Elucidation of the sex-pheromone biosynthesis producing 5,7-dodecadienes in Dendrolimus punctatus (Lepidoptera: Lasiocampidae) reveals Delta 11- and Delta 9-desaturases with unusual catalytic properties. - 2010
Elucidation of the sex-pheromone biosynthesis producing 5,7-dodecadienes in Dendrolimus punctatus (Lepidoptera: Lasiocampidae) reveals Delta 11- and Delta 9-desaturases with unusual catalytic properties.
[en] Sex pheromones produced by female moths of the Lasiocampidae family include conjugated 5,7-dodecadiene components with various oxygenated terminal groups. Here we describe the molecular cloning, heterologous expression and functional characterization of desaturases associated with the biosynthesis of these unusual chemicals. By homology-based PCR screening we characterized five cDNAs from the female moth pheromone gland that were related to other moth desaturases, and investigated their role in the production of the (Z)-5-dodecenol and (Z5,E7)-dodecadienol, major pheromone constituents of the pine caterpillar moth, Dendrolimus punctatus. Functional expression of two desaturase cDNAs belonging to the Delta 11-subfamily, Dpu-Delta 11(1)-APSQ and Dpu-Delta 11(2)-LPAE, showed that they catalysed the formation of unsaturated fatty acyls (UFAs) that can be chain-shortened by beta-oxidation and subsequently reduced to the alcohol components. A first (Z)-11-desaturation step is performed by Dpu- Delta 11(2)-LPAE on stearic acid that leads to (Z)-11-octadecenoic acyl, which is subsequently chain shortened to the (Z)-5-dodecenoic acyl precursor. The Dpu-Delta 11(1)-APSQ desaturase had the unusual property of producing Delta 8 mono-UFA of various chain lengths, but not when transformed yeast were grown in presence of (Z)-9-hexadecenoic acyl, in which case the biosynthetic intermediate (Z9,E11)-hexadecadienoic UFA was produced. In addition to a typical Z9 activity, a third transcript, Dpu- Delta 9-KPSE produced E9 mono-UFAs of various chain lengths. When provided with the (Z)-7-tetradecenoic acyl, it formed the (Z7,E9)-tetradecadienoic UFA, another biosynthetic intermediate that can be chain-shortened to (Z5,E7)-dodecadienoic acyl. Both Dpu-Delta 11(1)-APSQ and Dpu-Delta 9-KPSE thus exhibited desaturase activities consistent with the biosynthesis of the dienoic precursor. The combined action of three desaturases in generating a dienoic sex-pheromone component emphasizes the diversity and complexity of chemical reactions that can be catalysed by pheromone biosynthetic fatty-acyl-CoA desaturases in moths.
Disciplines :
Entomologie & lutte antiravageur
Auteur, co-auteur :
Lienard, Marjorie ; Université de Liège - ULiège > GIGA > GIGA Molecular Biology of Diseases ; Université de Liège - ULiège > Département des sciences de la vie
Lassance, Jean-Marc ; Université de Liège - ULiège > Département de gestion vétérinaire des Ressources Animales (DRA) > Génomique animale
Wang, Hong-Lei
Zhao, Cheng-Hua
Piskur, Jure
Johansson, Tomas
Lofstedt, Christer
Langue du document :
Anglais
Titre :
Elucidation of the sex-pheromone biosynthesis producing 5,7-dodecadienes in Dendrolimus punctatus (Lepidoptera: Lasiocampidae) reveals Delta 11- and Delta 9-desaturases with unusual catalytic properties.
