[en] The winter moth (Operophtera brumata L., Lepidoptera: Geometridae) utilizes a single hydrocarbon, 1,Z3,Z6,Z9-nonadecatetraene, as its sex pheromone. We tested the hypothesis that a fatty acid precursor, Z11,Z14,Z17,19-nonadecanoic acid, is biosynthesized from α-linolenic acid, through chain elongation by one 2-carbon unit, and subsequent methyl-terminus desaturation. Our results show that labeled α-linolenic acid is indeed incorporated into the pheromone component in vivo. A fatty-acyl-CoA desaturase gene that we found to be expressed in the abdominal epidermal tissue, the presumed site of biosynthesis for type II pheromones, was characterized and expressed heterologously in a yeast system. The transgenic yeast expressing this insect derived gene could convert Z11,Z14,Z17-eicosatrienoic acid into Z11,Z14,Z17,19-eicosatetraenoic acid. These results provide evidence that a terminal desaturation step is involved in the winter moth pheromone biosynthesis, prior to the decarboxylation.
Disciplines :
Biochemistry, biophysics & molecular biology
Author, co-author :
Ding, Bao-Jian; Functional Zoology, Department of Biology, Lund University, Sölvegatan 37, SE-22362 Lund, Sweden. bao-jian.ding@biol.lu.se
Lienard, Marjorie ; Université de Liège - ULiège > GIGA > GIGA Molecular Biology of Diseases ; Functional Zoology, Department of Biology, Lund University, SE-223 62 Lund, Sweden
Wang, Hong-Lei; Functional Zoology, Department of Biology, Lund University, SE-223 62 Lund, Sweden
Zhao, Cheng-Hua; State Key Laboratory of Integrated Management of Pest Insects and Rodents, Institute of Zoology, The Chinese Academy of Sciences, 100080 Beijing, China
Löfstedt, Christer; Functional Zoology, Department of Biology, Lund University, SE-223 62 Lund, Sweden
Language :
English
Title :
Terminal fatty-acyl-CoA desaturase involved in sex pheromone biosynthesis in the winter moth (Operophtera brumata).
The authors thank G. Szöcs at the Department of Zoology, Hungarian Academy of Science, Budapest, Hungary for regularly providing the insects over the years. We are thankful to Dr. R. Adlof (Northern Regional Research Center, USDA-ARS, Peoria, IL) for providing labeling compounds, and to Dr. W. Christie (Scottish Crop Research Institute) for advice on the mass spectrum of tetra-unsaturated fatty acid methylester. This project was supported by the Swedish Research Council (VR) .
Altschul S.F., Madden T.L., Schaeffer A.A., Zhang J., Zhang Z., Miller W., Lipman D.J. Gapped BLAST and PSI-BLAST: A new generation of protein database search programs. Nucleic Acids Res. 1997, 25:3389-3402.
Ando T., Inomata S., Yamamoto M. Lepidopteran sex pheromones. Top. Curr. Chem. 2004, 239:51-96.
Ando T., Kawai T., Matsuoka K. Epoxyalkenyl sex pheromones produced by female moths in highly evolved groups: biosynthesis and its endocrine regulation. J. Pestic. Sci. 2008, 33:17-20.
Arn H., Toth M., Priesner E. List of Sex Pheromones of Lepidoptera and Related Attractants 1992, OILB/IOBC-WPRS, Wenswil, Switzerland. second ed.
Bestmann H.J., Borsche T., Koschatzky K.H., Michaelis K., Platz H., Roth K., Suess J., Vostrosky O., Knauf W. Pheromones XLII. 1,3,6,9-nonadecatetraene, the sex pheromone of the winter moth Operophtera brumata Geometridae. Tetrahedron Lett. 1982, 23:4007-4010.
Billeter J.-C., Atallah J., Krupp J.J., Millar J.G., Levine J.D. Specialized cells tag sexual and species identity in Drosophila melanogaster. Nature 2009, 461:987-992.
Bjostad L.B., Roelofs W.L. Sex pheromone biosynthetic precursors in Bombyx mori. Insect Biochem. 1984, 14:275-278.
Brauner A., Budzikiewicz H., Boland W. Studies in chemical ionization mass spectrometry: V-localization of homoconjugated triene and tetraene units in aliphatic compounds. Org. Mass Spectrom 1982, 17:161-164.
