Advertisement

Epoxidases Involved in the Biosynthesis of Type II Sex Pheromones

  • Takeshi Fujii
  • Yu Rong
  • Yukio Ishikawa
Chapter
  • 27 Downloads
Part of the Entomology Monographs book series (ENTMON)

Abstract

In moth species that utilize alkenyl (type II) sex pheromones, selective epoxidation of double bonds in the alkene pheromone components confers further diversity on their chemical structures. Two arctiids, the fall webworm Hyphantria cunea and the mulberry tiger moth Lemyra imparilis, use the same epoxyalkene, Z3,Z6,epo9-21:H, as the main pheromone component. In these species, we recently identified cytochrome P450s (CYPs) belonging to the CYP341 family as enzymes involved in the specific epoxidation of a Z9 double bond of the pheromone precursor Z3,Z6,Z9-21:H. Furthermore, a cytochrome P450 belonging to a different family, CYP340, was identified as an enzyme responsible for the specific epoxidation of a Z3 double bond of the pheromone precursor Z3,Z6,Z9-19:H in the Japanese giant looper Ascotis selenaria, which uses epo3,Z6,Z9-19:H as the main pheromone component. These findings suggest that epoxidases (CYPs) with different regio-specificities evolved independently.

Keywords

Epoxidases Cytochrome P450 Type II sex pheromones 

Notes

Acknowledgment

We thank Prof. Tetsu Ando, Dr. Masanobu Yamamoto, and Dr. Masataka G. Suzuki for continuous support of this study.

