Iridoid Sex Pheromone Biosynthesis in Aphids Mimics Iridoid‐Producing Plants

Partridge, Suzanne J.; Withall, David M.; Caulfield, John C.; Pickett, John A.; Stockman, Robert A.; Oldham, Neil J.; Birkett, Michael A.

doi:10.1002/chem.202001356

Cited by 9 publications

(5 citation statements)

References 18 publications

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“…Here we elucidated the entire iridoid pathway in the pea aphid A. pisum . Previously reported feeding studies in pea aphids (21), as well as the spatial localization of nepetalactone biosynthesis (20), guided the identification of the six biosynthetic genes (Figure 1A). The characterization of these enzymes indicates that the plant and aphid nepetalactone biosynthetic pathways are composed of the same chemical transformations.…”

Section: Discussionmentioning

confidence: 87%

“…Notably, among these transcripts were eight genes encoding the entire mevalonate pathway starting from acetyl-CoA to IPP and DMAPP (Figure 1B). Previously reported isotopic labeling studies indicated that the iridoid pathways in pea aphids and plants share at least some of the same biosynthetic intermediates (21). We therefore assumed that the biochemical transformations in pea aphids were the same as those established in Nepeta .…”

Section: Resultsmentioning

confidence: 99%

“…The pea aphid Acyrthosiphon pisum, for example, has been reported to biosynthesize (1R,4aS,7S,7aR)-cis-trans-nepetalactol and (4aS,7S,7aR)-cis-trans-nepetalactone in glandular structures on the hind legs of sexual female aphids, from where they are released to attract male conspecifics (18,20). Recent studies with isotopically-labeled iridoid precursors suggest that the iridoid pathway in aphids follows the reaction sequence described for plants (21). However, the underlying enzymatic machinery of this pathway is completely unknown.…”

Section: Introductionmentioning

confidence: 99%

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Biosynthesis of iridoid sex pheromones in aphids

Köllner

David

Luck

et al. 2022

Preprint

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Iridoid monoterpenes, widely distributed in plants and insects, have many ecological functions. While the biosynthesis of iridoids has been extensively studied in plants, little is known about how insects synthesize these natural products. Here, we elucidated the biosynthesis of the iridoids cis-trans-nepetalactol and cis-trans-nepetalactone in the pea aphid Acyrthosiphon pisum [Harris], where they act as sex pheromones. The exclusive production of iridoids in hind legs of sexual female aphids allowed us to identify iridoid genes by searching for genes specifically expressed in this tissue. Biochemical characterization of candidate enzymes revealed that the iridoid pathway in aphids proceeds through the same sequence of intermediates as described for plants. The six identified aphid enzymes are unrelated to their counterparts in plants, conclusively demonstrating an independent evolution of the entire iridoid pathway in plants and insects. In contrast to the plant pathway, at least three of the aphid iridoid enzymes are likely membrane-bound. We demonstrated that a lipid environment facilitates the cyclization of a reactive enol intermediate to the iridoid cyclopentanoid-pyran scaffold in vitro, suggesting that membranes are an essential component of the aphid iridoid pathway. Altogether, our discovery of this complex insect metabolic pathway establishes the genetic and biochemical basis for the formation of iridoid sex pheromones in aphids and this discovery also serves as a foundation for understanding the convergent evolution of complex metabolic pathways between kingdoms.

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Section: Discussionmentioning

confidence: 87%

Section: Resultsmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Biosynthesis of iridoid sex pheromones in aphids

Köllner

David

Luck

et al. 2022

Preprint

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“…Recently, the biosynthetic pathways to nepetalactone in both Nepeta spp. (Lichman et al, 2019(Lichman et al, , 2020 and aphids (K€ ollner et al, 2022;Partridge et al, 2021) have been elucidated. In a remarkable example of convergent evolution, the chemical steps are identical but the enzymes are of distinct origins.…”

Section: Introductionmentioning

confidence: 99%

The genomic and enzymatic basis for iridoid biosynthesis in cat thyme (Teucrium marum)

