Table of Contents Author Guidelines
Genetics Research International
Volume 2017, Article ID 2624170, 14 pages
https://doi.org/10.1155/2017/2624170
Research Article

The Noncell Autonomous Requirement of Proboscipedia for Growth and Differentiation of the Distal Maxillary Palp during Metamorphosis of Drosophila melanogaster

Department of Biology, University of Western Ontario, London, ON, Canada N6A 5B7

Correspondence should be addressed to Anthony Percival-Smith; ac.owu@avicrepa

Received 11 November 2016; Accepted 18 January 2017; Published 5 March 2017

Academic Editor: Norman A. Doggett

Copyright © 2017 Anthony Percival-Smith et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. R. E. Snodgrass, Principles of Insect Morphogenesis, McGraw-Hill Book Co., New York, NY, USA, 1935.
  2. P. R. Grant and B. R. Grant, “Unpredictable evolution in a 30-year study of Darwin's finches,” Science, vol. 296, no. 5568, pp. 707–711, 2002. View at Publisher · View at Google Scholar · View at Scopus
  3. T. C. Kaufman, “Cytogenetic analysis of chromosome 3 in Drosophila melanogaster: isolation and characterization of four new alleles of the proboscipedia (pb) locus,” Genetics, vol. 90, no. 3, pp. 579–596, 1978. View at Google Scholar · View at Scopus
  4. G. Struhl, “Genes controlling segmental specification in the Drosophila thorax,” Proceedings of the National Academy of Sciences of the United States of America, vol. 79, no. 23 I, pp. 7380–7384, 1982. View at Publisher · View at Google Scholar · View at Scopus
  5. V. K. L. Merrill, F. R. Turner, and T. C. Kaufman, “A genetic and developmental analysis of mutations in the Deformed locus in Drosophila melanogaster,” Developmental Biology, vol. 122, no. 2, pp. 379–395, 1987. View at Publisher · View at Google Scholar · View at Scopus
  6. V. K. L. Merrill, R. J. Diederich, F. R. Turner, and T. C. Kaufman, “A genetic and developmental analysis of mutations in labial, a gene necessary for proper head formation in Drosophila melanogaster,” Developmental Biology, vol. 135, no. 2, pp. 376–391, 1989. View at Publisher · View at Google Scholar · View at Scopus
  7. D. L. Cribbs, C. Benassayag, F. M. Randazzo, and T. C. Kaufman, “Levels of homeotic protein function can determine developmental identity: evidence from low-level expression of the Drosophila homeotic gene proboscipedia under Hsp7O control,” EMBO Journal, vol. 14, no. 4, pp. 767–778, 1995. View at Google Scholar · View at Scopus
  8. R. W. Beeman, J. J. Stuart, M. S. Haas, and R. E. Denell, “Genetic analysis of the homeotic gene complex (HOM-C) in the beetle Tribolium castaneum,” Developmental Biology, vol. 133, no. 1, pp. 196–209, 1989. View at Publisher · View at Google Scholar · View at Scopus
  9. C. L. Hughes and T. C. Kaufman, “RNAi analysis of deformed, proboscipedia and sex combs reduced in the milkweed bug Oncopeltus fasciatus: novel roles for Hox genes in the Hemipteran head,” Development, vol. 127, no. 17, pp. 3683–3694, 2000. View at Google Scholar · View at Scopus
  10. T. C. Kaufman, M. A. Seeger, and G. Olsen, “Molecular and genetic organization of the antennapedia gene complex of Drosophila melanogaster,” Advances in Genetics, vol. 27, pp. 309–362, 1990. View at Google Scholar · View at Scopus
  11. M. A. Pultz, R. J. Diederich, D. L. Cribbs, and T. C. Kaufman, “The proboscipedia locus of the Antennapedia complex: a molecular and genetic analysis,” Genes & Development, vol. 2, no. 7, pp. 901–920, 1988. View at Publisher · View at Google Scholar · View at Scopus
  12. A. Percival-Smith, J. Weber, E. Gilfoyle, and P. Wilson, “Genetic characterization of the role of the two HOX proteins, Proboscipedia and Sex Combs Reduced, in determination of adult antennal, tarsal, maxillary palp and proboscis identities in Drosophila melanogaster,” Development, vol. 124, no. 24, pp. 5049–5062, 1997. View at Google Scholar · View at Scopus
  13. L. Sivanantharajah and A. Percival-Smith, “Analysis of the sequence and phenotype of Drosophila Sex combs reduced alleles reveals potential functions of conserved protein motifs of the Sex combs reduced protein,” Genetics, vol. 182, no. 1, pp. 191–203, 2009. View at Publisher · View at Google Scholar · View at Scopus
  14. G. Lebreton, C. Faucher, D. L. Cribbs, and C. Benassayag, “Timing of Wingless signalling distinguishes maxillary and antennal identities in Drosophila melanogaster,” Development, vol. 135, no. 13, pp. 2301–2309, 2008. View at Publisher · View at Google Scholar · View at Scopus
