Development Genes and Evolution

, Volume 216, Issue 7–8, pp 363–371

Conservation of upstream regulators of scute on the notum of cyclorraphous Diptera

Review

Abstract

Bristles on the notum of many cyclorraphous flies are arranged into species-specific stereotyped patterns. Differences in the spatial expression of the proneural gene scute correlate with the positions of bristles in those species looked at so far. However, the examination of a number of genes encoding trans-regulatory factors, such as pannier, stripe, u-shaped, caupolican and wingless, indicates that they are expressed in conserved domains on the prospective notum. This suggests that the function of a trans-regulatory network of genes is relatively unchanged in derived Diptera, and that many differences are likely to be due to changes in cis-regulatory sequences of scute. In contrast, in Anopheles gambiae, a basal species with no stereotyped bristle pattern, the expression patterns of pannier and wingless are not conserved, and expression of AgASH, the Anopheles proneural gene, does not correlate in a similar manner with the bristle pattern. We discuss the possibility that independently acting cis-regulatory sequences at the scute locus may have arisen in the lineage giving rise to cyclorraphous flies.

Keywords

Drosophila Calliphora vicina Anopheles gambiae Achaetescute Bristle pattern 

References

  1. Aldaz S, Morata G, Azpiazu N (2003) The Pax-homeobox gene eyegone is involved in the subdivision of the thorax of Drosophila. Development 130:4473–4482PubMedCrossRefGoogle Scholar
  2. Alonso MC, Cabrera CV (1988) The achaetescute gene complex of Drosophila melanogaster comprises four homologous genes. EMBO J 7:2585–2591PubMedGoogle Scholar
  3. Bertrand N, Castro DS, Guillemot F (2002) Proneural genes and the specification of neural cell types. Nat Rev Neurosci 3:517–530PubMedCrossRefGoogle Scholar
  4. Calleja M, Herranz H, Estella C, Casal J, Lawrence P, Simpson P, Morata G (2000) Generation of medial and lateral dorsal body domains by the pannier gene of Drosophila. Development 127:3971–3980PubMedGoogle Scholar
  5. Calleja M, Renaud O, Usui K, Pistillo D, Morata G, Simpson P (2002) How to pattern an epithelium: lessons from achaetescute regulation on the notum of Drosophila. Gene 292:1–12PubMedCrossRefGoogle Scholar
  6. Cavodeassi F, Diez Del Corral R, Campuzano S, Dominguez M (1999) Compartments and organising boundaries in the Drosophila eye: the role of the homeodomain Iroquois proteins. Development 126:4933–4942PubMedGoogle Scholar
  7. Cubadda Y, Heitzler P, Ray RP, Bourouis M, Ramain P, Gelbart W, Simpson P, Haenlin M (1997) u-shaped encodes a zinc finger protein that regulates the proneural genes achaete and scute during the formation of bristles in Drosophila. Genes Dev 11:3083–3095PubMedGoogle Scholar
  8. Cubas P, de Celis JF, Campuzano S, Modolell J (1991) Proneural clusters of achaete–scute expression and the generation of sensory organs in the Drosophila imaginal wing disc. Genes Dev 5:996–1008PubMedGoogle Scholar
  9. Diez del Corral R, Aroca P, Gomez-Skarmeta JL, Cavodeassi F, Modolell J (1999) The Iroquois homeodomain proteins are required to specify body wall identity in Drosophila. Genes Dev 13:1754–1761PubMedGoogle Scholar
  10. Fernandes JJ, Celniker SE, VijayRaghavan K (1996) Development of the indirect flight muscle attachment sites in Drosophila: role of the PS integrins and the stripe gene. Dev Biol 176:166–184PubMedCrossRefGoogle Scholar
  11. Frommer G, Vorbruggen G, Pasca G, Jackle H, Volk T (1996) Epidermal egr-like zinc finger protein of Drosophila participates in myotube guidance. EMBO J 15:1642–1649PubMedGoogle Scholar