References

  1. Ando T, Yamamoto M (2018) Internet Database. https://lepipheromone.sakura.ne.jp/lepi_phero_list
  2. Ando T, Ohtani K, Yamamoto M, Miyamoto T, Qi XR, Witjaksono (1997) Sex Pheromone of Japanese giant looper, Ascotis selenaria cretacea: identification and field tests. J Chem Ecol 23:2413–2423CrossRefGoogle Scholar
  3. Ando T, Inomata S, Yamamoto M (2004) Lepidopteran sex pheromones. Top Curr Chem 239:51–96CrossRefGoogle Scholar
  4. Antony B, Fujii T, Moto K, Matsumoto S, Fukuzawa M, Nakano R, Tatsuki S, Ishikawa Y (2009) Pheromone-gland-specific fatty-acyl reductase in the adzuki bean borer, Ostrinia scapulalis (Lepidoptera: Crambidae). Insect Biochem Mol Biol 39:90–95CrossRefGoogle Scholar
  5. Blomquist GJ (2010) Biosynthesis of cuticular hydrocarbons. In: Blomquist GJ, Bagnères AG (eds) Insect hydrocarbons: biology, biochemistry, and chemical ecology. Cambridge University Press, New York, pp 35–52CrossRefGoogle Scholar
  6. Calla B, Noble K, Johnson RM, Walden KK, Schuler MA, Robertson HM, Berenbaum MR (2017) Cytochrome P450 diversification and hostplant utilization patterns in specialist and generalist moths: birth, death and adaptation. Mol Ecol 26:6021–6035CrossRefGoogle Scholar
  7. Chino H (1985) Lipid transport: biochemistry of hemolymph lipophorin. In: Kerkut GA, Gilbert LI (eds) Comprehensive insect physiology, biochemistry and pharmacology, vol. 10. Pergamon Press, New York, pp 115–135Google Scholar
  8. Daborn PJ, Lumb C, Boey A, Wong W, Batterham P (2007) Evaluating the insecticide resistance potential of eight Drosophila melanogaster cytochrome P450 genes by transgenic over-expression. Insect Biochem Mol Biol 37:512–519CrossRefGoogle Scholar
  9. Daimon T, Kozaki T, Niwa R, Kobayashi I, Furuta K (2012) Precocious metamorphosis in the juvenile hormone-deficient mutant of the silkworm, Bombyx mori. PLoS Genet 8:e1002486CrossRefGoogle Scholar
  10. Després L, David JP, Gallet C (2007) The evolutionary ecology of insect resistance to plant chemicals. Trends Ecol Evol 22:298–307CrossRefGoogle Scholar
  11. Feyereisen R (2012) Insect CYP genes and P450 enzymes. In: Gilbert LI (ed) Insect molecular biology and biochemistry. Academic, New York, pp 236–316CrossRefGoogle Scholar
  12. Finet C, Slavik K, Pu J, Carroll SB, Chung H (2019) Birth-and-death evolution of the fatty acyl-CoA reductase (FAR) gene family and diversification of cuticular hydrocarbon synthesis in Drosophila. Genome Biol Evol 11:1541–1551.  https://doi.org/10.1101/509588CrossRefPubMedPubMedCentralGoogle Scholar
  13. Fujii T, Suzuki MG, Kawai T, Tsuneizumi K, Ohnishi A, Kurihara M, Matsumoto S, Ando T (2007) Determination of the pheromone-producing region that has epoxidation activity in the abdominal tip of the Japanese giant looper, Ascotis selenaria cretacea (Lepidoptera: Geometridae). J Insect Physiol 53:312–318CrossRefGoogle Scholar
  14. Fujii T, Suzuki MG, Katsuma S, Ito K, Rong Y, Matsumoto S, Ando T, Ishikawa Y (2013) Discovery of a disused desaturase gene from the pheromone gland of the moth Ascotis selenaria, which secretes an epoxyalkenyl sex pheromone. Biochem Biophys Res Comm 441:849–855CrossRefGoogle Scholar
  15. Fujii T, Yamamoto M, Nakano R, Nirazawa T, Rong Y, Dong SL, Ishikawa Y (2015) Alkenyl sex pheromone analogs in the hemolymph of an arctiid Eilema japonica and several non-arctiid moths. J Insect Physiol 82:109–113CrossRefGoogle Scholar
  16. Helvig C, Koener JF, Unnithan GC, Feyereisen R (2004) CYP15A1, the cytochrome P450 that catalyzes epoxidation of methyl farnesoate to juvenile hormone III in cockroach corpora allata. Proc Natl Acad Sci U S A 101:4024–4029CrossRefGoogle Scholar
  17. Jurenka R (2004) Insect pheromone biosynthesis. In: The chemistry of pheromones and other semiochemicals I. Springer, Berlin/Heidelberg, pp 97–132CrossRefGoogle Scholar
  18. Jurenka R, Subchev M (2000) Identification of cuticular hydrocarbons and the alkene precursor to the pheromone in hemolymph of the female gypsy moth, Lymantria dispar. Arch Insect Biochem Physiol 43:108–115CrossRefGoogle Scholar
  19. Liénard MA, Hagström ÅK, Lassance JM, Löfstedt C (2010) Evolution of multicomponent pheromone signals in small ermine moths involves a single fatty-acyl reductase gene. Proc Natl Acad Sci U S A 107:10955–10960CrossRefGoogle Scholar
  20. Liu W, Rooney AP, Xue B, Roelofs WL (2004) Desaturases from the spotted fireworm moth (Choristoneura parallela) shed light on the evolutionary origins of novel moth sex pheromone desaturases. Gene 342:303–311CrossRefGoogle Scholar
  21. MacLean M, Nadeau J, Gurnea T, Tittiger C, Blomquist GJ (2018) Mountain pine beetle (Dendroctonus ponderosae) CYP4Gs convert long and short chain alcohols and aldehydes to hydrocarbons. Insect Biochem Mol Biol 201:11–20CrossRefGoogle Scholar
  22. Matsumoto S, Hull JJ, Ohnishi A, Moto KI, Fónagy A (2007) Molecular mechanisms underlying sex pheromone production in the silkmoth, Bombyx mori: characterization of the molecular components involved in bombykol biosynthesis. J Insect Physiol 53:752–759CrossRefGoogle Scholar
  23. Matsuoka K, Tabunoki H, Kawai T, Ishikawa S, Yamamoto M, Sato R, Ando T (2006) Transport of a hydrophobic biosynthetic precursor by lipophorin in the hemolymph of geometrid female moth which secretes an epoxyalkenyl sex pheromone. Insect Biochem Mol Biol 36:576–583CrossRefGoogle Scholar
