A family of genes clustered at the Triplo-lethal locus of Drosophila melanogaster has an unusual evolutionary history and significant synteny with Anopheles gambiae (original) (raw)

Abstract

Within the unique Triplo-lethal region (Tpl) of the Drosophila melanogaster genome we have found a cluster of 20 genes encoding a novel family of proteins. This family is also present in the Anopheles gambiae genome and displays remarkable synteny and sequence conservation with the Drosophila cluster. The family is also present in the sequenced genome of D. pseudoobscura, and homologs have been found in Aedes aegypti mosquitoes and in four other insect orders, but it is not present in the sequenced genome of any noninsect species. Phylogenetic analysis suggests that the cluster evolved prior to the divergence of Drosophila and Anopheles (250 MYA) and has been highly conserved since. The ratio of synonymous to nonsynonymous substitutions and the high codon bias suggest that there has been selection on this family both for expression level and function. We hypothesize that this gene family is Tpl, name it the Osiris family, and consider possible functions. We also predict that this family of proteins, due to the unique dosage sensitivity and the lack of homologs in noninsect species, would be a good target for genetic engineering or novel insecticides.

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  1. Adams M. D., Celniker S. E., Holt R. A., Evans C. A., Gocayne J. D., Amanatides P. G., Scherer S. E., Li P. W., Hoskins R. A., Galle R. F. The genome sequence of Drosophila melanogaster. Science. 2000 Mar 24;287(5461):2185–2195. doi: 10.1126/science.287.5461.2185. [DOI] [PubMed] [Google Scholar]
  2. Akashi H. Synonymous codon usage in Drosophila melanogaster: natural selection and translational accuracy. Genetics. 1994 Mar;136(3):927–935. doi: 10.1093/genetics/136.3.927. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Altschul S. F., Gish W., Miller W., Myers E. W., Lipman D. J. Basic local alignment search tool. J Mol Biol. 1990 Oct 5;215(3):403–410. doi: 10.1016/S0022-2836(05)80360-2. [DOI] [PubMed] [Google Scholar]
  4. 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]
  5. Arbeitman Michelle N., Furlong Eileen E. M., Imam Farhad, Johnson Eric, Null Brian H., Baker Bruce S., Krasnow Mark A., Scott Matthew P., Davis Ronald W., White Kevin P. Gene expression during the life cycle of Drosophila melanogaster. Science. 2002 Sep 27;297(5590):2270–2275. doi: 10.1126/science.1072152. [DOI] [PubMed] [Google Scholar]
  6. Bonifacino J. S., Dell'Angelica E. C. Molecular bases for the recognition of tyrosine-based sorting signals. J Cell Biol. 1999 May 31;145(5):923–926. doi: 10.1083/jcb.145.5.923. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Cooley L., Kelley R., Spradling A. Insertional mutagenesis of the Drosophila genome with single P elements. Science. 1988 Mar 4;239(4844):1121–1128. doi: 10.1126/science.2830671. [DOI] [PubMed] [Google Scholar]
  8. Denell R. E. The genetic analysis of a uniquely dose-sensitive chromosomal region of Drosophila melanogaster. Genetics. 1976 Oct;84(2):193–210. doi: 10.1093/genetics/84.2.193. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Dorer D. R., Cadden M. A., Gordesky-Gold B., Harries G., Christensen A. C. Suppression of a lethal trisomic phenotype in Drosophila melanogaster by increased dosage of an unlinked locus. Genetics. 1993 May;134(1):243–249. doi: 10.1093/genetics/134.1.243. