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Hox Genes pp 133-144 | Cite as

Hox3/zen and the Evolution of Extraembryonic Epithelia in Insects

  • Urs Schmidt-Ott
  • Ab. Matteen Rafiqi
  • Steffen Lemke
Part of the Advances in Experimental Medicine and Biology book series (AEMB, volume 689)

Abstract

Insects have undergone dramatic evolutionary changes in extraembryonic development, which correlate with changes in the expression of the class-3 Hox gene zen. Here, we review the evolution of this gene in insects and point out how changes in zen expression may have affected extraembryonic development at the morphological and the genetic level.

Keywords

Dorsal Midline Holometabolous Insect Extraembryonic Tissue Amniotic Cavity Dorsal Closure 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

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References

  1. 1.
    Hughes CL, Kaufman TC. Hox genes and the evolution of the arthropod body plan. Evol Dev 2002; 4:459–499.CrossRefPubMedGoogle Scholar
  2. 2.
    Mann RS, Chan SK. Extra specificity from extradenticle: the partnership between HOX and PBX/ EXD homeodomain proteins. Trends Genet 1996; 12:258–62.CrossRefPubMedGoogle Scholar
  3. 3.
    Moens CB, Selleri L. Hox cofactors in vertebrate development. Dev Biol 2006; 291:193–206.CrossRefPubMedGoogle Scholar
  4. 4.
    Joshi R, Passner JM, Rohs R et al. Functional specificity of a Hox protein mediated by the recognition of minor groove structure. Cell 2007; 131:530–43.CrossRefPubMedGoogle Scholar
  5. 5.
    Hughes CL, Liu PZ, Kaufman TC. Expression patterns of the rogue Hox genes Hox3/zen and fushi tarazu. Evol Dev 2004; 6:393–401.CrossRefPubMedGoogle Scholar
  6. 6.
    Panfilio KA, Akam M. A comparison of Hox3 and Zen protein coding sequences in taxa that span the Hox3/zen divergence. Dev Genes Evol 2007; 217:323–9.CrossRefPubMedGoogle Scholar
  7. 7.
    Rushlow C, Doyle H, Hoey T et al. Molecular characterization of the zerknüllt region of the Antennapedia gene complex in Drosophila. Genes Dev 1987; 1:1268–1279.CrossRefPubMedGoogle Scholar
  8. 8.
    Panfilio KA. Extraembryonic development in insects and the acrobatics of blastokinesis. Dev Biol 2008; 313:471–91.CrossRefPubMedGoogle Scholar
  9. 9.
    Panfilio KA, Liu PZ, Akam M et al. Oncopeltus fasciatus zen is essential for serosal tissue function in katatrepsis. Dev Biol 2006; 292:226–43.CrossRefPubMedGoogle Scholar
  10. 10.
    Panfilio KA. Late extraembryonic morphogenesis and its zen RNAi-induced failure in the milkweed bug Oncopeltus fasciatus. Dev Biol 2009; 333:297–311.CrossRefPubMedGoogle Scholar
  11. 11.
    Machida R, Ando H. Evolutionary changes in developmental potentials of the embryo proper and embryonic membranes along with the derivative structures in Atelocerata, with special reference to hexapoda (arthropoda). Proc Arthropod Embryol Soc Jpn 1998; 33:1–12.Google Scholar
  12. 12.
    Sander K. In Insect Development. Lawrence PA, ed. Oxford: Blackwell Scientific Publications, 1976;35–52.Google Scholar
  13. 13.
    Anderson DT. In Developmental Systems: insects. Counce SJ, Waddington CH, eds. London: Academic, 1972;165–242.Google Scholar
  14. 14.
    Davis CWC. A comparative study of larval embryogenesis in the mosquito Culex fatigans Wiedemann (Diptera: Culicidae) and the sheep-fly Lucilia sericata Meigen (Diptera: Calliphoridae). Aust J Zool 1967; 15:547–579.CrossRefGoogle Scholar
  15. 15.
    Kahle W. Die Paedogenesis der Cecidomyiden. Zoologica, Stuttgart 1908; 21:1–80 (Plates I-VI).Google Scholar
  16. 16.
