Terpene synthases (TPSs) and trans-isoprenyl diphosphate synthases (IDSs) are among the core enzymes for creating the enormous diversity of terpenoids. Despite having no sequence homology, TPSs and IDSs share a conserved “α terpenoid synthase fold” and a trinuclear metal cluster for catalysis, implying a common ancestry with TPSs hypothesized to evolve from IDSs anciently. Here we report on the identification and functional characterization of novel IDS-like TPSs (ILTPSs) in fungi that evolved from IDS relatively recently, indicating recurrent evolution of TPSs from IDSs. Through large-scale bioinformatic analyses of fungal IDSs, putative ILTPSs that belong to the geranylgeranyl diphosphate synthase (GGDPS) family of IDSs were identified in three species of Melampsora. Among the GGDPS family of the two Melampsora species experimentally characterized, one enzyme was verified to be bona fide GGDPS and all others were demonstrated to function as TPSs. Melampsora ILTPSs displayed kinetic parameters similar to those of classic TPSs. Key residues underlying the determination of GGDPS versus ILTPS activity and functional divergence of ILTPSs were identified. Phylogenetic analysis implies a recent origination of these ILTPSs from a GGDPS progenitor in fungi, after the split of Melampsora from other genera within the class of Pucciniomycetes. For the poplar leaf rust fungus Melampsora larici-populina, the transcripts of its ILTPS genes were detected in infected poplar leaves, suggesting possible involvement of these recently evolved ILTPS genes in the infection process. This study reveals the recurrent evolution of TPSs from IDSs since their ancient occurrence and points to the possibility of a wide distribution of ILTPS genes in three domains of life.
Gibberellins (GAs) are a major class of plant hormones that regulates diverse developmental programs. Both acquiring abilities to synthesize GAs and evolving divergent GA receptors have been demonstrated to play critical roles in the evolution of land plants. In contrast, little is understood regarding the role of GA‐inactivating mechanisms in plant evolution. Here we report on the origin and evolution of GA methyltransferases (GAMTs), enzymes that deactivate GAs by converting bioactive GAs to inactive GA methylesters. Prior to this study, GAMT genes, which belong to the SABATH family, were known only from Arabidopsis . Through systematic searches for SABATH genes in the genomes of 260 sequenced land plants and phylogenetic analyses, we have identified a putative GAMT clade specific to seed plants. We have further demonstrated that both gymnosperm and angiosperm representatives of this clade encode active methyltransferases for GA methylation, indicating that they are functional orthologs of GAMT . In seven selected seed plants, GAMT genes were mainly expressed in flowers and/or seeds, indicating a conserved biological role in reproduction. GAMT genes are represented by a single copy in most species, if present, but multiple copies mainly produced by whole genome duplications have been retained in Brassicaceae. Surprisingly, more than 2/3 of the 248 flowering plants examined here lack GAMT genes, including all species of Poales (e.g., grasses), Fabales (legumes), and the large Superasterid clade of eudicots. With these observations, we discuss the significance of GAMT origination, functional conservation and diversification, and frequent loss during the evolution of flowering plants.
The ‘biogenetic isoprene rule’, formulated in the mid 20th century, predicted that terpenoids are biosynthesized via polymerization of C5 isoprene units. The polymerizing enzymes have been identified to be isoprenyl diphosphate synthases, products of which are catalyzed by terpene synthases (TPSs) to achieve vast structural diversity of terpene skeletons. Irregular terpenes (e.g, C11, C12, C16, C17) are also frequently observed, and they have presumed to be synthesized by the modification of terpene skeletons. This review highlights the exciting discovery of an additional route to the biosynthesis of irregular terpenes which involves the action of a newly discovered enzyme family of isoprenyl diphosphate methyltransferases (IDMTs). These enzymes methylate, and sometimes cyclize, the classical isoprenyl diphosphate substrates to produce modified, non-canonical substrates for specifically evolved TPSs. So far, this new pathway has been found only in bacteria. Structure and sequence comparisons of the IDMTs strongly indicate a conservation of their active pockets and overall topologies. Some bacterial IDMTs and TPSs appear in small gene clusters, which may facilitate future mining of bacterial genomes for identification of irregular terpene-producing enzymes. The IDMT-TPS route for terpenoid biosynthesis presents another example of nature's ingenuity in creating chemical diversity, particularly terpenoids, for organismal fitness. IDMT isoprenyl diphosphate methyltransferases IDPMT isopentenyl diphosphate methyltransferase GDPMT geranyl diphosphate methyltransferase FDPMT farnesyl diphosphate methyltransferases BGC biosynthetic gene cluster TPS terpene synthase MIBS 2-methylisoborneol synthase MBS 2-methylenebornane synthase DMADP Dimethylallyl diphosphate SAM S-adenosyl-L-methionine
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