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Dorer D. R., Christensen A. C., Johnson D. H. A novel RNA helicase gene tightly linked to the Triplo-lethal locus of Drosophila. Nucleic Acids Res. 1990 Sep 25;18(18):5489–5494. doi: 10.1093/nar/18.18.5489. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Dorer D. R., Christensen A. C. The unusual spectrum of mutations induced by hybrid dysgenesis at the Triplo-lethal locus of Drosophila melanogaster. Genetics. 1990 Aug;125(4):795–801. doi: 10.1093/genetics/125.4.795. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Duret Laurent. Evolution of synonymous codon usage in metazoans. Curr Opin Genet Dev. 2002 Dec;12(6):640–649. doi: 10.1016/s0959-437x(02)00353-2. [DOI] [PubMed] [Google Scholar]
  13. Eissenberg Joel C., Ma Jiyan, Gerber Mark A., Christensen Alan, Kennison James A., Shilatifard Ali. dELL is an essential RNA polymerase II elongation factor with a general role in development. Proc Natl Acad Sci U S A. 2002 Jul 2;99(15):9894–9899. doi: 10.1073/pnas.152193699. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Emanuelsson O., Nielsen H., Brunak S., von Heijne G. Predicting subcellular localization of proteins based on their N-terminal amino acid sequence. J Mol Biol. 2000 Jul 21;300(4):1005–1016. doi: 10.1006/jmbi.2000.3903. [DOI] [PubMed] [Google Scholar]
  15. Goder V., Spiess M. Topogenesis of membrane proteins: determinants and dynamics. FEBS Lett. 2001 Aug 31;504(3):87–93. doi: 10.1016/s0014-5793(01)02712-0. [DOI] [PubMed] [Google Scholar]
  16. Hoffman S., Edelman G. M. Kinetics of homophilic binding by embryonic and adult forms of the neural cell adhesion molecule. Proc Natl Acad Sci U S A. 1983 Sep;80(18):5762–5766. doi: 10.1073/pnas.80.18.5762. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Holt Robert A., Subramanian G. Mani, Halpern Aaron, Sutton Granger G., Charlab Rosane, Nusskern Deborah R., Wincker Patrick, Clark Andrew G., Ribeiro José M. C., Wides Ron. The genome sequence of the malaria mosquito Anopheles gambiae. Science. 2002 Oct 4;298(5591):129–149. doi: 10.1126/science.1076181. [DOI] [PubMed] [Google Scholar]
  18. Hurst Laurence D., Williams Elizabeth J. B., Pál Csaba. Natural selection promotes the conservation of linkage of co-expressed genes. Trends Genet. 2002 Dec;18(12):604–606. doi: 10.1016/s0168-9525(02)02813-5. [DOI] [PubMed] [Google Scholar]
  19. Jones D. T., Taylor W. R., Thornton J. M. The rapid generation of mutation data matrices from protein sequences. Comput Appl Biosci. 1992 Jun;8(3):275–282. doi: 10.1093/bioinformatics/8.3.275. [DOI] [PubMed] [Google Scholar]
  20. Keenan Curtis Kelly, Kane Patricia M. Novel vacuolar H+-ATPase complexes resulting from overproduction of Vma5p and Vma13p. J Biol Chem. 2001 Nov 20;277(4):2716–2724. doi: 10.1074/jbc.M107777200. [DOI] [PubMed] [Google Scholar]
  21. Keppy D. O., Denell R. E. A mutational analysis of the triplo-lethal region of Drosophila melanogaster. Genetics. 1979 Mar;91(3):421–441. doi: 10.1093/genetics/91.3.421. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Krebs Kendall C., Brzoza Kristina L., Lan Que. Use of subtracted libraries and macroarray to isolate developmentally specific genes from the mosquito, Aedes aegypti. Insect Biochem Mol Biol. 2002 Dec;32(12):1757–1767. doi: 10.1016/s0965-1748(02)00116-9. [DOI] [PubMed] [Google Scholar]
  23. Krogh A., Larsson B., von Heijne G., Sonnhammer E. L. Predicting transmembrane protein topology with a hidden Markov model: application to complete genomes. J Mol Biol. 2001 Jan 19;305(3):567–580. doi: 10.1006/jmbi.2000.4315. [DOI] [PubMed] [Google Scholar]