Choi M.-Y., Lim H., Park K.C., Adlof R., Wang S., Zhang A., Jurenka R. Identification and biosynthetic studies of the hydrocarbon sex pheromone in Utetheisa ornatrix. J. Chem. Ecol 2007, 33:1336-1345.
Diehl P.A. Synthesis and release of hydrocarbons by the oenocytes of the desert locust, Schistocera gregaria. J. Insect Physiol. 1975, 21:1237-1246.
Erik L.L., Sonnhammer G.V.H., Anders K. A hidden Markov model for predicting transmembrane helices in protein sequences. Proc. of Sixth Int. Conf. on Intelligent Systems for Molecular Biology 1998, 175-182. AAAI Press, Menlo Park, CA. J. Glasgow, T. Littlejohn, F. Major, R. Lathrop, D. Sankoff, C. Sensen (Eds.).
Fellenberg A.J., Johnson D.W., Poulos A., Sharp P. Simple mass spectrometric differentiation of the n-3, n-6 and n-9 series of methylene interrupted polyenoic acids. Biomed. Environ. Mass Spectrom. 1987, 14:127-130.
Ferveur J.-F., Savarit F., O'Kane C.J., Sureau G., Greenspan R.J., Jallon J.M. Genetic feminization of pheromones and its behavioral consequences in Drosophila males. Science 1997, 276:1555-1558.
Gehlsen U., Lindemann P., Rettig W., Moritz G., Tschuch G. Terminal double bonds in the alkenes and acetates of defensive secretion from the thrips Suocerathrips linguis Mound & Marullo, 1994 (Thysanoptera: Phlaeothripidae). Chemoecology 2009, 19:97-102.
Hall T.A. BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp. Ser. 1999, 41:95-98.
Hao G., Liu W., O'Connor M., Roelofs W.L. Acyl-CoA Z9- and Z10-desaturase genes from a New Zealand leafroller moth species, Planotortrix octo. Insect Biochem. Mol. Biol. 2002, 32:961-966.
Jeong S.E., Rosenfield C.-L., Marsella-Herrick P., You K.M., Knipple D.C. Multiple acyl-CoA desaturase-encoding transcripts in pheromone glands of Helicoverpa assulta, the oriental tobacco budworm. Insect Biochem. Mol. Biol. 2003, 33:609-622.
Jurenka R. Insect pheromone biosynthesis. Top. Curr. Chem. 2004, 239:97-132.
Jurenka R.A., Subchev M. Identification of cuticular hydrocarbons and the alkene precursor to the pheromone in hemolymph of the female gypsy moth, Lymantria dispar. Arch. Insect Biochem. Physiol. 2000, 43:108-115.
Jurenka R.A., Subchev M., Abad J.-L., Choi M.-Y., Fabrias G. Sex pheromone biosynthetic pathway for disparlure in the gypsy moth, Lymantria dispar. Proc. Natl. Acad. Sci. U.S.A. 2003, 100:809-814.
Knipple D.C., Rosenfield C.-L., Miller S.J., Liu W., Tang J., Ma P.W.K., Roelofs W.L. Cloning and functional expression of a cDNA encoding a pheromone gland-specific acyl-CoA Δ11-desaturase of the cabbage looper moth, Trichoplusia ni. Proc. Natl. Acad. Sci. U.S.A. 1998, 95:15287-15292.
Knipple D.C., Rosenfield C.-L., Nielsen R., You K.M., Jeong S.E. Evolution of the integral membrane desaturase gene family in moths and flies. Genetics 2002, 162:1737-1752.
Liénard M.A., Lassance J.-M., Wang H.-L., Zhao C.-H., Piskur J., Johansson T., Löfstedt C. Elucidation of the sex-pheromone biosynthesis producing 5,7-dodecadienes in Dendrolimus punctatus (Lepidoptera: Lasiocampidae) reveals Δ 11-and Δ 9-desaturases with unusual catalytic properties. Insect Biochem. Mol. Biol. 2010, 40:440-452.
Liénard M.A., Strandh M., Hedenstrom E., Johansson T., Löfstedt C. Key biosynthetic gene subfamily recruited for pheromone production prior to the extensive radiation of Lepidoptera. BMC Evol. Biol. 2008, 8. Article No.: 270.