    Gambrell FL. The embryology of the blackfly Simulium pinctipes Hagen. Ann Entomol Soc Am 1933; 26:641–671.Google Scholar
  17. 17.
    Butt FH. Embryology of Sciara. Ann Entomol Soc Am 1934; 27:565–579.Google Scholar
  18. 18.
    Rafiqi AM, Lemke SJ, Ferguson S et al. Evolutionary origin of the amnioserosa in cyclorrhaphan flies correlates with spatial and temporal expression changes of zen. Proc Natl Acad Sci USA 2008; 105:234–239.CrossRefPubMedGoogle Scholar
  19. 19.
    Campos-Ortega JA, Hartenstein V. The embryonic development of Drosophila melanogaster (Springer-Verlag, Berlin, Heidelberg, New York, 1997).Google Scholar
  20. 20.
    Reed BH, Wilk R, Schöck F et al. Integrin-dependent apposition of Drosophila extraembryonic membranes promotes morphogenesis and prevents anoikis. Curr Biol 2004; 14:372–380.CrossRefPubMedGoogle Scholar
  21. 21.
    Falciani F, Hausdorf B, Schröder R et al. Class 3 Hox genes in insects and the origin of zen. Proc Natl Acad Sci USA 1996; 93:8479–8484.CrossRefPubMedGoogle Scholar
  22. 22.
    Dearden P, Grbic M, Falciani F et al. Maternal expression and early zygotic regulation of the Hox3/ zen gene in the grasshopper Schistocerca gregaria. Evol Dev 2000; 2:261–270.CrossRefPubMedGoogle Scholar
  23. 23.
    van der Zee M, Berns N, Roth S. Distinct functions of the Tribolium zerknüllt genes in serosa specification and dorsal closure. Curr Biol 2005; 15:624–636.CrossRefPubMedGoogle Scholar
  24. 24.
    Goltsev Y, Fuse N, Frasch M et al. Evolution of the dorsal-ventral patterning network in the mosquito, Anopheles gambiae. Development 2007;2415–2424.Google Scholar
  25. 25.
    Stauber M, Prell A, Schmidt-Ott U. A single Hox3 gene with composite bicoid and zerknüllt expression characteristics in non-Cyclorrhaphan flies. Proc Natl Acad Sci USA 2002; 99:274–279.CrossRefPubMedGoogle Scholar
  26. 26.
    Brown S, Fellers J, Shippy T et al. A strategy for mapping bicoid on the phylogenetic tree. Curr Biol 2001; 11:R43–R44.CrossRefPubMedGoogle Scholar
  27. 27.
    Pultz, MA Diederich RJ, Cribbs DL et al. The proboscipedia locus of the antennapedia complex: a molecular and genetic analysis. Genes Dev 1988; 2:901–920.CrossRefPubMedGoogle Scholar
  28. 28.
    Rafiqi AM. Morphological transitions and the genetic basis of the evolution of extraembryonic tissues in flies. Ph.D. Thesis, Wageningen University (NL) 2008.Google Scholar
  29. 29.
    Stauber M, Lemke S, Schmidt-Ott U. Expression and regulation of caudal in the lower cyclorrhaphan fly Megaselia. Dev Genes Evol 2008; 218:81–7.CrossRefPubMedGoogle Scholar
  30. 30.
    Newfeld SJ, Wisotzkey RG, Kumar S. Molecular evolution of a developmental pathway: phylogenetic analyses of transforming growth factor-beta family ligands, receptors and Smad signal transducers. Genetics 1999; 152:783–95.PubMedGoogle Scholar
  31. 31.
    O’Connor MB, Umulis D, Othmer HG et al. Shaping BMP morphogen gradients in the Drosophila embryo and pupal wing. Development 2006; 133:183–93.CrossRefPubMedGoogle Scholar
  32. 32.
    Ferguson EL, Anderson KV. Decapentaplegic acts as a morphogen to organize dorsal-ventral pattern in the Drosophila embryo. Cell 1992; 71:451–61.CrossRefPubMedGoogle Scholar
  33. 33.
    Dorfman R, Shilo BZ. Biphasic activation of the BMP pathway patterns the Drosophila embryonic dorsal region. Development 2001; 128:965–972.PubMedGoogle Scholar
  34. 34.
    Tanimoto H, Itoh S, ten Dijke P et al. Hedgehog creates a gradient of DPP activity in Drosophila wing imaginal discs. Mol Cell 2000; 5:59–71.CrossRefPubMedGoogle Scholar
  35. 35.
