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Journal of Molecular Evolution

, Volume 86, Issue 6, pp 379–394 | Cite as

Evolution of the Biosynthetic Pathway for Cyanogenic Glucosides in Lepidoptera

  • Mika Zagrobelny
  • Mikael Kryger Jensen
  • Heiko Vogel
  • René Feyereisen
  • Søren Bak
Original Article

Abstract

Cyanogenic glucosides are widespread defence compounds in plants, and they are also found in some arthropods, especially within Lepidoptera. The aliphatic linamarin and lotaustralin are the most common cyanogenic glucosides in Lepidoptera, and they are biosynthesised de novo, and/or sequestered from food plants. Their biosynthetic pathway was elucidated in the burnet moth, Zygaena filipendulae, and consists of three enzymes: two cytochrome P450 enzymes, CYP405A2 and CYP332A3, and a glucosyl transferase, UGT33A1. Heliconius butterflies also produce linamarin and lotaustralin and have close homologs to CYP405A2 and CYP332A3. To unravel the evolution of the pathway in Lepidoptera, we performed phylogenetic analyses on all available CYP405 and CYP332 sequences. CYP332 sequences were present in almost all Lepidoptera, while the distribution of CYP405s among butterflies and moths was much more limited. Negative purifying selection was found in both CYP enzyme families, indicating that the biosynthesis of CNglcs is an old trait, and not a newly evolved pathway. We compared CYP405A2 to its close paralog, CYP405A3, which is not involved in the biosynthetic pathway. The only significant difference between these two enzymes is a smaller substrate binding pocket in CYP405A2, which would make the enzyme more substrate specific. We consider it likely that the biosynthetic pathway of CNglcs in butterflies and moths have evolved from a common pathway, perhaps based on a predisposition for detoxifying aldoximes by way of a CYP332. Later the aldoxime metabolising CYP405s evolved, and a UGT was recruited into the pathway to establish de novo biosynthesis of CNglcs.

Keywords

CYP405 CYP332 CYP324 Heliconius Zygaena Cytochrome P450 

Notes

Acknowledgements

Axel Hofmann, Eric Drouet and Marc Nicolle are thanked for providing species of Zygaenoidea. We are grateful to Lene Dalsten for sequencing CYP405A2 from all Zygaenoidea species included in this study. Dr. David R. Nelson is thanked for assigning official names to all unnamed CYPs extracted from Genbank and private transcriptomes according to the general P450 nomenclature. We are grateful to Adam Takos for providing E. postvittana larvae and adults from Australia, and Camilla Knudsen for Pieris brassicae larvae from Copenhagen. This work was supported by the Danish Council for Independent Research (DFF–1323-00088).

Supplementary material

239_2018_9854_MOESM1_ESM.txt (59 kb)
Supplementary File S1 (TXT 58 KB)
239_2018_9854_MOESM2_ESM.docx (17 kb)
Supplementary Table S1 (DOCX 16 KB)

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Authors and Affiliations

  1. 1.Department of Plant and Environmental SciencesUniversity of CopenhagenCopenhagenDenmark
  2. 2.Department of EntomologyMax Planck Institute of Chemical EcologyJenaGermany

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