  24. Millar JG (2000) Polyene hydrocarbons and epoxides: a second major class of lepidopteran sex attractant pheromones. Annu Rev Entomol 45:575–604CrossRefGoogle Scholar
  25. Millar JG (2010) Polyene hydrocarbons, epoxides, and related compounds as components of lepidopteran pheromone blends. In: Blomquist GJ, Bagnères AG (eds) Insect Hydrocarbons. Cambridge University Press, New York, pp 390–447CrossRefGoogle Scholar
  26. Miyamoto T, Yamamoto M, Ono A, Ohtani K, Ando T (1999) Substrate specificity of the epoxidation reaction in sex pheromone biosynthesis of the Japanese giant looper (Lepidoptera: Geometridae). Insect Biochem Mol Biol 29:63–69CrossRefGoogle Scholar
  27. Moto K, Yoshiga T, Yamamoto M, Takahashi S, Okano K, Ando T, Nakata T, Matsumoto S (2003) Pheromone gland-specific fatty-acyl reductase of the silkmoth, Bombyx mori. Proc Natl Acad Sci U S A 100:9156–9161CrossRefGoogle Scholar
  28. Moto K, Suzuki GM, Hull JJ, Kurata R, Takahashi S, Yamamoto M, Okano K, Imai K, Ando T, Matsumoto S (2004) Involvement of a bifunctional fatty-acyl desaturase in the biosynthesis of the silkmoth, Bombyx mori, sex pheromone. Proc Natl Acad Sci U S A 101:8631–8636CrossRefGoogle Scholar
  29. Niu G, Rupasinghe SG, Zangerl AR, Siegel JP, Schuler MA, Berenbaum MR (2011) A substrate-specific cytochrome P450 monooxygenase, CYP6AB11, from the polyphagous navel orangeworm (Amyelois transitella). Insect Biochem Mol Biol 41:244–253.  https://doi.org/10.1016/j.ibmb.2010.12.009CrossRefPubMedGoogle Scholar
  30. Niwa R, Matsuda T, Yoshiyama T, Namiki T, Mita K, Fujimoto Y, Kataoka H (2004) CYP306A1, a cytochrome P450 enzyme, is essential for ecdysteroid biosynthesis in the prothoracic glands of Bombyx and Drosophila. J Biol Chem 279:35942–35949CrossRefGoogle Scholar
  31. Ortiz de Montellano PR (2015) Substrate oxidation by cytochrome P450 enzymes. In: Ortiz de Montellano PR (ed) Cytochrome P450. Springer, Boston, pp 111–176Google Scholar
  32. Parker RE, Isaacs NS (1959) Mechanisms of epoxide reactions. Chem Rev 59:737–799CrossRefGoogle Scholar
  33. Qiu Y, Tittiger C, Wicker–Thomas C, Le Goff G, Young S, Wajnberg E, Fricauxc T, Taquetc N, Blomquist GJ, Feyereisen R (2012) An insect–specific P450 oxidative decarbonylase for cuticular hydrocarbon biosynthesis. Proc Natl Acad Sci USA 109:14858–14863CrossRefGoogle Scholar
  34. Regier JC, Mitter C, Mitter K, Cummings MP, Bazinet AL, Hallwachs W, Janzen DH, Zwick A (2017) Further progress on the phylogeny of Noctuoidea (Insecta: Lepidoptera) using an expanded gene sample. Syst Entomol 42(1):82–93CrossRefGoogle Scholar
  35. Rong Y, Fujii T, Katsuma S, Yamamoto M, Ando T, Ishikawa Y (2014) CYP341B14: a cytochrome P450 involved in the specific epoxidation of pheromone precursors in the fall webworm Hyphantria cunea. Insect Biochem Mol Biol 54:122–128CrossRefGoogle Scholar
  36. Rong Y, Fujii T, Naka H, Yamamoto M, Ishikawa Y (2019a) Functional characterization of the epoxidase gene, Li_epo1 (CYP341B14), involved in generation of epoxyalkene pheromones in the mulberry tiger moth Lemyra imparilis. Insect Biochem Mol Biol 107:46–52CrossRefGoogle Scholar
  37. Rong Y, Fujii T, Ishikawa Y (2019b) CYPs in different families are involved in the divergent regio-specific epoxidation of alkenyl sex pheromone precursors in moths. Insect Biochem Mol Biol 108:9–15CrossRefGoogle Scholar
  38. Schal C, Sevala V (1998) Novel and highly specific transport of a volatile sex pheromone by hemolymph lipophorin in moths. Naturwissenschaften 85:339–342CrossRefGoogle Scholar
  39. Schuler MA (2011) P450s in plant-insect interactions. Biochim Biophys Acta 1814:36–45.  https://doi.org/10.1016/j.bbapap.2010.09.012CrossRefPubMedGoogle Scholar
  40. Schuler MA, Berenbaum MR (2013) Structure and function of cytochrome P450s in insect adaptation to natural and synthetic toxins: insights gained from molecular modeling. J Chem Ecol 39:1232–1245.  https://doi.org/10.1007/s10886-013-0335-7CrossRefPubMedGoogle Scholar
  41. Wei W, Miyamoto T, Endo M, Murakawa T, Pu G-Q, Ando T (2003) Polyunsaturated hydrocarbons in the hemolymph: biosynthetic precursors of epoxy pheromones of geometrid and Arctiid moths. Insect Biochem Mol Biol 33:397–405CrossRefGoogle Scholar
  42. Wei W, Yamamoto M, Asato T, Fujii T, Pu GQ, Ando T (2004) Selectivity and neuroendocrine regulation of the precursor uptake by pheromone glands from hemolymph in geometrid female moths, which secrete epoxyalkenyl sex pheromones. Insect Biochem Mol Biol 34:1215–1224CrossRefGoogle Scholar
  43. Yu L, Tang W, He W, Ma X, Vasseur L, Baxter SW, Yang G, Huang S, Song F, You M (2015) Characterization and expression of the cytochrome P450 gene family in diamondback moth, Plutella xylostella (L.). Sci Rep 5:8952CrossRefGoogle Scholar
  44. Yu Z, Zhang X, Wang Y, Moussian B, Zhu KY, Li S, Ma E, Zhang J (2016) LmCYP4G102: an oenocyte-specific cytochrome P450 gene required for cuticular waterproofing in the migratory locust, Locusta migratoria. Sci Rep 6:29980CrossRefGoogle Scholar
  45. Zahiri R, Holloway JD, Kitching IJ, Donald Lafontaine J, Mutanen M, Wahlberg N (2012) Molecular phylogenetics of Erebidae (Lepidoptera, Noctuoidea). Syst Entomol 37(1):102–124CrossRefGoogle Scholar

Copyright information

© Springer Nature Singapore Pte Ltd. 2020

Authors and Affiliations

  • Takeshi Fujii
    • 1
  • Yu Rong
    • 1
  • Yukio Ishikawa
    • 1
  1. 1.Laboratory of Applied Entomology, Graduate School of Agricultural and Life SciencesThe University of TokyoTokyoJapan

Personalised recommendations