British Columbia, Vancouver, British Columbia, V6T 1Z4 Canada

Corresponding author: H. Ramsay, 6270 University Boulevard, Vancouver, BC, Canada, V6T 1Z4. Phone: 604-827-3535. Fax: 604-822-6089. E-mail: hrhrhr{at}interchange.ubc.ca

Received for publication October 27, 2008. Revision received January 23, 2009. Accepted for publication January 26, 2009.

Genes are expected to face stronger selective constraint and to evolve more slowly if they encode enzymes upstream as opposed to downstream in metabolic pathways, since upstream genes are more pleiotropic, being required for a wider range of end-products. However, few clear examples of this trend in evolutionary rate variation exist. We examined whether genes involved in plant terpenoid biosynthesis exhibit such a pattern, using data for 40 genes from five fully-sequenced angiosperms, Oryza, Vitis, Arabidopsis, Populus and Ricinus. Our results show that dN/dS does in fact correlate with pathway position along pathways converting glucose to the terpenoid phytohormones abscissic acid, gibberellic acid and brassinosteroids. Upstream versus downstream rate variation is particularly strong in the gibberellic acid pathway. In contrast, we found no or little apparent variation in dN/dS with gene copy number. We also introduce a new measure of pathway position, the Pathway Pleiotropy Index (PPI), which counts groups of enzymes between pathway branch points. We found that this measure is superior to pathway position in explaining variation in dN/dS along each pathway. Although at least 8 of the 40 genes showed evidence of positive selection, correlations of dN/dS with PPI remain significant when these genes are removed. Therefore, our results are consistent with the prediction that selective constraint is progressively relaxed along metabolic pathways.

Key Words: terpenoid synthesis • metabolic pathways • nucleotide substitution rates • evolutionary rate variation • positional rate variation • selective constraint


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