Altschul S.F., Madden T.L., Schäffer A.A., Zhang J., Zhang Z., Miller W., and Lipman D.J. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 25 (1997) 3389-3402
Ando T., Vu H.M., Yoshida S., Takahashi N., Tatsuki S., Katagiri K., Yamane A., and Ikeda T. (5Z,7E)-5,7-dodecadien-1-ol: female sex pheromone of the pine moth Dendrolimus spectabilis Butler. Agric. Biol. Chem. 46 (1982) 709-715
Ando T., Hase T., Arima R., and Uchiyama M. Biosynthetic pathway of bombykol, the sex pheromone of the female silkworm moth. Agric. Biol. Chem. 52 (1988) 473-478
Berglund P., Holmquist M., Hedenström E., Hult K., and Högberg H.-E. 2-Methylalkanoic acids resolved by esterification catalysed by lipase from Candida rugosa: alcohol chain length and enantioselectivity. Tetrahedron Asymmetry 4 (1993) 1869-1878
Bestmann H.J., Attygalle A., Garbe W., Kern F., Martichonok V., Schäfer D., Vostrowsky O., and Hasenfus I. Chemical structure and final steps of biosynthesis of the female sex pheromone of Gastropacha quercifolia (Lepidoptera: Lasiocampidae). Insect Biochem. Mol. Biol. 23 (1993) 791-799
Bjostad L.B., and Roelofs W.L. Sex pheromone biosynthesis in Trichoplusia ni: key steps involve delta-11 desaturation and chain-shortening. Science 220 (1983) 1387-1389
Bjostad L.B., and Roelofs W.L. Sex pheromone biosynthetic precursors in Bombyx mori. Insect Biochem. 14 (1984) 275-278
Bjostad L.B., Wolf W., and Roelofs W.L. Pheromone biosynthesis in lepidopterans: desaturation and chain-shortening. In: Blomquist G.J., and Prestwich G.D. (Eds). Pheromone Biochemistry (1987), Academic Press, New York 77-120
Blomquist G.J., Jurenka R.A., Schal C., and Tittiger C. Biochemistry and molecular biology of pheromone production. In: Gilbert L.I., Iatrou K., and Gill S. (Eds). Comprehensive Molecular Insect Science (2005), Elsevier Academic San Francisco, Gilbert 705-751
Buser H.-R., Arn H., Guerin P., and Rauscher S. Determination of double bond position in mono-unsaturated acetates by mass spectrometry of dimethyl disulfide adducts. Anal. Chem. 55 (1983) 818-822
Cardé R.T., and Haynes K.F. Structure of the pheromone communication channel in moths. In: Cardé R.T., and Millar J.G. (Eds). Advances in Insect Chemical Ecology (2004), Cambridge University Press 283-332
Coyne J.A., Wicker-Thomas C., and Jallon J.-M. A gene responsible for a cuticular hydrocarbon polymorphism in Drosophila melanogaster. Genet. Res. 73 (1999) 189-203
Dallerac R., Labeur C., Jallon J.-M., Knipple D.C., Roelofs W.L., and Wicker-Thomas C. A delta9 desaturase gene with a different substrate specificity is responsible for the cuticular diene hydrocarbon polymorphism in Drosophila melanogaster. Proc. Natl. Acad. Sci. U.S.A. 97 (2000) 9449-9454
Fang N., Teal P.E.A., Doolittle R.E., and Tumlinson J.H. Biosynthesis of conjugated olefinic systems in the sex pheromone gland of female tobacco hornworm moths Manduca sexta (L.). Insect Biochem. Mol. Biol. 25 (1995) 39-48
Ferveur J.-F. Cuticular hydrocarbons: their evolution and roles in Drosophila pheromonal communication. Behav. Genet. 35 (2005) 279-295
Foster S.P., and Roelofs W.L. Biosynthesis of a monoene and a conjugated diene sex pheromone component of the lightbrown apple moth by Δ11 desaturation. Experientia 46 (1990) 269-273
Hall T.A. BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp. Ser. 41 (1999) 95-98
Hao G., Liu W., O'Connor M., and Roelofs W.L. Acyl-CoA Z9- and Z10-desaturase genes from a New Zealand leafroller moth species, Planotortrix octo. Insect Biochem. Mol. Biol. 32 (2001) 961-966
Hao G., O'Connor M., Liu W., and Roelofs W.L. Characterization of Z/E11- and Z9-desaturases from the obliquebanded leafroller moth, Choristoneura rosaceana. J. Insect Sci. 2 (2002) 26
