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, yet surprisingly, flower chemical defenses were rarely investigated. We show here that two clustered terpene synthase and cytochrome P450 encoding genes (TPS11 and CYP706A3) on chromosome 5 of Arabidopsis thaliana are tightly co-expressed in floral tissues, upon anthesis and during floral bud development. TPS11 was previously reported to generate a blend of sesquiterpenes. By heterologous co-expression of TPS11 and CYP706A3 in yeast and Nicotiana benthamiana, we demonstrate that CYP706A3 metabolizes TPS11 products and also further oxidizes its primary oxidation products. Analysis of headspace and soluble metabolites of CYP706A3 insertion and overexpression mutants indicates that CYP706A3-mediated metabolism largely suppresses sesquiterpene and most monoterpene emission from opening flowers, and generates terpene oxides retained in floral tissues. In flower buds, concerted expression of TPS11 and CYP706A3 also suppresses volatile emission and generates soluble sesquiterpene oxides. Florivory assays performed with the Brassicaceae specialist Plutella xylostella demonstrate that insect larvae avoid feeding on bud expressing CYP706A3 and accumulating terpene oxides. In addition, CYP706A3 expression deeply alters composition of the floral microbiome. TPS11 and CYP706A3 co-evolved with Brassicaceae to form the smallest and most versatile functional gene cluster so far described in higher plants.