Skip to main content
PMC home page
Genetics logoLink to Genetics
. 2002 Dec;162(4):1737–1752. doi: 10.1093/genetics/162.4.1737

Evolution of the integral membrane desaturase gene family in moths and flies.

Douglas C Knipple 1, Claire-Lise Rosenfield 1, Rasmus Nielsen 1, Kyung Man You 1, Seong Eun Jeong 1
PMCID: PMC1462379  PMID: 12524345

Abstract

Lepidopteran insects use sex pheromones derived from fatty acids in their species-specific mate recognition system. Desaturases play a particularly prominent role in the generation of structural diversity in lepidopteran pheromone biosynthesis as a result of the diverse enzymatic properties they have evolved. These enzymes are homologous to the integral membrane desaturases, which play a primary role in cold adaptation in eukaryotic cells. In this investigation, we screened for desaturase-encoding sequences in pheromone glands of adult females of eight lepidopteran species. We found, on average, six unique desaturase-encoding sequences in moth pheromone glands, the same number as is found in the genome database of the fly, Drosophila melanogaster, vs. only one to three in other characterized eukaryotic genomes. The latter observation suggests the expansion of this gene family in insects before the divergence of lepidopteran and dipteran lineages. We present the inferred homology relationships among these sequences, analyze nonsynonymous and synonymous substitution rates for evidence of positive selection, identify sequence and structural correlates of three lineages containing characterized enzymatically distinct desaturases, and discuss the evolution of this sequence family in insects.