Haynes K., McLaughlin J., Stamper S., Rucker C., Webster F., Czokajlo D., and Kirsch P. Pheromone trap for the eastern tent caterpilar moth. Environ. Entomol. 36 (2007) 1199-1205
Higgins D.J., Thompson J.D., and 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. 22 (1994) 4673-4680
Hughes A.L. The evolution of functionally novel proteins after gene duplications. Proc. R. Soc. Lond. B 256 (1994) 119-124
Jeong S.E., Rosenfield C.-L., Herrick-Marsella P., You K.M., and Knipple D.C. Multiple acyl-CoA desaturase-encoding transcripts in pheromone glands of Helicoverpa assulta, the oriental tobacco budworm. Insect Biochem. Mol. Biol. 33 (2003) 609-622
Jurenka R.A., and Roelofs W.L. Biosynthesis and endocrine regulation of fatty acid derived pheromones in moths. In: Stanley-Samuelson D.W., and Nelson D.R. (Eds). Insect Lipids: Chemistry, Biochemistry and Biology (1993), University of Nebraska Press, Lincoln, Nebraska 353-388
Klun J.A., Baranchikov Y.N., Mastro V.C., Hijji Y., Nicholson J., Ragenovich I., and Vshivkova T.A. A sex attractant for the Siberian moth Dendrolimus superans sibiricus (Lepidoptera: Lasiocampidae). J. Entomol. Sci. 35 (2000) 158-166
Knipple D.C., Rosenfield C.-L., Miller S.J., Liu W., Tang J., Ma P.W.K., and 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. 95 (1998) 15287-15292
Knipple D.C., Rosenfield C.-L., Nielsen R., You K.M., and Jeong S.E. Evolution of the integral membrane desaturase gene family in moths and flies. Genetics 162 (2002) 1737-1752
Kochansky J., Hill A., Neal J.W.J., Bentz J.-A., and Roelofs W.L. The pheromone of the eastern tent caterpillar, Malacosoma americanum (F.) (Lepidoptera: Lasiocampidae). J. Chem. Ecol. 22 (1996) 2251-2261
Kong X.-B., Zhao C.-H., and Wei G. Identification of sex pheromones of four economically important species in the genus Dendrolimus. Chin. Sci. Bull. 46 (2001) 2077-2082
Kong X.B., Zhang Z., Zhao C.-H., and Wang H.B. Female sex pheromone of the Yunnan pine caterpillar moth Dendrolimus houi: first (E,Z)-isomers in pheromone components of Dendrolimus spp. J. Chem. Ecol. 33 (2007) 1316-1327
Liénard M.A., Strandh M., Hedenström E., Johansson T., and Löfstedt C. Key biosynthetic gene subfamily recruited for pheromone production prior to the extensive radiation of Lepidoptera. BMC Evol. Biol. 8 (2008) 270
Liu W., Ma P.W.K., Marsella-Herrick P., Rosenfield C.-L., Knipple D.C., and Roelofs W.L. 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. 29 (1999) 435-443
Liu W., Jiao H., Murray N.C., O'Connor M., and 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. 99 (2002) 620-624
Liu W., Jiao H., O'Connor M., and Roelofs W.L. Moth desaturase characterized that produces both Z and E isomers of Δ11-tetradecenoic acids. Insect Biochem. Mol. Biol. 32 (2002) 1489-1495
Liu W., Rooney A.P., Xue B., and Roelofs W.L. Desaturases from the spotted fireworm moth (Choristoneura parallela) shed light on the evolutionary origins of novel moth sex pheromone desaturases. Gene 342 (2004) 303-311
Livak K., and Schmittgen T. Analysis of relative gene expression data using real-time quantitative PCR and the 2-ΔΔCt method. Methods 25 (2001) 402-408
Löfstedt C., and Bengtsson M. Sex pheromone biosynthesis of (E,E)-8,10-dodecadienol in codling moth Cydia pomonella involves E9 desaturation. J. Chem. Ecol. 14 (1988) 903-915
Lynch M., and Conery J.S. The evolutionary fate and consequences of duplicate genes. Science 290 (2000) 1151-1155
Lynch M., and Force A.G. The probability of duplicate gene preservation by subfunctionalization. Genetics 154 (2000) 459-473
Marques F.A., Millar J.G., and McElfresh S. Efficient method to locate double bond positions in conjugated trienes. J. Chromatogr. A 1048 (2004) 59-65
Martin C.E., Oh C.-S., Kandasamy P., Chellapa R., and Vemula M. Yeast desaturases. Biochem. Soc. Trans. 30 (2002) 1080-1082