Liu W., Jiao H., Murray N.C., O'Connor M., Roelofs W.L. Gene characterized for membrane desaturase that produces (E)-11 isomers of mono- and diunsaturated fatty acids. Proc. Natl. Acad. Sci. U.S.A. 2002, 99:620-624.
Liu W., Jiao H., O'Connor M., Roelofs W.L. Moth desaturase characterized that produces both Z and E isomers of DELTA11-tetradecenoic acids. Insect Biochem. Mol. Biol. 2002, 32:1489-1495.
Liu W., Ma P.W.K., Marsella-Herrick P., Rosenfield C.-L., Knipple D.C., Roelofs W. Cloning and functional expression of a cDNA encoding a metabolic acyl-CoA Δ9-desaturase of the cabbage looper moth, Trichoplusia ni. Insect Biochem. Mol. Biol. 1999, 29:435-443.
Liu W., Rooney A.P., Xue B., Roelofs W.L. Desaturases from the spotted fireworm moth (Choristoneura parallela) shed light on the evolutionary origins of novel moth sex pheromone desaturases. Gene 2004, 342:303-311.
Matoušková P., Pichova I., Svatos A. Functional characterization of a desaturase from the tobacco hornworm moth (Manduca sexta) with bifunctional Z11- and 10,12-desaturase activity. Insect Biochem. Mol. Biol. 2007, 37:601-610.
Matsuoka K., Tabunoki H., Kawai T., Ishikawa S., Yamamoto M., Sato R., Ando T. Transport of a hydrophobic biosynthetic precursor by lipophorin in the hemolymph of a geometrid female moth which secretes an epoxyalkenyl sex pheromone. Insect Biochem. Mol. Biol. 2006, 36:576-583.
Meyer F., Harrison A.G. A mechanism for tropylium ion formation by electron impact. J. Am. Chem. Soc. 1964, 86(22):4757-4761.
Millar, J.G., 2000. Polyene hydrocarbons and epoxides: a second major class of Lepidopteran sex attractant pheromones. In: Berenbaum, M.R., Carde, R.T., Robinson, G.E. (Eds.,). Annual Review of Entomology. Annual Reviews, pp. 575-604.
Moto K.i., Suzuki M.G., Hull J.J., Kurata R., Takahashi S., Yamamoto M., Okano K., Imai K., Ando T., Matsumoto S. Involvement of a bifunctional fatty-acyl desaturase in the biosynthesis of the silkmoth, Bombyx mori, sex pheromone. Proc. Natl. Acad. Sci. U.S.A. 2004, 101:8631-8636.
Patel O., Fernley R., MacReadie I. Saccharomyces cerevisiae expression vectors with thrombin-cleavable N- and C-terminal 6x(His) tags. Biotechnol. Lett. 2003, 25:331-334.
Rafaeli A. Pheromone biosynthesis activating neuropeptide (PBAN): regulatory role and mode of action. Gen. Comp. Endocrinol. 2009, 162:69-78.
Rafaeli A., Jurenka R.A. PBAN regulation of pheromone biosynthesis in female moths. Insect Pheromone Biochemistry and Molecular Biology 2003, 107-136. Elsevier, Amsterdam. G. Blomquist, R. Vogt (Eds.).
Raina A.K., Jaffe H., Kempe T.G., Keim P., Blacher R.W., Fales H.M., Riley C.T., Klun J.A., Ridgway R.L., Hayes D.K. Identification of a neuropeptide hormone that regultes sex pheromone production in female moths. Science 1989, 244:796-798.
Roelofs W.L., Hill A.S., Linn C.E., Meinwald J., Jain S.C., Herbert H.J., Smith R.F. Sex pheromone of the winter moth, a geometrid with unusually low temperature precopulatory responses. Science 1982, 217:657-659.
Roelofs W.L., Rooney A.P. Molecular genetics and evolution of pheromone biosynthesis in Lepidoptera. Proc. Natl. Acad. Sci. U.S.A. 2003, 100:9179-9184.
Rosenfield C.-L., You K.M., Marsella-Herrick P., Roelofs W.L., Knipple D.C. Structural and functional conservation and divergence among acyl-CoA desaturases of two noctuid species, the corn earworm, Helicoverpa zea, and the cabbage looper, Trichoplusia ni. Insect Biochem. Mol. Biol. 2001, 31:949-964.
