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Four enzymes control natural variation in the steroid core of Erysimum cardenolides.
bioRxiv 2024 April 12
UNLABELLED: Plants commonly produce families of structurally related metabolites with similar defensive functions. This apparent redundancy raises the question of underlying molecular mechanisms and adaptive benefits of such chemical variation. Cardenolides, a class defensive compounds found in the wallflower genus Erysimum (L., Brassicaceae) and scattered across other plant families, show substantial structural variation, with glycosylation and hydroxylation being common modifications of a steroid core, which itself may vary in terms of stereochemistry and saturation. Through a combination of chemical mutagenesis and analysis of gene coexpression networks, we identified four enzymes involved in cardenolide biosynthesis in Erysimum that work together to determine stereochemistry at carbon 5 of the steroid core: Ec3βHSD, a 3β-hydroxysteroid dehydrogenase, Ec3KSI, a ketosteroid isomerase, EcP5βR2, a progesterone 5β-reductase, and EcDET2, a steroid 5α-reductase. We biochemically characterized the activity of these enzymes in vitro and generated CRISPR/Cas9 knockout lines to confirm activity in vivo . Cardenolide biosynthesis was not eliminated in any of the knockouts. Instead, mutant plants accumulated cardenolides with altered saturation and stereochemistry of the steroid core. Furthermore, we found variation in carbon 5 configuration among the cardenolides of 44 species of Erysimum , where the occurrence of some 5β-cardenolides is associated with the expression and sequence of P5βR2. This may have allowed Erysimum species to fine-tune their defensive profiles to target specific herbivore populations over the course of evolution.
SIGNIFICANCE STATEMENT: Plants use an array of toxic compounds to defend themselves from attack against insects and other herbivores. One mechanism through which plants may evolve more toxic compounds is through modifications to the structure of compounds they already produce. In this study, we show how plants in the wallflower genus Erysimum use four enzymes to fine-tune the structure of toxic metabolites called cardenolides. Natural variation in the sequence and expression of a single enzyme called progesterone 5β-reductase 2 partly explains the variation in cardenolides observed across the Erysimum genus. These alterations to cardenolide structure over the course of evolution suggests that there may be context-dependent benefits to Erysimum to invest in one cardenolide variant over another.
SIGNIFICANCE STATEMENT: Plants use an array of toxic compounds to defend themselves from attack against insects and other herbivores. One mechanism through which plants may evolve more toxic compounds is through modifications to the structure of compounds they already produce. In this study, we show how plants in the wallflower genus Erysimum use four enzymes to fine-tune the structure of toxic metabolites called cardenolides. Natural variation in the sequence and expression of a single enzyme called progesterone 5β-reductase 2 partly explains the variation in cardenolides observed across the Erysimum genus. These alterations to cardenolide structure over the course of evolution suggests that there may be context-dependent benefits to Erysimum to invest in one cardenolide variant over another.
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