Full Text

The Full Text of this article is available as a PDF (1.5 MB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Altschul S. F., Madden T. L., Schäffer 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 Sep 1;25(17):3389–3402. doi: 10.1093/nar/25.17.3389. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Bjostad L. B., Roelofs W. L. Sex Pheromone Biosynthesis in Trichoplusia ni: Key Steps Involve Delta-11 Desaturation and Chain-Shortening. Science. 1983 Jun 24;220(4604):1387–1389. doi: 10.1126/science.220.4604.1387. [DOI] [PubMed] [Google Scholar]
  3. Bordo D., Argos P. Suggestions for "safe" residue substitutions in site-directed mutagenesis. J Mol Biol. 1991 Feb 20;217(4):721–729. doi: 10.1016/0022-2836(91)90528-e. [DOI] [PubMed] [Google Scholar]
  4. Coyne J. A., Oyama R. Localization of pheromonal sexual dimorphism in Drosophila melanogaster and its effect on sexual isolation. Proc Natl Acad Sci U S A. 1995 Oct 10;92(21):9505–9509. doi: 10.1073/pnas.92.21.9505. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Coyne J. A., Wicker-Thomas C., Jallon J. M. A gene responsible for a cuticular hydrocarbon polymorphism in Drosophila melanogaster. Genet Res. 1999 Jun;73(3):189–203. doi: 10.1017/s0016672398003723. [DOI] [PubMed] [Google Scholar]
  6. Dallerac R., Labeur C., Jallon J. M., Knipple D. C., Roelofs W. L., Wicker-Thomas C. A delta 9 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. 2000 Aug 15;97(17):9449–9454. doi: 10.1073/pnas.150243997. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Force A., Lynch M., Pickett F. B., Amores A., Yan Y. L., Postlethwait J. Preservation of duplicate genes by complementary, degenerative mutations. Genetics. 1999 Apr;151(4):1531–1545. doi: 10.1093/genetics/151.4.1531. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Hazel J. R., Williams E. E. The role of alterations in membrane lipid composition in enabling physiological adaptation of organisms to their physical environment. Prog Lipid Res. 1990;29(3):167–227. doi: 10.1016/0163-7827(90)90002-3. [DOI] [PubMed] [Google Scholar]
  9. Higgins D. G., Thompson J. D., Gibson T. J. Using CLUSTAL for multiple sequence alignments. Methods Enzymol. 1996;266:383–402. doi: 10.1016/s0076-6879(96)66024-8. [DOI] [PubMed] [Google Scholar]
  10. Hirokawa T., Boon-Chieng S., Mitaku S. SOSUI: classification and secondary structure prediction system for membrane proteins. Bioinformatics. 1998;14(4):378–379. doi: 10.1093/bioinformatics/14.4.378. [DOI] [PubMed] [Google Scholar]
  11. Jallon J. -M., Kunesch G., Bricard L., Pennanec'h M. Incorporation of fatty acids into cuticular hydrocarbons of male and female Drosophila melanogaster. J Insect Physiol. 1997 Nov;43(12):1111–1116. doi: 10.1016/s0022-1910(97)00082-6. [DOI] [PubMed] [Google Scholar]
  12. Jeong S. E., Lee Y., Hwang J. H., Knipple D. C. Effects of the sap of the common oleander Nerium indicum (Apocyanaceae) on male fertility and spermatogenesis in the oriental tobacco budworm Helicoverpa assulta (Lepidoptera, Noctuidae). J Exp Biol. 2001 Nov;204(Pt 22):3935–3942. doi: 10.1242/jeb.204.22.3935. [DOI] [PubMed] [Google Scholar]
  13. Jeong S. E., Lee Y., Hwang J. H., Knipple D. C. Effects of the sap of the common oleander Nerium indicum (Apocyanaceae) on male fertility and spermatogenesis in the oriental tobacco budworm Helicoverpa assulta (Lepidoptera, Noctuidae). J Exp Biol. 2001 Nov;204(Pt 22):3935–3942. doi: 10.1242/jeb.204.22.3935. [DOI] [PubMed] [Google Scholar]
  14. Jurenka R. A. Biosynthetic pathway for producing the sex pheromone component (Z,E)-9,12-tetradecadienyl acetate in moths involves a delta 12 desaturase. Cell Mol Life Sci. 1997 Jun;53(6):501–505. doi: 10.1007/s000180050062. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Knipple D. C., Rosenfield C. L., Miller S. J., Liu W., Tang J., Ma P. W., Roelofs W. L. Cloning and functional expression of a cDNA encoding a pheromone gland-specific acyl-CoA Delta11-desaturase of the cabbage looper moth, Trichoplusia ni. Proc Natl Acad Sci U S A. 1998 Dec 22;95(26):15287–15292. doi: 10.1073/pnas.95.26.15287. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Kyte J., Doolittle R. F. A simple method for displaying the hydropathic character of a protein. J Mol Biol. 1982 May 5;157(1):105–132. doi: 10.1016/0022-2836(82)90515-0. [DOI] [PubMed] [Google Scholar]
  17. Lichtarge O., Bourne H. R., Cohen F. E. An evolutionary trace method defines binding surfaces common to protein families. J Mol Biol. 1996 Mar 29;257(2):342–358. doi: 10.1006/jmbi.1996.0167. [DOI] [PubMed] [Google Scholar]
  18. Liu W., Ma P. W., Marsella-Herrick P., Rosenfield C. L., Knipple D. C., Roelofs W. Cloning and functional expression of a cDNA encoding a metabolic acyl-CoA delta 9-desaturase of the cabbage looper moth, Trichoplusia ni. Insect Biochem Mol Biol. 1999 May;29(5):435–443. doi: 10.1016/s0965-1748(99)00020-x. [DOI] [PubMed] [Google Scholar]
