An ancient role for theCYP73gene family int-cinnamic acid 4-hydroxylation, phenylpropanoid biosynthesis and embryophyte development

Abstract

ABSTRACTThe phenylpropanoid pathway is a plant metabolism intimately linked to the transition to terrestrial life. It produces phenolic compounds that play essential roles in stress mitigation and ecological interactions. The pathway also provides the building blocks for hydrophobic polymers that form apoplastic diffusion barriers and make up a significant fraction of the land plant biomass. Despite its significance in embryophytes (i.e., land plants), the origin and evolutionary history of the phenylpropanoid pathway remain poorly understood. In particular, little is known about the organization and function of the pathway in bryophytes, the non-vascular embryophytes. In this study, we conducted a multidisciplinary analysis of theCYP73gene family that encodest-cinnamic acid 4-hydroxylase (C4H), the first plant-specific enzyme in the pathway. Our results indicate that C4H activity originated with the emergence of theCYP73gene family in an ancestor of land plants and was supported by an arginine residue that stabilizes its substrate in the active site. C4H deficiency in the mossPhyscomitrium patens, the liverwortMarchantia polymorphaand the hornwortAnthoceros agrestisresulted in a shortage of phenylpropanoids and abnormal plant development. The latter could be rescued in the moss by the exogenous supply ofp-coumaric acid, the product of C4H. Our findings establish the emergence of theCYP73gene family as a foundational event for the development of the canonical plant phenylpropanoid pathway and underscores the deep-rooted conservation of the C4H enzyme function in embryophyte biology.