Genomic Organization of Plant Terpene Synthases and Molecular Evolutionary Implications

TLDR

Terpenoids, the largest and most diverse class of plant natural products, are synthesized via prenyl diphosphate precursors by monoterpene, sesquiterpene, and diterpene synthases, and over 30 related cDNAs have been cloned and characterized. The study isolates and analyzes six genomic clones of terpene synthases from conifers and Taxus brevifolia to investigate their roles in natural product biosynthesis. The authors compared intron and exon organization of the six gymnosperm terpene synthase genes with eight angiosperm genes and six Arabidopsis sequences to assess genome structure differences. The analysis revealed three terpene synthase gene classes, indicating sequential intron loss from an ancestral conifer-like gene, and supports a model where the superfamily evolved from primary metabolism genes through duplication and divergence, with broad implications for natural product origins and plant phylogenetics.

Abstract

Abstract Terpenoids are the largest, most diverse class of plant natural products and they play numerous functional roles in primary metabolism and in ecological interactions. The first committed step in the formation of the various terpenoid classes is the transformation of the prenyl diphosphate precursors, geranyl diphosphate, farnesyl diphosphate, and geranylgeranyl diphosphate, to the parent structures of each type catalyzed by the respective monoterpene (C10), sesquiterpene (C15), and diterpene synthases (C20). Over 30 cDNAs encoding plant terpenoid synthases involved in primary and secondary metabolism have been cloned and characterized. Here we describe the isolation and analysis of six genomic clones encoding terpene synthases of conifers, [(-)-pinene (C10), (-)-limonene (C10), (E)-α-bisabolene (C15), δ-selinene (C15), and abietadiene synthase (C20) from Abies grandis and taxadiene synthase (C20) from Taxus brevifolia], all of which are involved in natural products biosynthesis. Genome organization (intron number, size, placement and phase, and exon size) of these gymnosperm terpene synthases was compared to eight previously characterized angiosperm terpene synthase genes and to six putative terpene synthase genomic sequences from Arabidopsis thaliana. Three distinct classes of terpene synthase genes were discerned, from which assumed patterns of sequential intron loss and the loss of an unusual internal sequence element suggest that the ancestral terpenoid synthase gene resembled a contemporary conifer diterpene synthase gene in containing at least 12 introns and 13 exons of conserved size. A model presented for the evolutionary history of plant terpene synthases suggests that this superfamily of genes responsible for natural products biosynthesis derived from terpene synthase genes involved in primary metabolism by duplication and divergence in structural and functional specialization. This novel molecular evolutionary approach focused on genes of secondary metabolism may have broad implications for the origins of natural products and for plant phylogenetics in general.