Smit,

Ayten,

Radzikowska

et al. 2024

The Plant Journal

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SUMMARYIridoids are non‐canonical monoterpenoids produced by both insects and plants. An example is the cat‐attracting and insect‐repelling volatile iridoid nepetalactone, produced by Nepeta sp. (catmint) and aphids. Recently, both nepetalactone biosynthetic pathways were elucidated, showing a remarkable convergent evolution. The iridoid, dolichodial, produced by Teucrium marum (cat thyme) and multiple insect species, has highly similar properties to nepetalactone but its biosynthetic origin remains unknown. We set out to determine the genomic, enzymatic, and evolutionary basis of iridoid biosynthesis in T. marum. First, we generated a de novo chromosome‐scale genome assembly for T. marum using Oxford Nanopore Technologies long reads and proximity‐by‐ligation Hi‐C reads. The 610.3 Mb assembly spans 15 pseudomolecules with a 32.9 Mb N50 scaffold size. This enabled identification of iridoid biosynthetic genes, whose roles were verified via activity assays. Phylogenomic analysis revealed that the evolutionary history of T. marum iridoid synthase, the iridoid scaffold‐forming enzyme, is not orthologous to typical iridoid synthases but is derived from its conserved paralog. We discovered an enzymatic route from nepetalactol to diverse iridoids through the coupled activity of an iridoid oxidase cytochrome P450 and acetyltransferases, via an inferred acylated intermediate. This work provides a genomic resource for specialized metabolite research in mints and demonstration of the role of acetylation in T. marum iridoid diversity. This work will enable future biocatalytic or biosynthetic production of potent insect repellents, as well as comparative studies into iridoid biosynthesis in insects.

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“…The iridoid pathway involves the catalysis of geranyl diphosphate by geranyl diphosphate diphosphatase (GES) to produce geraniol [ 5 ]. Subsequently, geraniol is catalyzed by geraniol 10-hydroxylase (G8H) and 8-hydroxygeraniol dehydrogenase (8HGO) to form 10-Oxogeranial [ 6 , 7 ]. The catalysis of 10-Oxogeranial involves iridodial synthase (IS) and iridodial oxidoreductase (IO), resulting in the formation of 7-Deoxyloganetic acid [ 8 ].…”

Section: Introductionmentioning

confidence: 99%

Genome-Wide Mining of CULLIN E3 Ubiquitin Ligase Genes from Uncaria rhynchophylla

Shao,

Mu,

Zhou

et al. 2024

Plants

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CULLIN (CUL) protein is a subtype of E3 ubiquitin ligase that is involved in a variety of biological processes and responses to stress in plants. In Uncaria rhynchophylla, the CUL gene family has not been identified and its role in plant development, stress response and secondary metabolite synthesis has not been studied. In this study, 12 UrCUL gene members all contained the typical N-terminal domain and C-terminal domain identified from the U. rhynchophylla genome and were classified into four subfamilies based on the phylogenetic relationship with CULs in Arabidopsis thaliana. They were unevenly distributed on eight chromosomes but had a similar structural composition in the same subfamily, indicating that they were relatively conserved and potentially had similar gene functions. An interspecific and intraspecific collinearity analysis showed that fragment duplication played an important role in the evolution of the CUL gene family. The analysis of the cis-acting elements suggests that the UrCULs may play an important role in various biological processes, including the abscisic acid (ABA) response. To investigate this hypothesis, we treated the roots of U. rhynchophylla tissue-cultured seedlings with ABA. The expression pattern analysis showed that all the UrCUL genes were widely expressed in roots with various expression patterns. The co-expression association analysis of the UrCULs and key enzyme genes in the terpenoid indole alkaloid (TIA) synthesis pathway revealed the complex expression patterns of 12 UrCUL genes and some key TIA enzyme genes, especially UrCUL1, UrCUL1-likeA, UrCUL2-likeA and UrCUL2-likeB, which might be involved in the biosynthesis of TIAs. The results showed that the UrCULs were involved in the response to ABA hormones, providing important information for elucidating the function of UrCULs in U. rhynchophylla. The mining of UrCULs in the whole genome of U. rhynchophylla provided new information for understanding the CUL gene and its function in plant secondary metabolites, growth and development.

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Iridoid Sex Pheromone Biosynthesis in Aphids Mimics Iridoid‐Producing Plants

Cited by 9 publications

References 18 publications

Biosynthesis of iridoid sex pheromones in aphids

Biosynthesis of iridoid sex pheromones in aphids

The genomic and enzymatic basis for iridoid biosynthesis in cat thyme (Teucrium marum)

Genome-Wide Mining of CULLIN E3 Ubiquitin Ligase Genes from Uncaria rhynchophylla

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