  15. W. J. Brook, F. J. Diaz-Benjumea, and S. M. Cohen, “Organizing spatial pattern in limb development,” Annual Review of Cell and Developmental Biology, vol. 12, pp. 161–180, 1996. View at Publisher · View at Google Scholar · View at Scopus
  16. T. Lecuit and S. M. Cohen, “Proximal-distal axis formation in the drosophila leg,” Nature, vol. 388, no. 6638, pp. 139–145, 1997. View at Publisher · View at Google Scholar · View at Scopus
  17. R. E. Ward, P. Reid, A. Bashirullah, P. P. D'Avino, and C. S. Thummel, “GFP in living animals reveals dynamic developmental responses to ecdysone during Drosophila metamorphosis,” Developmental Biology, vol. 256, no. 2, pp. 389–402, 2003. View at Publisher · View at Google Scholar · View at Scopus
  18. C. Vinegoni, C. Pitsouli, D. Razansky, N. Perrimon, and V. Ntziachristos, “In vivo imaging of Drosophila melanogaster pupae with mesoscopic fluorescence tomography,” Nature Methods, vol. 5, no. 1, pp. 45–47, 2008. View at Publisher · View at Google Scholar · View at Scopus
  19. A. Percival-Smith and D. J. Hayden, “Analysis in Drosophila melanogaster of the interaction between sex combs reduced and extradenticle activity in the determination of tarsus and arista identity,” Genetics, vol. 150, pp. 189–198, 1998. View at Google Scholar · View at Scopus
  20. C. Benassayag, S. Plaza, P. Callaerts et al., “Evidence for a direct functional antagonism of the selector genes proboscipedia and eyeless in Drosophila head development,” Development, vol. 130, no. 3, pp. 575–586, 2003. View at Publisher · View at Google Scholar · View at Scopus
  21. G. Dietzl, D. Chen, F. Schnorrer et al., “A genome-wide transgenic RNAi library for conditional gene inactivation in Drosophila,” Nature, vol. 448, no. 7150, pp. 151–156, 2007. View at Publisher · View at Google Scholar · View at Scopus
  22. O. Gerlitz, D. Nellen, M. Ottiger, and K. Basler, “A screen for genes expressed in Drosophila imaginal discs,” International Journal of Developmental Biology, vol. 46, no. 1, pp. 173–176, 2002. View at Google Scholar · View at Scopus
  23. K. Staehling-Hampton, P. D. Jackson, M. J. Clark, A. H. Brand, and F. M. Hoffmann, “Specificity of bone morphogenetic protein-related factors: cell fate and gene expression changes in Drosophila embryos induced by decapentaplegic but not 60A,” Cell Growth and Differentiation, vol. 5, no. 6, pp. 585–593, 1994. View at Google Scholar · View at Scopus
  24. D. L. Cribbs, M. A. Pultz, D. Johnson, M. Mazzulla, and T. C. Kaufman, “Structural complexity and evolutionary conservation of the Drosophila homeotic gene proboscipedia,” EMBO Journal, vol. 11, no. 4, pp. 1437–1449, 1992. View at Google Scholar · View at Scopus
  25. M. A. Glicksman and D. L. Brower, “Expression of the Sex combs reduced protein in Drosophila larvae,” Developmental Biology, vol. 127, no. 1, pp. 113–118, 1988. View at Publisher · View at Google Scholar · View at Scopus
  26. H. J. Bellen, C. J. O'Kane, C. Wilson, U. Grossniklaus, R. K. Pearson, and W. J. Gehring, “P-element-mediated enhancer detection: a versatile method to study development in Drosophila,” Genes & Development, vol. 3, no. 9, pp. 1288–1300, 1989. View at Publisher · View at Google Scholar · View at Scopus
  27. E. Wieschaus and C. Nusslein-Volhard, “Looking at embryos,” in Drosophila: A Practical Approach, D. B. Roberts, Ed., pp. 199–228, IRL Press, Oxford, UK, 1986. View at Google Scholar
  28. T. Xu and G. M. Rubin, “Analysis of genetic mosaics in developing and adult Drosophila tissues,” Development, vol. 117, no. 4, pp. 1223–1237, 1993. View at Google Scholar · View at Scopus
  29. Y. He, X. Fang, K. Emoto, Y.-N. Jan, and P. N. Adler, “The tricornered Ser/Thr protein kinase is regulated by phosphorylation and interacts with furry during Drosophila wing hair development,” Molecular Biology of the Cell, vol. 16, no. 2, pp. 689–700, 2005. View at Publisher · View at Google Scholar · View at Scopus
  30. J. L. Haynie and P. J. Bryant, “Development of the eye-antenna imaginal disc and morphogenesis of the adult head in Drosophila melanogaster,” Journal of Experimental Zoology, vol. 237, no. 3, pp. 293–308, 1986. View at Publisher · View at Google Scholar · View at Scopus
  31. H. Tanimoto, S. Itoh, P. Ten Dijke, and T. Tabata, “Hedgehog creates a gradient of DPP activity in Drosophila wing imaginal discs,” Molecular Cell, vol. 5, no. 1, pp. 59–71, 2000. View at Publisher · View at Google Scholar · View at Scopus
