Sex Attractants; Oxidoreductases; Amino Acid Sequence; Animals; Female; Molecular Sequence Data; Moths/enzymology; Oxidoreductases/metabolism; Sequence Alignment; Sex Attractants/biosynthesis; Sex Attractants/chemistry; Biochemistry, Genetics and Molecular Biology (all); Agricultural and Biological Sciences (all); Multidisciplinary
Abstract :
[en] [en] BACKGROUND: Sex pheromones are essential in moth mate communication. Information on pheromone biosynthetic genes and enzymes is needed to comprehend the mechanisms that contribute to specificity of pheromone signals. Most heliothine moths use sex pheromones with (Z)-11-hexadecenal as the major component in combination with minor fatty aldehydes and alcohols. In this study we focus on four closely related species, Heliothis virescens, Heliothis subflexa, Helicoverpa armigera and Helicoverpa assulta, which use (Z)-11-hexadecenal, (Z)-9-tetradecanal, and (Z)-9-hexadecenal in different ratios in their pheromone blend. The components are produced from saturated fatty acid precursors by desaturation, β-oxidation, reduction and oxidation.
RESULTS: We analyzed the composition of fatty acyl pheromone precursors and correlated it to the pheromone composition. Next, we investigated whether the downstream fatty-acyl reduction step modulates the ratio of alcohol intermediates before the final oxidation step. By isolating and functionally characterizing the Fatty Acyl Reductase (pgFAR) from each species we found that the pgFARs were active on a broad set of C8 to C16 fatty acyl substrates including the key pheromone precursors, Z9-14, Z9-16 and Z11-16:acyls. When presenting the three precursors in equal ratios to yeast cultures expressing any of the four pgFARs, all reduced (Z)-9-tetradecenoate preferentially over (Z)-11-hexadecenoate, and the latter over (Z)-9-hexadecenoate. Finally, when manipulating the precursor ratios in vitro, we found that the pgFARs display small differences in the biochemical activity on various substrates.
CONCLUSIONS: We conclude that a pgFAR with broad specificity is involved in heliothine moth pheromone biosynthesis, functioning as a semi-selective funnel that produces species-specific alcohol product ratios depending on the fatty-acyl precursor ratio in the pheromone gland. This study further supports the key role of these in pheromone biosynthesis and emphasizes the interplay between the pheromone fatty acyl precursors and the Lepidoptera specific pgFARs in shaping the pheromone composition.
Disciplines :
Biochemistry, biophysics & molecular biology
Author, co-author :
Hagström, Asa K; Pheromone group, Department of Biology, Lund University, Lund, Sweden. asa.hagstrom@biol.lu.se
Lienard, Marjorie ; Université de Liège - ULiège > GIGA > GIGA Molecular Biology of Diseases ; Pheromone group, Department of Biology, Lund University, Lund, Sweden
Groot, Astrid T; Institute for Biodiversity and Ecosystem Dynamics, University of Amsterdam, Amsterdam, Netherlands ; Department of Entomology, Max Planck Institute for Chemical Ecology, Jena, Germany
Hedenström, Erik; Department of Natural Sciences, Engineering and Mathematics, Mid Sweden University, Sundsvall, Sweden
Löfstedt, Christer; Pheromone group, Department of Biology, Lund University, Lund, Sweden
Language :
English
Title :
Semi-selective fatty acyl reductases from four heliothine moths influence the specific pheromone composition.
Bardwell L, Cook JG, Inouye CJ, Thorner J, (1994) Signal Propagation and Regulation in the Mating Pheromone Response Pathway of the Yeast Saccharomyces cerevisiae. Dev Biol 166: 363-379.
Wyatt TD, (2003) Pheromones and animal behaviour: Communication by smell and taste Cambridge Cambridge University Press.
Butenandt A, Beckmann R, Stamm D, Hecker E, (1959) Über den Sexuallockstoff den Seidenspinners Bombyx mori. Reindarstellung und Konstitution. Z Naturforsch 14b: 283-284.
Tillman JA, Seybold SJ, Jurenka RA, Blomquist GJ, (1999) Insect pheromones - an overview of biosynthesis and endocrine regulation. Insect Biochem Molec 29: 481-514.
Knipple DC, Rosenfield CL, Nielsen R, You KM, Jeong SE, (2002) Evolution of the Integral Membrane Desaturase Gene Family in Moths and Flies. Genetics 162: 1737-1752.
