Scent biosynthesis and emission in rose flowers: an historical perspective highlighting recent advances in VOC biosynthesis and regulation

Abstract

Among the traits that define the appeal of rose flowers, fragrance, which results from complex blends of volatile organic compounds (VOCs) holds a central cultural, sensory and economic role. These VOCs mainly include terpenoids, phenylpropanoid/benzenoid derivatives, phenolic methyl ethers and norisoprenoids, with strong variation among species and cultivars. In this review, we provide a broad, near-comprehensive and chronological synthesis of research on biosynthesis, regulation and emission of rose VOCs, with particular attention to the experimental approaches that have shaped the field, from classical biochemical and molecular studies to recent advances enabled by metabolic analyses, genomic resources and functional genomics. These developments have recently enabled to decipher major pathways leading to rose VOCs and highlighted the contribution of gene duplication, enzyme diversification and natural variation to scent diversity. Recent findings have been especially important for terpenoids. These includes the discovery of original cytosolic terpene biosynthetic pathways involving both terpene synthase-dependent and terpene synthase-independent routes, the cytosolic origin of the geraniol precursor GPP, the enzymatic conversion of geraniol to β-citronellol and the characterization of numerous terpene synthases involved in the production of major terpenes produced by rose flowers. We also discuss advances in the regulation of VOC biosynthesis, together with emerging questions regarding tissue specialization, intracellular trafficking, transport and emission of scent compounds. By integrating historical discoveries with recent findings, this review outlines how rose scent biology has been reshaped and discuss remaining challenges for understanding, breeding and engineering desirable floral fragrances.