  19. Liu Weitian, Jiao Hongmei, Murray Nancy C., O'Connor Marion, Roelofs Wendell 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 Jan 22;99(2):620–624. doi: 10.1073/pnas.221601498. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Mitaku S., Hirokawa T. Physicochemical factors for discriminating between soluble and membrane proteins: hydrophobicity of helical segments and protein length. Protein Eng. 1999 Nov;12(11):953–957. doi: 10.1093/protein/12.11.953. [DOI] [PubMed] [Google Scholar]
  21. Mitaku S., Ono M., Hirokawa T., Boon-Chieng S., Sonoyama M. Proportion of membrane proteins in proteomes of 15 single-cell organisms analyzed by the SOSUI prediction system. Biophys Chem. 1999 Dec 13;82(2-3):165–171. doi: 10.1016/s0301-4622(99)00116-7. [DOI] [PubMed] [Google Scholar]
  22. Nielsen R., Yang Z. Likelihood models for detecting positively selected amino acid sites and applications to the HIV-1 envelope gene. Genetics. 1998 Mar;148(3):929–936. doi: 10.1093/genetics/148.3.929. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. 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 Sep;31(10):949–964. doi: 10.1016/s0965-1748(01)00043-1. [DOI] [PubMed] [Google Scholar]
  24. Saitou N., Nei M. The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol. 1987 Jul;4(4):406–425. doi: 10.1093/oxfordjournals.molbev.a040454. [DOI] [PubMed] [Google Scholar]
  25. Sanger F., Nicklen S., Coulson A. R. DNA sequencing with chain-terminating inhibitors. Proc Natl Acad Sci U S A. 1977 Dec;74(12):5463–5467. doi: 10.1073/pnas.74.12.5463. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Shanklin John, Cahoon Edgar B. DESATURATION AND RELATED MODIFICATIONS OF FATTY ACIDS1. Annu Rev Plant Physiol Plant Mol Biol. 1998 Jun;49(NaN):611–641. doi: 10.1146/annurev.arplant.49.1.611. [DOI] [PubMed] [Google Scholar]
  27. Sonnhammer E. L., von Heijne G., Krogh A. A hidden Markov model for predicting transmembrane helices in protein sequences. Proc Int Conf Intell Syst Mol Biol. 1998;6:175–182. [PubMed] [Google Scholar]
  28. Takahashi A., Tsaur S. C., Coyne J. A., Wu C. I. The nucleotide changes governing cuticular hydrocarbon variation and their evolution in Drosophila melanogaster. Proc Natl Acad Sci U S A. 2001 Mar 20;98(7):3920–3925. doi: 10.1073/pnas.061465098. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Tiku P. E., Gracey A. Y., Macartney A. I., Beynon R. J., Cossins A. R. Cold-induced expression of delta 9-desaturase in carp by transcriptional and posttranslational mechanisms. Science. 1996 Feb 9;271(5250):815–818. doi: 10.1126/science.271.5250.815. [DOI] [PubMed] [Google Scholar]
  30. Tillman J. A., Seybold S. J., Jurenka R. A., Blomquist G. J. Insect pheromones--an overview of biosynthesis and endocrine regulation. Insect Biochem Mol Biol. 1999 Jun;29(6):481–514. doi: 10.1016/s0965-1748(99)00016-8. [DOI] [PubMed] [Google Scholar]
  31. Tusnády G. E., Simon I. Principles governing amino acid composition of integral membrane proteins: application to topology prediction. J Mol Biol. 1998 Oct 23;283(2):489–506. doi: 10.1006/jmbi.1998.2107. [DOI] [PubMed] [Google Scholar]
  32. Tusnády G. E., Simon I. The HMMTOP transmembrane topology prediction server. Bioinformatics. 2001 Sep;17(9):849–850. doi: 10.1093/bioinformatics/17.9.849. [DOI] [PubMed] [Google Scholar]
  33. Vigh L., Los D. A., Horváth I., Murata N. The primary signal in the biological perception of temperature: Pd-catalyzed hydrogenation of membrane lipids stimulated the expression of the desA gene in Synechocystis PCC6803. Proc Natl Acad Sci U S A. 1993 Oct 1;90(19):9090–9094. doi: 10.1073/pnas.90.19.9090. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Wicker-Thomas C., Henriet C., Dallerac R. Partial characterization of a fatty acid desaturase gene in Drosophila melanogaster. Insect Biochem Mol Biol. 1997 Nov;27(11):963–972. doi: 10.1016/s0965-1748(97)00077-5. [DOI] [PubMed] [Google Scholar]
  35. Yang Z., Nielsen R., Goldman N., Pedersen A. M. Codon-substitution models for heterogeneous selection pressure at amino acid sites. Genetics. 2000 May;155(1):431–449. doi: 10.1093/genetics/155.1.431. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Yang Z., Nielsen R. Synonymous and nonsynonymous rate variation in nuclear genes of mammals. J Mol Evol. 1998 Apr;46(4):409–418. doi: 10.1007/pl00006320. [DOI] [PubMed] [Google Scholar]
  37. Yang Ziheng, Nielsen Rasmus. Codon-substitution models for detecting molecular adaptation at individual sites along specific lineages. Mol Biol Evol. 2002 Jun;19(6):908–917. doi: 10.1093/oxfordjournals.molbev.a004148. [DOI] [PubMed] [Google Scholar]
  38. Yoshiga T., Okano K., Mita K., Shimada T., Matsumoto S. cDNA cloning of acyl-CoA desaturase homologs in the silkworm, Bombyx mori. Gene. 2000 Apr 4;246(1-2):339–345. doi: 10.1016/s0378-1119(00)00047-0. [DOI] [PubMed] [Google Scholar]

Articles from Genetics are provided here courtesy of Oxford University Press

RESOURCES