  24. Lindsley D. L., Sandler L., Baker B. S., Carpenter A. T., Denell R. E., Hall J. C., Jacobs P. A., Miklos G. L., Davis B. K., Gethmann R. C. Segmental aneuploidy and the genetic gross structure of the Drosophila genome. Genetics. 1972 May;71(1):157–184. doi: 10.1093/genetics/71.1.157. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Makalowski W., Boguski M. S. Evolutionary parameters of the transcribed mammalian genome: an analysis of 2,820 orthologous rodent and human sequences. Proc Natl Acad Sci U S A. 1998 Aug 4;95(16):9407–9412. doi: 10.1073/pnas.95.16.9407. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Preston C. R., Sved J. A., Engels W. R. Flanking duplications and deletions associated with P-induced male recombination in Drosophila. Genetics. 1996 Dec;144(4):1623–1638. doi: 10.1093/genetics/144.4.1623. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Roehrdanz R. L., Lucchesi J. C. Mutational Events in the Triplo- and Haplo-Lethal Region (83de) of the DROSOPHILA MELANOGASTER Genome. Genetics. 1980 Jun;95(2):355–366. doi: 10.1093/genetics/95.2.355. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Royle Stephen J., Bobanović Laura K., Murrell-Lagnado Ruth D. Identification of a non-canonical tyrosine-based endocytic motif in an ionotropic receptor. J Biol Chem. 2002 Jul 8;277(38):35378–35385. doi: 10.1074/jbc.M204844200. [DOI] [PubMed] [Google Scholar]
  29. 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]
  30. Spradling A. C., Stern D., Beaton A., Rhem E. J., Laverty T., Mozden N., Misra S., Rubin G. M. The Berkeley Drosophila Genome Project gene disruption project: Single P-element insertions mutating 25% of vital Drosophila genes. Genetics. 1999 Sep;153(1):135–177. doi: 10.1093/genetics/153.1.135. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. 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 Nov 11;22(22):4673–4680. doi: 10.1093/nar/22.22.4673. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Urban Sinisa, Freeman Matthew. Intramembrane proteolysis controls diverse signalling pathways throughout evolution. Curr Opin Genet Dev. 2002 Oct;12(5):512–518. doi: 10.1016/s0959-437x(02)00334-9. [DOI] [PubMed] [Google Scholar]
  33. Vincent J. P., Kassis J. A., O'Farrell P. H. A synthetic homeodomain binding site acts as a cell type specific, promoter specific enhancer in Drosophila embryos. EMBO J. 1990 Aug;9(8):2573–2578. doi: 10.1002/j.1460-2075.1990.tb07438.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Whitfield Charles W., Band Mark R., Bonaldo Maria F., Kumar Charu G., Liu Lei, Pardinas Jose R., Robertson Hugh M., Soares M. Bento, Robinson Gene E. Annotated expressed sequence tags and cDNA microarrays for studies of brain and behavior in the honey bee. Genome Res. 2002 Apr;12(4):555–566. doi: 10.1101/gr.5302. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Wright F. The 'effective number of codons' used in a gene. Gene. 1990 Mar 1;87(1):23–29. doi: 10.1016/0378-1119(90)90491-9. [DOI] [PubMed] [Google Scholar]
  36. Yuan J., Amend A., Borkowski J., DeMarco R., Bailey W., Liu Y., Xie G., Blevins R. MULTICLUSTAL: a systematic method for surveying Clustal W alignment parameters. Bioinformatics. 1999 Oct;15(10):862–863. doi: 10.1093/bioinformatics/15.10.862. [DOI] [PubMed] [Google Scholar]
  37. Zdobnov Evgeny M., von Mering Christian, Letunic Ivica, Torrents David, Suyama Mikita, Copley Richard R., Christophides George K., Thomasova Dana, Holt Robert A., Subramanian G. Mani. Comparative genome and proteome analysis of Anopheles gambiae and Drosophila melanogaster. Science. 2002 Oct 4;298(5591):149–159. doi: 10.1126/science.1077061. [DOI] [PubMed] [Google Scholar]