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Identification of two Drosophila TGF-β family members in the grasshopper Schistocerca americana

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Abstract

Intercellular signaling molecules of the transforming growth factor-β (TGF-β) superfamily are required for pattern formation in many multicellular organisms. The decapentaplegic (dpp) gene of Drosophila melanogaster has several developmental roles. To improve our understanding of the evolutionary diversification of this large family we identified dpp in the grasshopper Schistocerca americana. S. americana diverged from D. melanogaster approximately 350 million years ago, utilizes a distinct developmental program, and has a 60-fold-larger genome than D. melanogaster. Our analyses indicate a single dpp locus in D. melanogaster and S. americana, suggesting that dpp copy number does not correlate with increasing genome size. Another TGF-β superfamily member, the D. melanogaster gene 60A, is also present in only one copy in each species. Comparison of homologous sequences from D. melanogaster, S. americana, and H. sapiens, representing roughly 900 million years of evolutionary distance, reveals significant constraint on sequence divergence for both dpp and 60A. In the signaling portion of the dpp protein, the amino acid identity between these species exceeds 74%. Our results for the TGF-β superfamily are consistent with current hypotheses describing gene duplication and diversification as a frequent response to high levels of selective pressure on individual family members.

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References

  • Arora K, Levine MS, O'Conner MB (1994) The screw gene encodes a ubiquitously expressed member of the TGF-β family required for specification of dorsal cell fates in the Drosophila embryo. Genes Dev 21:2588–2601

    Google Scholar 

  • Bentley D, Keshishian H, Shankland M, Toroian-Raymond A (1979) Quantitative staging of embryonic development of the grasshopper Schistocerca nitens. J Embryol Exp Morphol 54:47–74

    Google Scholar 

  • Chomczynski P, Saachi N (1987) Single step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal Biochem 162:156–159

    Article  CAS  PubMed  Google Scholar 

  • Echelard Y, Epstein DJ, St-Jacques B, Shen L, Mohler J, McMahon JA, McMahon AP (1993) Sonic hedgehog, a member of a family of putative signalling molecules, is implicated in the regulation of CNS polarity. Cell 75:1417–1430

    CAS  PubMed  Google Scholar 

  • Field KG, Olsen GJ, Lane DJ, Giovanni SJ, Ghiselin MT, Raff EC, Pace NR, Raff RA (1988) Molecular phylogeny of the animal kingdom. Science 239:748–753

    CAS  PubMed  Google Scholar 

  • Hennig W (1981) Insect phylogeny. John Wiley & Sons, New York

    Google Scholar 

  • Irish VF, Gelbart WM (1987) The haplo-insufficient region of the decapentaplegic gene is required for dorsal-ventral patterning of the Drosophila embryo. Genes Dev 1:868–879

    Google Scholar 

  • Kingsley DM (1994) The TGF-β superfamily: new members, new receptors, and new tests of genetic function in different organisms. Genes Dev 8:133–146

    Google Scholar 

  • Li W-H (1983) Evolution of duplicate genes and pseudogenes. In: Nei M, Koehn RK (eds) Evolution of genes and proteins. Simmer Associates, Sunderland, MA, pp 14–37

    Google Scholar 

  • Loh EY, Elliott JF, Cwirla S, Lanier LL, Davis M (1989) Polymerase chain reaction with single sided specificity: analysis of T cell receptor delta chain. Science 243:217–222

    Google Scholar 

  • Massagué J (1990) The transforming growth factor-β family. An Rev Cell Biol 6:597–641

    Google Scholar 

  • Newfeld SJ, Smoller DA, Yedvobnick B (1991) Interspecific comparison of the unusually repetitive Drosophila locus mastermind. J Mol Evol 32:415–420

    Google Scholar 

  • Newfeld SJ, Schmid AT, Yedvobnick B (1993) Homopolymer length variation in the Drosophila gene mastermind. J Mol Evol 37:483–495

    Google Scholar 

  • Padgett RW, St Johnston RD, Gelbart WM (1987) A transcript from a Drosophila pattern gene predicts a protein homologous to the transforming growth factor beta gene family. Nature 325:81–84

    Google Scholar 

  • Padgett RW, Wozney JM, Gelbart WM (1993) Human BMP sequences can confer normal dorsal-ventral patterning in the Drosophila embryo. Proc Natl Acad Sci USA 90:2905–2909

    Google Scholar 

  • Panganiban GEF, Rashka KE, Neitzel MD, Hoffman MF (1990) Biochemical characterization of the Drosophila dpp protein, a member of the transforming growth factor β family of growth factors. Mol Cell Biol 10:2669–2677.

    Google Scholar 

  • Patel NH, Ball EE, Goodman CS (1992) Changing role of even-skipped during the evolution of insect pattern formation. Nature 357:339–342

    Google Scholar 

  • Sambrook J, Fritsch E, Maniatis T (1989) Molecular cloning: a laboratory manual (2nd ed). Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY

    Google Scholar 

  • Sampath TK, Rashka KE, Doctor JS, Tucker RF, Hoffman MF (1993) Drosophila TGF-β superfamily proteins induce endochondrial bone formation in mammals. Proc Natl Acad Sci USA 90:6004–6008

    Google Scholar 

  • Segal D, Gelbart WM (1985) Shortvein, a new component of the decapentaplegic gene complex in Drosophila melanogaster. Genetics 109:119–143

    Google Scholar 

  • Smith RF, Smith TF (1990) Automatic generation of primary sequence patterns from sets of related protein sequences. Proc Natl Acad Sci USA 87:118–122

    Google Scholar 

  • Snow PM, Zinn K, Harrelson AL, McAllister L, Schilling J, Bastiani MJ, Makk G, Goodman CS (1988) Characterization and cloning of fasciclin I and fasciclin II glycoproteins in the grasshopper. Proc Natl Acad Sci USA 85:5291–5295

    Google Scholar 

  • Spencer FA, Hoffman FM, Gelbart WM (1982) Decapentaplegic: a gene complex affecting morphogenesis in Drosophila melanogaster. Cell 28:451–461

    Google Scholar 

  • St. Johnston RD, Hoffman FM, Blackman RK, Sejal D, Grimaila R et al. (1990) Molecular organization of the decapentaplegic gene in Drosophila melanogaster. Genes Dev 4:1114–1127

    Google Scholar 

  • Wharton KA, Thomsen GH, Gelbart WM (1991) Drosophila 60A gene, another transforming growth factor beta family member, is closely related to human bone morphogenetic proteins. Proc Natl Acad Sci USA 88:9214–9218

    Google Scholar 

  • Wilmore PJ, Brown AK (1975) Molecular properties of orthopteran DNA. Chromosoma 51:337–345

    Google Scholar 

  • Wozney JM, Rosen V, Celeste AJ, Mitsock LM, Whitters MJ, Driz RW, Hewick RM, Wang EA (1988) Novel regulators of bone formation: molecular clones and activities. Science 242:1528–1534

    Google Scholar 

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Newfeld, S.J., Gelbart, W.M. Identification of two Drosophila TGF-β family members in the grasshopper Schistocerca americana . J Mol Evol 41, 155–160 (1995). https://doi.org/10.1007/BF00170667

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