Martinez T., Fabriás G., and Camps F. Sex pheromone biosynthesis pathway in Spodoptera littoralis and its activation by a neurohormone. J. Biol. Chem. 265 (1990) 1381-1387
Matoušková P., Pichová I., and Svatoš 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. 37 (2007) 601-610
Matoušková P., Luxová A., Matoušková J., Jiroš P., Svatoš A., Valterová I., and Pichova I. A Δ9 desaturase from Bombus lucorum males: investigation of the biosynthetic pathway of marking pheromones. ChemBioChem 9 (2008) 2534-2541
Michaelson L.V., Napier J.A., Lewis M., Griffiths G., Lazarus C., and Stobart A.K. Functional identification of a fatty acid delta 5 desaturase gene from Caenorhabditis elegans. FEBS Lett. 439 (1998) 215-218
Moto K., Suzuki M.G., Hull J.J., Kurata R., Takahashi S., Yamamoto M., Okano K., Imai K., Ando T., and 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. 101 (2004) 8631-8636
Navarro I., Mas E., Fabriàs G., and Camps F. Identification and biosynthesis of (E,E)-10,12-tetradecadienyl acetate in Spodoptera littoralis female sex pheromone gland. Bioorg. Med. Chem. Lett. 5 (1997) 1267-1274
Nei M., and Rooney A.P. Concerted and birth-and-death evolution of multigene families. Annu. Rev. Genet. 39 (2005) 121-152
Ono A., Imai T., Inomata S., Watanabe A., and Ando T. Biosynthetic pathway for production of a conjugated dienyl sex pheromone of a plusiinae moth, Thysanoplusia intermixta. Insect Biochem. Mol. Biol. 32 (2002) 701-708
Ohnishi A., Hull J.J., and Matsumoto S. Targeted disruption of genes in the Bombyx mori sex pheromone biosynthetic pathway. Proc. Natl. Acad. Sci. U.S.A. 103 (2006) 4398-4403
Otto S.P., and Yong P. The evolution of gene duplicates. Adv. Genet. 46 (2002) 451-483
Park H.Y., Kim M.S., Paek A., Jeong S.E., and Knipple D.C. An abundant acyl-CoA (Δ9) desaturase transcript in pheromone glands of the cabbage moth, Mamestra brassicae, encodes a catalytically inactive protein. Insect Biochem. Mol. Biol. 38 (2008) 581-595
Patel O., Fernley R., and Macreadie I. Saccharomyces cerevisiae expression vectors with thrombin-cleavable N- and C-terminal 6×(His) tags. Biotechnol. Lett. 25 (2003) 331-334
Percy-Cunningham J.E., and MacDonald J.A. Biology and ultrastructure of sex pheromone producing glands. In: Blomquist G.J., and Prestwich G.D. (Eds). Pheromone Biochemistry (1987), Academic Press, New York 27-76
Phelan P.L. Evolution of mate-signaling in moths: phylogenetic considerations and predictions from the asymmetric tracking hypothesis. In: Choe J.C., and Crespi B.J. (Eds). The Evolution of Mating Systems in Insects and Arachnids (1997), University Press, Cambridge 240-256
Riddervold M.H., Tittiger C., Blomquist G.J., and Borgeson C.E. Biochemical and molecular characterization of house cricket (Acheta domesticus, Orthoptera: Gryllidae) Δ9 desaturase. Insect Biochem. Mol. Biol. 32 (2002) 1731-1740
Rodríguez S., Clapés P., Camps F., and Fabriàs G. Stereospecificity of an enzymatic monoene 1,4-dehydrogenation reaction: conversion of (Z)-11-tetradecenoic acid into (E,E)-10,12, tetradecadienoic acid. J. Org. Chem. 67 (2002) 2228-2233
Rodríguez S., Hao G., Liu W., Piña B., Rooney A.P., Camps F., Roelofs W.L., and Fabriàs G. Expression and evolution of Δ9 and Δ11 desaturase genes in the moth Spodoptera littoralis. Insect Biochem. Mol. Biol. 34 (2004) 1315-1328
Roelofs W., and Bjostad L. Biosynthesis of Lepidopteran pheromones. Bioorg. Chem. 12 (1984) 279-298
Roelofs W.L., and Rooney A.P. Molecular genetics and evolution of pheromone biosynthesis in Lepidoptera. Proc. Natl. Acad. Sci. U.S.A. 5 (2003) 9179-9184
Roelofs W.L., Liu W., Hao G., Jiao H., Rooney A.P., and Linn C.E. Evolution of moth sex pheromones via ancestral genes. Proc. Natl. Acad. Sci. U.S.A. 99 (2002) 13621-13626