  32. T. E. Haerry, O. Khalsa, M. B. O'Connor, and K. A. Wharton, “Synergistic signaling by two BMP ligands through the SAX and TKV receptors controls wing growth and patterning in Drosophila,” Development, vol. 125, no. 20, pp. 3977–3987, 1998. View at Google Scholar · View at Scopus
  33. M. M. Kulkarni, M. Booker, S. J. Silver et al., “Evidence of off-target effects associated with long dsRNAs in Drosophila melanogaster cell-based assays,” Nature Methods, vol. 3, no. 10, pp. 833–838, 2006. View at Publisher · View at Google Scholar · View at Scopus
  34. Y. Ma, A. Creanga, L. Lum, and P. A. Beachy, “Prevalence of off-target effects in Drosophila RNA interference screens,” Nature, vol. 443, no. 7109, pp. 359–363, 2006. View at Publisher · View at Google Scholar · View at Scopus
  35. J. Mohler and K. Vani, “Molecular organization and embryonic expression of the hedgehog gene involved in cell-cell communication in segmental patterning of Drosophila,” Development, vol. 115, no. 4, pp. 957–971, 1992. View at Google Scholar · View at Scopus
  36. K. Immerglück, P. A. Lawrence, and M. Bienz, “Induction across germ layers in Drosophila mediated by a genetic cascade,” Cell, vol. 62, no. 2, pp. 261–268, 1990. View at Publisher · View at Google Scholar · View at Scopus
  37. A. Percival-Smith, W. A. Teft, and J. L. Barta, “Tarsus determination in Drosophila melanogaster,” Genome, vol. 48, no. 4, pp. 712–721, 2005. View at Publisher · View at Google Scholar · View at Scopus
  38. G. Struhl, “A homoeotic mutation transforming leg to antenna in Drosophila,” Nature, vol. 292, no. 5824, pp. 635–638, 1981. View at Publisher · View at Google Scholar · View at Scopus
  39. L. Joulia, H.-M. Bourbon, and D. L. Cribbs, “Homeotic proboscipedia function modulates hedgehog-mediated organizer activity to pattern adult Drosophila mouthparts,” Developmental Biology, vol. 278, no. 2, pp. 495–510, 2005. View at Publisher · View at Google Scholar · View at Scopus
  40. L. Joulia, J. Deutsch, H.-M. Bourbon, and D. L. Cribbs, “The specification of a highly derived arthropod appendage, the Drosophila labial palps, requires the joint action of selectors and signaling pathways,” Development Genes and Evolution, vol. 216, no. 7-8, pp. 431–442, 2006. View at Publisher · View at Google Scholar · View at Scopus
  41. M. A. Crickmore and R. S. Mann, “Hox control of organ size by regulation of morphogen production and mobility,” Science, vol. 313, no. 5783, pp. 63–68, 2006. View at Publisher · View at Google Scholar · View at Scopus
  42. M. A. Crickmore and R. S. Mann, “Hox control of morphogen mobility and organ development through regulation of glypican expression,” Development, vol. 134, no. 2, pp. 327–334, 2007. View at Publisher · View at Google Scholar · View at Scopus
  43. R. K. Mann and P. A. Beachy, “Novel lipid modifications of secreted protein signals,” Annual Review of Biochemistry, vol. 73, pp. 891–923, 2004. View at Publisher · View at Google Scholar · View at Scopus
  44. D. R. Angelini and T. C. Kaufman, “Insect appendages and comparative ontogenetics,” Developmental Biology, vol. 286, no. 1, pp. 57–77, 2005. View at Publisher · View at Google Scholar · View at Scopus
  45. D. R. Angelini, F. W. Smith, A. C. Aspiras, M. Kikuchi, and E. L. Jockusch, “Patterning of the adult mandibulate mouthparts in the red flour beetle, Tribolium castaneum,” Genetics, vol. 190, no. 2, pp. 639–654, 2012. View at Publisher · View at Google Scholar · View at Scopus
  46. G. Morata and P. A. Lawrence, “Development of the eye-antenna imaginal disc of Drosophila,” Developmental Biology, vol. 70, no. 2, pp. 355–371, 1979. View at Publisher · View at Google Scholar · View at Scopus
  47. G. Campbell, “Distalization of the Drosophila leg by graded EGF-receptor activity,” Nature, vol. 418, no. 6899, pp. 781–785, 2002. View at Publisher · View at Google Scholar · View at Scopus
  48. M. I. Galindo, S. A. Bishop, and J. P. Couso, “Dynamic EGFR-Ras signalling in Drosophila leg development,” Developmental Dynamics, vol. 233, no. 4, pp. 1496–1508, 2005. View at Publisher · View at Google Scholar · View at Scopus
  49. M. Boube, C. Benassayag, L. Seroude, and D. L. Cribbs, “Ras1-mediated modulation of Drosophila homeotic function in cell and segment identity,” Genetics, vol. 146, no. 2, pp. 619–628, 1997. View at Google Scholar · View at Scopus