Abstract
Comparative genomics analysis unravels lineage-specific bursts of gene duplications related to the emergence of specialized pathways. The CYP76C subfamily of cytochrome P450 enzymes is specific to Brassicaceae. Two of its members were recently associated with monoterpenol metabolism. This prompted us to investigate the CYP76C subfamily genetic and functional diversification. Our study revealed high rates of CYP76C gene duplication and loss in Brassicaceae, suggesting the association of the CYP76C subfamily with species-specific adaptive functions. Gene differential expression and enzyme functional specialization in Arabidopsis thaliana, including metabolism of different monoterpenols and formation of different products, support this hypothesis. In addition to linalool metabolism, CYP76C1, CYP76C2, and CYP76C4 metabolized herbicides belonging to the class of phenylurea. Their ectopic expression in the whole plant conferred herbicide tolerance. CYP76Cs from A. thaliana. thus provide a first example of promiscuous cytochrome P450 enzymes endowing effective metabolism of both natural and xenobiotic compounds. Our data also suggest that the CYP76C gene family provides a suitable genetic background for a quick evolution of herbicide resistance.
Highlights
Comparative genomics analysis unravels lineage-specific bursts of gene duplications related to the emergence of specialized pathways
Eight CYP76 genes have been annotated in the A. thaliana genome
One member belongs to the CYP76G subfamily (CYP76G1), and the seven others fall into the CYP76C subfamily
Summary
Comparative genomics analysis unravels lineage-specific bursts of gene duplications related to the emergence of specialized pathways. Two of its members were recently associated with monoterpenol metabolism This prompted us to investigate the CYP76C subfamily genetic and functional diversification. Our study revealed high rates of CYP76C gene duplication and loss in Brassicaceae, suggesting the association of the CYP76C subfamily with species-specific adaptive functions. Extensive monoterpenol (especially linalool) oxidative metabolism has been described in many plant species, leading to fragrant and bioactive compounds as diverse as alcohols, aldehydes, acids, and epoxides (Williams et al, 1982; Matich et al, 2003, 2011; Luan et al, 2005, 2006; Ginglinger et al, 2013), pyranoid or furanoid linalool derivatives (Pichersky et al, 1994; Raguso and Pichersky, 1999), and geraniol-derived iridoids and secoiridoids (Dinda et al, 2007a, 2007b, 2011; Tundis et al, 2008), limited information is available on the enzymes generating these oxygenated compounds. The geraniol 8-hydroxylase (often named geraniol 10-hydroxylase) CYP76B6, involved in the biosynthesis of secoiridoids and monoterpene indole alkaloid anticancer
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