Abstract
BackgroundSelection of genes involved in metabolic pathways could target them differently depending on the position of genes in the pathway and on their role in controlling metabolic fluxes. This hypothesis was tested in the carotenoid biosynthesis pathway using population genetics and phylogenetics.Methodology/Principal FindingsEvolutionary rates of seven genes distributed along the carotenoid biosynthesis pathway, IPI, PDS, CRTISO, LCYB, LCYE, CHXE and ZEP, were compared in seven dicot taxa. A survey of deviations from neutrality expectations at these genes was also undertaken in cultivated carrot (Daucus carota subsp. sativus), a species that has been intensely bred for carotenoid pattern diversification in its root during its cultivation history. Parts of sequences of these genes were obtained from 46 individuals representing a wide diversity of cultivated carrots. Downstream genes exhibited higher deviations from neutral expectations than upstream genes. Comparisons of synonymous and nonsynonymous substitution rates between genes among dicots revealed greater constraints on upstream genes than on downstream genes. An excess of intermediate frequency polymorphisms, high nucleotide diversity and/or high differentiation of CRTISO, LCYB1 and LCYE in cultivated carrot suggest that balancing selection may have targeted genes acting centrally in the pathway.Conclusions/SignificanceOur results are consistent with relaxed constraints on downstream genes and selection targeting the central enzymes of the carotenoid biosynthesis pathway during carrot breeding history.
Highlights
One of the most important objectives of molecular evolution studies is to understand which factors influence genetic variations in the genome
This study aimed at testing a first hypothesis: downstream genes in the carotenoid biosynthesis pathway are less constrained than upstream genes
The second hypothesis we examined is that the selection on carotenoid biosynthesis genes is most pronounced at pathway nodes
Summary
One of the most important objectives of molecular evolution studies is to understand which factors influence genetic variations in the genome. Understanding how selection acts on genes involved in pathways or networks has received increasing attention in the study of molecular evolution in recent years [1,2]. Two key factors were shown to be of particular relevance for explaining the evolution of metabolic pathways: node connectivity and the position of the gene in the pathway or network. Selection of genes involved in metabolic pathways could target them differently depending on the position of genes in the pathway and on their role in controlling metabolic fluxes. This hypothesis was tested in the carotenoid biosynthesis pathway using population genetics and phylogenetics
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