A Promiscuous CYP706A3 Reduces Terpene Volatile Emission from Arabidopsis Flowers, Affecting Florivores and the Floral Microbiome

Flowers are essential but vulnerable plant organs, exposed to pollinators and florivores; however, flower chemical defenses are rarely investigated. We show here that two clustered terpene synthase and cytochrome P450 encoding genes ( and ) on chromosome 5 of Arabidopsis () are tightly coexpressed in floral tissues, upon anthesis and during floral bud development. TPS11 was previously reported to generate a blend of sesquiterpenes. By heterologous coexpression of and in yeast () and , we demonstrate that CYP706A3 is active on TPS11 products and also further oxidizes its own primary oxidation products. Analysis of headspace and soluble metabolites in and mutants indicate that CYP706A3-mediated metabolism largely suppresses sesquiterpene and most monoterpene emissions from opening flowers, and generates terpene oxides that are retained in floral tissues. In flower buds, the combined expression of and also suppresses volatile emissions and generates soluble sesquiterpene oxides. Florivory assays with the specialist demonstrate that insect larvae avoid feeding on buds expressing and accumulating terpene oxides. Composition of the floral microbiome appears also to be modulated by expression. and simultaneously evolved within and form the most versatile functional gene cluster described in higher plants so far.plantcell;31/12/2947/FX1F1fx1.