Roelofs WL, Liu W, Hao G, Jiao H, Rooney AP, et al. (2002) Evolution of moth sex pheromones via ancestral genes. Proc Natl Acad Sci U S A 99: 13621-13626.
Moto K, Suzuki MG, Hull JJ, Kurata R, Takahashi S, et al. (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: 8631-8636.
Serra M, Pina B, Bujons J, Camps F, Fabrias G, (2006) Biosynthesis of 10,12-dienoic fatty acids by a bifunctional D11 desaturase in Spodoptera littoralis. Insect Biochem Molec 36: 634-641.
Liénard MA, Strandh M, Hedenström E, Johansson T, Löfstedt C, (2008) Key biosynthetic gene subfamily recruited for pheromone production prior to the extensive radiation of Lepidoptera. BMC Evol Biol 8: 1-15.
Wang H-L, Liénard MA, Zhao C-H, Wang C-Z, Löfstedt C, (2010) Neofunctionalization in an ancestral insect desaturase lineage led to rare Δ6 pheromone signals in the Chinese tussah silkworm. Insect Biochem Molec 40: 742-751.
Moto K, Yoshiga T, Yamamoto M, Takahashi S, Okano K, et al. (2003) Pheromone gland-specific fatty-acyl reductase of the silkmoth, Bombyx mori. Proc Natl Acad Sci U S A 100: 9156-9161.
Antony B, Fujii T, Moto K, Matsumoto S, Fukuzawa M, et al. (2008) Pheromone-gland-specific fatty-acyl reductase in the adzuki bean borer, Ostrinia scapulalis (Lepidoptera: Crambidae). Insect Biochem Molec 39: 90-95.
Lassance JM, Groot AT, Liénard MA, Anthony B, Bogwardt C, et al. (2010) Allelic variation in a fatty-acyl reductase gene causes divergence in moth sex pheromones. Nature 466: 486-491.
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: 10955-10960.
Cho S, Mitchell A, Mitter C, Regier J, Matthews M, et al. (2008) Molecular phylogenetics of heliothine moths (Lepidoptera: Noctuidae: Heliothinae), with comments on the evolution of host range and pest status. Syst Entomol 33: 581-594.
Teal PEA, Tumlinson JH, Heath RR, (1986) Chemical and behavioral analyses of volatile sex pheromone components released by calling Heliothis virescens (F.) females (Lepidoptera: Noctuidae). J Chem Ecol 12: 107-126.
Klun JA, Bierl-Leonhardt BA, Plimmer JR, Sparks AN, Primani M, et al. (1980) Sex pheromone chemistry of the female Tobacco budworm moth, Heliothis virescens. J Chem Ecol 6: 177-183.
Klun JA, Leonhardt BA, Lopez JD, Lachance LE, (1982) Female Heliothis subflexa (Lepidoptera: Noctuidae) Sex Pheromone: Chemistry and Congeneric Comparisons. Environ Entomol 11: 1084-1090.
Teal PEA, Heath RR, Tumlinson JH, McLaughlin JR, (1981) Identification of a sex pheromone of Heliothis subflexa (GN.) (Lepidoptera: Noctuidae) and field trapping studies using different blends of components. J Chem Ecol 7: 1011-1022.
Wang H-L, Zhao C-H, Wang C-Z, (2005) Comparative study of sex pheromone composition and biosynthesis in Helicoverpa armigera, H. assulta and their hybrid. Insect Biochem Molec 35: 575-583.
Choi MY, Groot AT, Jurenka R, (2005) Pheromone Biosynthetic Pathway in the Moths Heliothis subflexa and Heliothis virescens. Arch Insect Biochem 59: 53-58.
Liénard MA, Löfstedt C, (2010) Functional flexibility as a prelude to signal diversity? Comm Int Biol 3: 586-588.
Roelofs WL, Rooney AP, (2003) Molecular genetics and evolution of pheromone biosynthesis in Lepidoptera. Proc Natl Acad Sci U S A 100: 9179-9184.
Teal PEA, Tumlinson JH, (1986) Terminal steps in pheromone biosynthesis by Heliothis virescens and H. zea. J Chem Ecol 12: 353-366.
Wang H-L, Ming Q-L, Zhao C-H, Wang C-Z, (2008) Genetic basis of sex pheromone blend difference between Helicoverpa armigera (Hubner) and Helicoverpa assulta (Guenee)(Lepidoptera: Noctuidae). J Insect Physiol 54: 813-817.