Rule G.S., Roelofs W.L. Biosynthesis of sex pheromone components from linolenic acid in arctiid moths. Arch. Insect Biochem. Physiol. 1989, 12:89-98.
Schal C., Sevala V., Carde R.T. Novel and highly specific transport of a volatile sex pheromone by hemolymph lipophorin in moths. Naturwissenschaften 1998, 85:339-342.
Schal C., Sevala V.L., Young H.P., Bachmann J.A.S. Sites of synthesis and transport pathways of insect hydrocarbons: cuticle and ovary as target tissues. Am. Zool. 1998, 38:382-393.
Schneiter R., Tatzer V., Gogg G., Leitner E., Kohlwein S.D. Elo1p-dependent carboxy-terminal elongation of C14:Δ9 to C16:Δ11 fatty acids in Saccharomyces cerevisiae. J. Bacteriol. 2000, 182:3655-3660.
Serra M., Pina B., Abad J.L., Camps F., Fabrias G. A multifunctional desaturase involved in the biosynthesis of the processionary moth sex pheromone. Proc. Natl. Acad. Sci. U.S.A. 2007, 104:16444-16449.
Serra M.S., Pina B., Bujons J., Camps F., Fabrias G. Biosynthesis of 10,12-dienoic fatty acids by a bifunctional Δ11 desaturase in Spodoptera littoralis. Insect Biochem. Mol. Biol. 2006, 36:634-641.
Shanklin J., Cahoon E.B. Desaturation and related modifications of fatty acids. Annual Review of Plant Physiology and Plant Molecular Biology 1998, 611-641. Annual Reviews Inc. R.L. Jones, C.R. Somerville, V. Walbot (Eds.).
Shanklin J., Whittle E., Fox B.G. Eight histidine residues are catalytically essential in a membrane-associated iron enzyme, stearoyl-CoA desaturase, and are conserved in alkane hydroxylase and xylene monooxygenase. Biochemistry 1994, 33:12787-12794.
Stanley-Samuelson D.W., Jurenka R.A., Cripps C., Blomquist G.J., De Renobales M. Fatty acids in insects composition metabolism and biological significance. Arch. Insect Biochem. Physiol. 1988, 9:1-34.
Stanley-Samuelson D.W., Jurenka R.A., Loher W., Blomquist G.J. Metablism of polyunsaturated fatty acids by larvae of the vaxmoth Gallerla mellonella. Arch. Insect Biochem. Physiol. 1987, 6:141-150.
Tamura K., Dudley J., Nei M., Kumar S. MEGA4: molecular evolutionary genetics analysis (MEGA) software version 4.0. Mol. Biol. Evol. 2007, 24:1596-1599.
Thompson J.D., Higgins D.G., Gibson T.J. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res. 1994, 22:4673-4680.
Wang H.-L., Zhao C.-H., Millar J.G., Cardé R.T., Löfstedt C. Biosynthesis of unusual moth pheromone components involves two different pathways in the navel orangeworm, Amyelois transitella. J. Chem. Ecol 2010, 36:535-547.
Wang H.-L., Liénard M.A., Zhao C.-H., Wang C.-Z., Löfstedt C. Neofunctionalization in an ancestral insect desaturase lineage led to rare Δ6 pheromone signals in the Chinese tussah silkworm. Insect Biochem. Mol. Biol. 2010, 40:742-751.
Wei W., Miyamoto T., Endo M., Murakawa T., Pu G.Q., Ando T. Polyunsaturated hydrocarbons in the hemolymph: biosynthetic precursors of epoxy pheromones of geometrid and arctiid moths. Insect Biochem. Mol. Biol. 2003, 33:397-405.
Wei W., Yamamoto M., Asato T., Fujii T., Pu G.-Q., Ando T. 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. 2004, 34:1215-1224.
Wicker-Thomas C., Guenachi I., Keita Y.F. Contribution of oenocytes and pheromones to courtship behaviour in Drosophila. BMC Biochem. 2009, 10. Article No.: 21.
Yamamoto M., Yamakawa R., Oga T., Takei Y., Kinjo M., Ando T. Synthesis and chemical characterization of hydrocarbons with a 6,9,11-, 3,6,9,11-, or 1,3,6,9-polyene system, pheromone candidates in Lepidoptera. J. Chem. Ecol 2008, 34:1057-1064.