De novo formation of an aggregation pheromone precursor by an isoprenyl diphosphate synthase-related terpene synthase in the harlequin bug

Lancaster, Jason; Khrimian, Ashot; Young, Sharon M.; Lehner, Bryan; Luck, Katrin; Wallingford, Anna; Ghosh, Saikat; Zerbe, Philipp; Muchlinski, Andrew; Marek, Paul E.; Sparks, Michael E.; Tokuhisa, James G.; Tittiger, Claus; Köllner, Tobias G.; Weber, Donald C.; Gundersen‐Rindal, Dawn E.; Kuhar, Thomas P.; Tholl, Dorothea

doi:10.1073/pnas.1800008115

Cited by 53 publications

(88 citation statements)

References 58 publications

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“…Recently, insect TPSs from a stink bug and a beetle species have been characterized. These enzymes produce different monocyclic, bisabolene-like isoprenoids from (E,E)-FPP (22,23). Experimental evidence is very strong because of a combination of heterologous expression and knockdown studies.…”

Section: Terpenesmentioning

confidence: 99%

The biosynthetic diversity of the animal world

Torres

Schmidt

2019

Journal of Biological Chemistry

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Secondary metabolites are often considered within the remit of bacterial or plant research, but animals also contain a plethora of these molecules with important functional roles. Classical feeding studies demonstrate that, whereas some are derived from diet, many of these compounds are made within the animals. In the past 15 years, the genetic and biochemical origin of several animal natural products has been traced to partnerships with symbiotic bacteria. More recently, a number of animal genome-encoded pathways to microbe-like natural products have come to light. These pathways are sometimes horizontally acquired from bacteria, but more commonly they unveil a new and diverse animal biochemistry. In this review, we highlight recent examples of characterized animal biosynthetic enzymes that reveal an unanticipated breadth and intricacy in animal secondary metabolism. The results so far suggest that there may be an immense diversity of animal small molecules and biosynthetic enzymes awaiting discovery. This biosynthetic dark matter is just beginning to be understood, providing a relatively untapped frontier for discovery.

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Section: Terpenesmentioning

confidence: 99%

The biosynthetic diversity of the animal world

Torres

Schmidt

2019

Journal of Biological Chemistry

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“…In previous structural studies, the arginine in a bacterial FDPS in the equivalent position of R81 was hypothesized to be involved in forming a salt bridge to interact with IDP pyrophosphate 41 . It is also interesting to note that when the "KKxR" motif in MhFDPS, a FDS from the insect M. histrionica, were substituted with a SDAW motif found in MhTPS, a FDS-like terpene synthase, the MhFDPS mutant lost the IDS activity 17 . The arginine in "KKxR" of MhFDPS is in the equivalent positon of R81.…”

Section: Discussionmentioning

confidence: 99%

“…5 ). It is interestingly to note that while ILTPSs from Melampsora evolved from geranylgeranyl diphosphate synthase (GGDPS), several IDS-like terpene synthases identified from insects were derived from farnesyl diphosphate synthase (FDPS) 17 – 19 . This indicates not only an independent occurrence of the evolution of terpene synthases from IDSs in distantly related lineages but also distinct paths in which different types of IDSs served as progenitors.…”

Section: Discussionmentioning

confidence: 99%

“…Some organisms do not contain TPS genes but are known to use terpenoids for adaptive functions, raising the question whether they are synthesized by novel, non-classic TPS genes. Another direct evidence to support this hypothesis comes from the studies on terpenoid pheromones in a number of insect species, in which the precursors of terpenoid pheromones were demonstrated to be synthesized by IDS-like enzymes belonging to the farnesyl diphosphate synthase (FDPS) family [17][18][19][20] . It is notable that insects do not contain classic TPS genes.…”

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confidence: 99%

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Evolution of isoprenyl diphosphate synthase-like terpene synthases in fungi

Guo

Eberl

Chen

et al. 2020

Sci Rep

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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.

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“…Similar to these findings, insects are now emerging as a rich source of IDS that carry out atypical reactions. Four trans-IDS from the flea beetle Phyllotreta striolata and one trans-IDS each from the harlequin bug Murgantia histrionica or Southern green stink bug Nezara viridula were shown not to catalyze prenyl elongation steps at all, but to be bona fide TPS (Beran et al 2016;Lancaster et al 2018a;Lancaster et al 2018b). P. striolata also has an unusually high number of IDS and IDS-like enzymes in its genome and another trans-IDS was shown to produce the cisoid products neryl diphosphate from IDP and DMADP and (Z,E)-FDP from (E)-GDP and IDP, making it the first trans-IDS to yield cisoid products (Beran et al 2016) (Figure 2).…”

Section: Ids Catalyzing Alternate Reactionsmentioning

confidence: 99%

Isoprenyl diphosphate synthases: the chain length determining step in terpene biosynthesis

Nagel

Schmidt

Peters

2018

Planta

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Main Conclusion This review summarizes the recent developments in the study of isoprenyl diphosphate synthases with an emphasis on analytical techniques, product length determination, and the physiological consequences of manipulating expression in planta. The highly diverse structures of all terpenes are synthesized from the five carbon precursors dimethylallyl diphosphate and a varying number of isopentenyl diphosphate units through 1'-4 alkylation reactions. These elongation reactions are catalyzed by isoprenyl diphosphate synthases (IDS). IDS are classified depending on the configuration of the ensuing double bond as transand cis-IDS. In addition, IDS are further stratified by the length of their prenyl diphosphate product. This review discusses analytical techniques for the determination of product length and the factors that control product length, with an emphasis on alternative mechanisms. With recent advances in analytics, multiple IDS of Arabidopsis thaliana have been recently reinvestigated and demonstrated to yield products of different lengths than originally reported, which is summarized here. As IDS dictate prenyl diphosphate length and thereby which class of terpenes is ultimately produced, another focus of this review is the impact that altering IDS expression has on terpenoid natural product accumulation. Finally, recent findings regarding the ability of a few IDS to not catalyze 1'-4 alkylation reactions, but instead produce irregular products, with unusual connectivity, or act as terpene synthases, are also discussed.

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De novo formation of an aggregation pheromone precursor by an isoprenyl diphosphate synthase-related terpene synthase in the harlequin bug

Cited by 53 publications

References 58 publications

The biosynthetic diversity of the animal world

The biosynthetic diversity of the animal world

Evolution of isoprenyl diphosphate synthase-like terpene synthases in fungi

Isoprenyl diphosphate synthases: the chain length determining step in terpene biosynthesis

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