Ahn SJ, Choi MY, Boo KS, (2002) Mating effect on sex pheromone production of the Oriental tobacco budworm, Helicoverpa assulta. J Asia Pac Entomol 5: 43-48.
Foster SP, (2005) Lipid Analysis of the Sex Pheromone Gland of the Moth Heliothis virescens. Arch Insect Biochem 59: 80-90.
Vogel H, Heidel AJ, Heckel DG, Groot AT, (2010) Transcriptome analysis of the sex pheromone gland of the noctuid moth Heliothis virescens. BMC Genomics 11: 1-21.
Hall, (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp 41: 95-98.
Altschul SF, Madden TL, Schäffer AA, Zhang J, Zhang Z, et al. (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25: 3389-3402.
Chenna R, Sugawara H, Koike T, Lopez R, Gibson TJ, et al. (2003) Multiple sequence alignment with the Clustal series of programs. Nucleic Acids Res 31: 3497-500.
Tamura K, Dudley J, Nei M, Kumar S, (2007) MEGA4: Molecular evolutionary genetics analysis (MEGA) software version 4.0. Mol Biol Evol 24: 1596-1599.
Groot AT, Fan Y-L, Brownie C, Jurenka RA, Gould F, et al. (2005) Effect of PBAN on pheromone production by mated Heliothis virescens and Heliothis subflexa females. J Chem Ecol 31: 15-28.
Sonnhammer EL, Eddy SR, Durbin R, (1997) Pfam: a comprehensive database of protein domain families based on seed alignments. Proteins 28: 405-420.
Rafaeli A, (2005) Mechanisms involved in the control of pheromone production in female moths: recent developments. Entomol Ex App 115: 7-15.
Wanders RJA, Waterham HR, (2006) Biochemistry of Mammalian Peroxisomes Revisited. Annu Rev Biochem 75: 295-332.
Zhu JW, Zhao CH, Bengtsson M, Löfstedt C, (1996) Reductase specificity and the ratio regulation of E/Z isomers in the pheromone biosynthesis of the European corn borer, Ostrinia nubilalis (Lepidoptera: Pyralidae). Insect Biochem Mol Biol 26: 171-176.
Cheng JB, Russell DW, (2004) Identification of two Fatty Acyl-CoenzymeA Reductases with different substrate specificities and tissue distributions. J Biol Chem 279: 37789-37797.
Pi N, Leary JA, (2004) Determination of enzyme/substrate specificity constants using a multiple substrate ESI-MS assay. J Am Soc Mass Spectrom 15: 233-243.
Liesener A, Perchuc A-M, Schöni R, Wilmer M, Karst U, (2005) Screening for proteolytic activities in snake venom by means of a multiplexing electrospray ionization mass spectrometry assay scheme. Rap Comm Mass Spectrom 19: 2923-2928.
Bouwman J, van Eunen K, Tuzun I, Postmus J, Canelas A, et al. (2006) Standardization and 'In vivo'-like enzyme activity measurements in yeast. ESCEC, Rüdesheim, Rhein, Germany.
Berg JM, Tymoczko JL, Stryer L, (2002) Enzymes: Basic Concepts and Kinetics, In: Julet M, Moran S, editors. Biochemistry New York W H Freeman pp. 209-219.
Schellenberger V, Siegel RA, Rutter WJ, (1993) Analysis of enzyme specificity by multiple substrate kinetics. Biochemistry 32: 4344-8.
Beaulieu L, Groleau D, Miguez CB, Jetté JF, Aomari H, et al. (2005) Production of pediocin PA-1 in the methylotrophic yeast Pichia pastoris reveals unexpected inhibition of its biological activity due to the presence of collagen-like material. Prot Expr Pur 43: 111-125.
Groot AT, Estock ML, Hamilton J, Santangelso RG, Schal C, et al. (2009) QTL analysis of sex pheromone blend differences between two closely related moths: Insights into divergence in biosynthetic pathways. Insect Biochem Molec 39: 568-577.
Scheck AL, Groot AT, Ward CM, Gemeno C, Wang J, et al. (2006) Genetics of sex pheromone blend differenced between Heliothis virescens and Heliothis subflexa: a chromosome mapping approach. J Evol Biol 19: 600-617.