  12. Garcia-Garcia MJ, Ramain P, Simpson P, Modolell J (1999) Different contributions of pannier and wingless to the patterning of the dorsal mesothorax of Drosophila. Development 126:3523–3532PubMedGoogle Scholar
  13. Ghazi A, Paul L, VijayRaghavan K (2003) Prepattern genes and signalling molecules regulate stripe expression to specify Drosophila flight muscle attachment sites. Mech Dev 120:519–528PubMedCrossRefGoogle Scholar
  14. Gomez-Skarmeta JL, Rodriguez I, Martinez C, Culi J, Ferres-Marco D, Beamonte D, Modolell J (1995) Cis-regulation of achaete and scute: shared enhancer-like elements drive their coexpression in proneural clusters of the imaginal discs. Genes Dev 9:1869–1882PubMedGoogle Scholar
  15. Gomez-Skarmeta JL, del Corral RD, de la Calle-Mustienes E, Ferre-Marco D, Modolell J (1996) Araucan and caupolican, two members of the novel iroquois complex, encode homeoproteins that control proneural and vein-forming genes. Cell 85:95–105PubMedCrossRefGoogle Scholar
  16. Haenlin M, Cubadda Y, Blondeau F, Heitzler P, Lutz Y, Simpson P, Ramain P (1997) 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 11:3096–3108PubMedGoogle Scholar
  17. Heitzler P, Haenlin M, Ramain P, Calleja M, Simpson P (1996) A genetic analysis of pannier, a gene necessary for viability of dorsal tissues and bristle positioning in Drosophila. Genetics 143:1271–1286PubMedGoogle Scholar
  18. Herranz H, Morata G (2001) The functions of pannier during Drosophila embryogenesis. Development 128:4837–4846PubMedGoogle Scholar
  19. Lee JC, VijayRaghavan K, Celniker SE, Tanouy MA (1995) Identification of a Drosophila muscle development gene with structural homology to mammalian early growth response transcription factors. Proc Natl Acad Sci USA 92:10344–10348PubMedCrossRefGoogle Scholar
  20. Levine J, Hughes M (1973) Stereotaxic map of muscle fibres in indirect flight muscles of Drosophila melanogaster. J Morphol 140:153–158CrossRefGoogle Scholar
  21. Lewis MA (2005) Characterisation of regulatory factors of achaetescute in Anopheles gambiae. Ph.D. thesis, University of CambridgeGoogle Scholar
  22. Leyns L, Gomez-Skarmeta JL, Dambly-Chaudiere C (1996) iroquois: a prepattern gene that controls the formation of bristles on the thorax of Drosophila. Mech Dev 59:63–72PubMedCrossRefGoogle Scholar
  23. Mann RS, Morata G (2000) The developmental and molecular biology of genes that subdivide the body of Drosophila. Annu Rev Cell Dev Biol 16:243–271PubMedCrossRefGoogle Scholar
  24. McAlpine JF (1981) Manual of nearctic diptera. Research Branch, Agriculture Canada, OttawaGoogle Scholar
  25. Melzer RR, Sprenger J, Nicastro D, Smola U (1999) Larva-adult relationships in an ancestral dipteran: a re-examination of sensillar pathways across the antenna and leg anlagen of Chaoborus crystallinus (DeGeer, 1776; Chaoboridae). Dev Genes Evol 209:103–112PubMedCrossRefGoogle Scholar
  26. Modolell J, Campuzano S (1998) The achaetescute complex as an integrating device. Int J Dev Biol 42:275–282PubMedGoogle Scholar
  27. Neumann D, Spindler KD (1991) Circasemilunar control of imaginal disc development in Clunio marinus: temporal switching point, temperature-compensated developmental time and ecdysteroid profile. J Insect Physiol 37:101–109CrossRefGoogle Scholar
  28. Nishiura JT (2002) Coordinated morphological changes in midgut, imaginal discs and respiratory trumpets during metamorphosis of Aedes Aegypti (Diptera: Culicidae). Ann Entomol Soc Am 95:498–504CrossRefGoogle Scholar
  29. Phillips RG, Whittle JR (1993) Wingless expression mediates determination of peripheral nervous system elements in late stages of Drosophila wing disc development. Development 118:427–438PubMedGoogle Scholar