    Persson U, Izumi H, Souchelnytskyi S et al. The L45 loop in type I receptors for TGF-beta family members is a critical determinant in specifying Smad isoform activation. FEBS Lett 1998; 434:83–7.CrossRefPubMedGoogle Scholar
  36. 36.
    Wang Y-C, Ferguson EL. Spatial bistability of Dpp-receptor interactions during Drosophila dorsal-ventral patterning. Nature 2005; 434:229–234.CrossRefPubMedGoogle Scholar
  37. 37.
    van der Zee M, Stockhammer O, von Levetzow C et al. Sog/Chordin is required for ventral-to-dorsal Dpp/BMP transport and head formation in a short germ insect. Proc Natl Acad Sci USA 2006; 103:16307–16312.CrossRefPubMedGoogle Scholar
  38. 38.
    Schoppmeier M, Schröder R. Maternal torso signaling controls body axis elongation in a short germ insect. Curr Biol 2005; 15:2131–6.CrossRefPubMedGoogle Scholar
  39. 39.
    Angelini DR, Kaufman TC. Functional analyses in the milkweed bug (Hemiptera) support a role for Wnt signaling in body segmentation but not appendage development. Dev Biol 2005; 283:409–23.CrossRefPubMedGoogle Scholar
  40. 40.
    Chang T, Mazotta J, Dumstrei K et al. Dpp and Hh signaling in the Drosophila embryonic eye field. Development 2001; 128:4691–4704.PubMedGoogle Scholar
  41. 41.
    Frank LH, Rushlow C. A group of genes required for maintenance of the amnioserosa tissue in Drosophila. Development 1996; 122:1343–1352.PubMedGoogle Scholar
  42. 42.
    Yip MLR, Lamka ML, Lipshitz HD. Control of germ-band retraction in Drosophila by the zinc-finger protein Hindsight. Development 1997; 124:2129–2141.PubMedGoogle Scholar
  43. 43.
    Reim I, Lee H-H, Frasch M. The T-box-encoding dorsocross genes function in amnioserosa development and the patterning of the dorsolateral germ band downstream of Dpp. Development 2003; 130:3187–3204.CrossRefPubMedGoogle Scholar
  44. 44.
    Winick J, Abel T, Leonard MW et al. A GATA family transcription factor is expressed along the embryonic dorsoventral axis in Drosophila melanogaster. Development 1993; 119:1055–1065.PubMedGoogle Scholar
  45. 45.
    Heitzler P, Haenlin M, Ramain P et al. A genetic analysis of pannier, a gene necessary for viability of dorsal tissues and bristle positioning in Drosophila. Genetics 1996; 143:1271–1286.PubMedGoogle Scholar
  46. 46.
    Ashe HL, Mannervik M, Levine M. Dpp signaling thresholds in the dorsal ectoderm of the Drosophila embryo. Development 2000; 127:3305–12.PubMedGoogle Scholar
  47. 47.
    Haenlin M, Cubadda Y, Blondeau F et al. Transcriptional activity of pannier is regulated negatively by heterodimerization of the GATA DNA-binding domain with a cofactor encoded by the u-shaped gene of Drosophila. Genes Dev 1997; 11:3096–108.CrossRefPubMedGoogle Scholar
  48. 48.
    Herranz H, Morata G. The functions of pannier during Drosophila embryogenesis. Development 2001; 128:4837–46.PubMedGoogle Scholar
  49. 49.
    Lin MC, Park J, Kirov N et al. Threshold response of C15 to the Dpp gradient in Drosophila is established by the cumulative effect of Smad and Zen activators and negative cues. Development 2006; 133:4805–13.CrossRefPubMedGoogle Scholar
  50. 50.
    Campbell G. Regulation of gene expression in the distal region of the Drosophila leg by the Hox11 homolog, C15. Dev Biol 2005; 278:607–18.CrossRefPubMedGoogle Scholar
  51. 51.
    Grimaldi D, Engel MS. Evolution of insects. Cambridge: Cambridge University Press, 2005.Google Scholar

Copyright information

© Landes Bioscience and Springer Science+Business Media 2010

Authors and Affiliations

  • Urs Schmidt-Ott
    • 1
  • Ab. Matteen Rafiqi
    • 1
  • Steffen Lemke
    • 1
  1. 1.Department of Organismal Biology and AnatomyUniversity of ChicagoChicago

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