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Terpene Synthases as Metabolic Gatekeepers in the Evolution of Plant Terpenoid Chemical Diversity.

ABSTRACT: Terpenoids comprise tens of thousands of small molecule natural products that are widely distributed across all domains of life. Plants produce by far the largest array of terpenoids with various roles in development and chemical ecology. Driven by selective pressure to adapt to their specific ecological niche, individual species form only a fraction of the myriad plant terpenoids, typically representing unique metabolite blends. Terpene synthase (TPS) enzymes are the gatekeepers in generating terpenoid diversity by catalyzing complex carbocation-driven cyclization, rearrangement, and elimination reactions that enable the transformation of a few acyclic prenyl diphosphate substrates into a vast chemical library of hydrocarbon and, for a few enzymes, oxygenated terpene scaffolds. The seven currently defined clades (a-h) forming the plant TPS family evolved from ancestral triterpene synthase- and prenyl transferase-type enzymes through repeated events of gene duplication and subsequent loss, gain, or fusion of protein domains and further functional diversification. Lineage-specific expansion of these TPS clades led to variable family sizes that may range from a single TPS gene to families of more than 100 members that may further function as part of modular metabolic networks to maximize the number of possible products. Accompanying gene family expansion, the TPS family shows a profound functional plasticity, where minor active site alterations can dramatically impact product outcome, thus enabling the emergence of new functions with minimal investment in evolving new enzymes. This article reviews current knowledge on the functional diversity and molecular evolution of the plant TPS family that underlies the chemical diversity of bioactive terpenoids across the plant kingdom.

SUBMITTER: Karunanithi PS

PROVIDER: S-EPMC6779861 | biostudies-literature | 2019

REPOSITORIES: biostudies-literature

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Terpene Synthases as Metabolic Gatekeepers in the Evolution of Plant Terpenoid Chemical Diversity.

Karunanithi Prema S PS Zerbe Philipp P

Frontiers in plant science 20191001

Terpenoids comprise tens of thousands of small molecule natural products that are widely distributed across all domains of life. Plants produce by far the largest array of terpenoids with various roles in development and chemical ecology. Driven by selective pressure to adapt to their specific ecological niche, individual species form only a fraction of the myriad plant terpenoids, typically representing unique metabolite blends. Terpene synthase (TPS) enzymes are the gatekeepers in generating t ...[more]

PMID: 31632418

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Project description:Terpenes are organic compounds and play important roles in plant development and stress response. Terpene synthases (TPSs) are the key enzymes for the biosynthesis of terpenes. For Rosaceae species, terpene composition represents a critical quality attribute, but limited information is available regarding the evolution and expansion occurring in the terpene synthases gene family. Here, we selected eight Rosaceae species with sequenced and annotated genomes for the identification of TPSs, including three Prunoideae, three Maloideae, and two Rosoideae species. Our data showed that the TPS gene family in the Rosaceae species displayed a diversity of family numbers and functions among different subfamilies. Lineage and species-specific expansion of the TPSs accompanied by frequent domain loss was widely observed within different TPS clades, which might have contributed to speciation or environmental adaptation in Rosaceae. In contrast to Maloideae and Rosoideae species, Prunoideae species owned less TPSs, with the evolution of Prunoideae species, TPSs were expanded in modern peach. Both tandem and segmental duplication significantly contributed to TPSs expansion. Ka/Ks calculations revealed that TPSs genes mainly evolved under purifying selection except for several pairs, where the divergent time indicated TPS-e clade was diverged relatively anciently. Gene function classification of TPSs further demonstrated the function diversity among clades and species. Moreover, based on already published RNA-Seq data from NCBI, the expression of most TPSs in Malus domestica, Prunus persica, and Fragaria vesca displayed tissue specificity and distinct expression patterns either in tissues or expression abundance between species and TPS clades. Certain putative TPS-like proteins lacking both domains were detected to be highly expressed, indicating the underlying functional or regulatory potentials. The result provided insight into the TPS family evolution and genetic information that would help to improve Rosaceae species quality.

Dataset Information

Terpene Synthases as Metabolic Gatekeepers in the Evolution of Plant Terpenoid Chemical Diversity.

Publications

Terpene Synthases as Metabolic Gatekeepers in the Evolution of Plant Terpenoid Chemical Diversity.

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