Rosenfield C.-L., You K.M., Herrick-Marsella P., Roelofs W.L., and 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. 31 (2001) 949-964
Rotundo G., Germinara G.S., and de Cristofaro A. Chemical, electrophysiological, and behavioral investigations on the sex pheromone of lackey moth, Malacosoma neustrium. J. Chem. Ecol. 30 (2004) 2057-2069
Schmidt B., Roland J., and Wakarchuk D. Evaluation of synthetic pheromones for monitoring forest tent caterpillar (Lepidoptera: Lasiocampidae) populations. Environ. Entomol. 32 (2003) 214-219
Schneiter R., Tatzer V., Gogg G., Leitner E., and Kohlwein S.D. Elo1-dependent carboxy-terminal elongation of C14:1Delta(9) to C16:1Delta(11) fatty acids in Saccharomyces cerevisiae. J. Bacteriol. 182 (2000) 3655-3660
Serra M., Piña B., Bujons J., Camps F., and Fabriàs G. Biosynthesis of 10,12-dienoic fatty acids by a bifunctional Δ11 desaturase in Spodoptera littoralis. Insect Biochem. Mol. Biol. 36 (2006) 634-641
Serra M., Piña B., Abad J.L., Camps F., and Fabriàs G. A multifunctional desaturase involved in the biosynthesis of the processionary moth sex pheromone. Proc. Natl. Acad. Sci. U.S.A. 104 (2007) 16444-16449
Shanklin J., Whittle E., and 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 33 (1994) 12787-12794
Shanklin J., and Cahoon E.B. Desaturation and related modifications of fatty acids. Annu. Rev. Plant Physiol. 49 (1998) 611-641
Sperling P., Ternes P., Zank T.K., and Heinz E. The evolution of desaturases. Prostaglandins Leukot. Essent. Fatty Acids 68 (2003) 73-95
Stuckey J.E., McDonough V.M., and Martin C.E. The OLE1 gene of Saccharomyces cerevisiae encodes the Δ9 fatty acid desaturase and can be functionally replaced by the rat stearoyl-CoA desaturase gene. J. Biol. Chem. 265 (1990) 20144-20149
Tamaki Y. Sex pheromones. Comprehensive Insect Physiology, Biochemistry and Pharmacology vol. 9 (1985), Pergamon Press, Oxford 145-191
Tamura K., Nei M., and Kumar S. MEGA4: molecular evolutionary genetics analysis software version 4.0. Mol. Biol. Evol. 24 (2007) 1596-1599
Tillman J.A., Seybold S.J., Jurenka R.A., and Blomquist G.J. Insect pheromones - an overview of biosynthesis and endocrine regulation. Insect Biochem. Mol. Biol. 29 (1999) 481-514
Tocher D.R., Leaver M.J., and Hodgson P.A. Recent advances in the biochemistry and molecular biology of fatty acyl desaturases. Prog. Lipid Res. 37 (1998) 73-117
Tsfadia O., Azrielli A., Falach L., Zada A., Roelofs W., and Rafaeli A. Pheromone biosynthetic pathways: PBAN-regulated rate-limiting steps and differential expression of desaturase genes in moth species. Insect Biochem. Mol. Biol. 38 (2008) 552-567
Underhill E.W., Chisholm M.D., and Steck W. (E)-5,(Z)-7-dodecadienal, a sex pheromone component of the western tent caterpillar, Malacosoma californicum (Lepidoptera, Lasiocampidae). Can. Entomol. 112 (1980) 629-631
Wyatt T.D. Pheromones and Animal Behaviour. Communication by Smell and Taste (2003), Cambridge University Press p. 391
Yamaoka R., Taniguchi Y., and Hayashiya K. Bombykol biosynthesis from deuterium-labelled (Z)-11-hexadecenoic acid. Experientia 40 (1984) 80-81
Zhao C.-H., Li Q., Guo X.-Y., and Wang X.-Y. New components of sex pheromone in the pine caterpillar moth, Dendrolimus punctatus: identification of chemical structures and field tests. Acta Entomol. Sin. 36 (1993) 247-250
Zhao C.-H., Adlof R.O., and Löfstedt C. Sex pheromone biosynthesis in the pine caterpillar moth, Dendrolimus punctatus (Lepidoptera: Lasiocampidae): pathways leading to Z5-monoene and 5,7-conjugated diene components. Insect Biochem. Mol. Biol. 34 (2004) 261-271
Zhou X.-R., Horne I., Damcevski K., Haritos V., Green A., and Singh S. Isolation and functional characterization of two independently-evolved fatty acid Δ12-desaturase genes from insects. Insect Mol. Biol. 17 (2008) 667-676
