Evolutionary interplay between sister cytochrome P450 genes shapes plasticity in plant metabolism.

Zhenhua Liu,Raquel Tavares,Evan S Forsythe,Hugues Renault,Danièle Werck-Reichhart,Stéphanie Boutet-Mercey,Gabriella Jonasson,François André,Takayuki Tohge,Mark A Beilstein,Raphaël Lugan

doi:10.1038/ncomms13026

Abstract

Expansion of the cytochrome P450 gene family is often proposed to have a critical role in the evolution of metabolic complexity, in particular in microorganisms, insects and plants. However, the molecular mechanisms underlying the evolution of this complexity are poorly understood. Here we describe the evolutionary history of a plant P450 retrogene, which emerged and underwent fixation in the common ancestor of Brassicales, before undergoing tandem duplication in the ancestor of Brassicaceae. Duplication leads first to gain of dual functions in one of the copies. Both sister genes are retained through subsequent speciation but eventually return to a single copy in two of three diverging lineages. In the lineage in which both copies are maintained, the ancestral functions are split between paralogs and a novel function arises in the copy under relaxed selection. Our work illustrates how retrotransposition and gene duplication can favour the emergence of novel metabolic functions.

Highlights

HAL is a multi-disciplinary open access archive for the deposit and dissemination of scientific research documents, whether they are published or not
A few lineage-specific duplications are inferred in phylogenies of CYP98A3 across land plants. One such duplication occurred via transposition within Brassicales and was followed by a tandem duplication giving rise to CYP98A8 and CYP98A9 genes leading to the formation of N1,N5-di(hydroxyferuloyl)-N10-sinapoyl-spermidine, a major pollen coat and wall constituent in A. thaliana[18,22]
We demonstrate that the fate and function of the resulting paralogs differ between the Brassicaceae lineages, with either loss of one of the paralogs, the other maintaining a dual function in lineage II and III, or conservation of the two gene copies in lineage I, with subfunctionalization and gain of an additional activity in flavonoid metabolism by one of the duplicates

Summary

Introduction

HAL is a multi-disciplinary open access archive for the deposit and dissemination of scientific research documents, whether they are published or not. The parent gene, represented by CYP98A3 in Arabidopsis thaliana (family Brassicaceae, order Brassicales), controls a major branch point in the plant phenolic pathway[19,20]. It is broadly expressed in plants, especially in vascular tissues, and encodes the phenolic ring meta-hydroxylase of lignin precursors. A few lineage-specific duplications are inferred in phylogenies of CYP98A3 across land plants One such duplication occurred via transposition within Brassicales and was followed by a tandem duplication giving rise to CYP98A8 and CYP98A9 genes leading to the formation of N1,N5-di(hydroxyferuloyl)-N10-sinapoyl-spermidine, a major pollen coat and wall constituent in A. thaliana[18,22]. The recent emergence of this pathway and the sequencing of a representative set of Brassicales genomes offers the opportunity to determine the evolutionary process leading to these new P450 functions

Methods

Results

Conclusion