  30. Pistillo D, Skaer N, Simpson P (2002) scute expression in Calliphora vicina reveals an ancestral pattern of longitudinal stripes on the thorax of higher Diptera. Development 129:563–572PubMedGoogle Scholar
  31. Ramain P, Heitzler P, Haenlin M, Simpson P (1993) Pannier, a negative regulator of achaete and scute in Drosophila, encodes a zinc finger protein with homology to the vertebrate transcription factor GATA-1. Development 119:1277–1291PubMedGoogle Scholar
  32. Ramain P, Khechumian R, Khechumian K, Arbogast N, Ackermann C, Heitzler P (2000) Interactions between chip and the achaete/scute-daughterless heterodimers are required for pannier-driven proneural patterning. Mol Cell 6:781–790PubMedCrossRefGoogle Scholar
  33. Richardson J, Simpson P (2006) A conserved trans-regulatory landscape for scute expression on the notum of cyclorraphous Diptera. Dev Genes Evol 216(1):29–38PubMedCrossRefGoogle Scholar
  34. Ruiz-Gomez M, Modolell J (1987) Deletion analysis of the achaetescute locus of Drosophila melanogaster. Genes Dev 1:1238–1246PubMedGoogle Scholar
  35. Simpson P, Woehl R, Usui K (1999) The development and evolution of bristle patterns in Diptera. Development 126:1349–1364PubMedGoogle Scholar
  36. Skaer N, Pistillo D, Gibert JM, Lio P, Wulbeck C, Simpson P (2002) Gene duplication at the achaetescute complex and morphological complexity of the peripheral nervous system in Diptera. Trends Genet 18:399–405PubMedCrossRefGoogle Scholar
  37. Skeath JB, Carroll SB (1991) Regulation of achaetescute gene expression and sensory organ pattern formation in the Drosophila wing. Genes Dev 5:984–995PubMedGoogle Scholar
  38. Spinner W (1969) Transplantationsversuche zur Blastemgliederung, Regenerations- und Differenzierungsleistung der Beinanlagan von Culex pipiens. Wilhelm Roux’ Arch 163:259–286CrossRefGoogle Scholar
  39. Sudarsan V, Anant S, Guptan P, VijayRaghavan K, Skaer H (2001) Myoblast diversification and ectodermal signaling in Drosophila. Dev Cell 1:829–839PubMedCrossRefGoogle Scholar
  40. Tiegs O (1955) The flight muscles of insects—their anatomy and histology; with some observations on the structure of striated muscle in general. Philos Trans R Soc Lond B Biol Sci 238:221–359Google Scholar
  41. Usui K, Pistillo D, Simpson P (2004) Mutual exclusion of sensory bristles and tendons on the notum of dipteran flies. Curr Biol 14:1047–1055PubMedCrossRefGoogle Scholar
  42. Villares R, Cabrera CV (1987) The achaetescute gene complex of D. melanogaster: conserved domains in a subset of genes required for neurogenesis and their homology to myc. Cell 50:415–424PubMedCrossRefGoogle Scholar
  43. Volk T (1999) Singling out Drosophila tendon cells: a dialogue between two distinct cell types. Trends Genet 15:448–453PubMedCrossRefGoogle Scholar
  44. Wheeler SR, Carrico ML, Wilson BA, Brown SJ, Skeath JB (2003) The expression and function of the achaetescute genes in Tribolium castaneum reveals conservation and variation in neural pattern formation and cell fate specification. Development 130:4373–4381PubMedCrossRefGoogle Scholar
  45. Wülbeck C, Simpson P (2000) Expression of achaete–scute homologues in discrete proneural clusters on the developing notum of the medfly Ceratitis capitata, suggests a common origin for the stereotyped bristle patterns of higher Diptera. Development 127:1411–1420PubMedGoogle Scholar
  46. Wülbeck C, Simpson P (2002) The expression of pannier and achaetescute homologues in a mosquito suggests an ancient role of pannier as a selector gene in the regulation of the dorsal body pattern. Development 129:3861–3871PubMedGoogle Scholar

Copyright information

© Springer-Verlag 2006

Authors and Affiliations

  1. 1.Department of ZoologyUniversity of CambridgeCambridgeUK
  2. 2.Department of Biomedical ScienceFirth Court, Western BankSheffieldUK

Personalised recommendations