Skip to main content
SpringerLink
Log in

Metamorphosis and the Formation of the Adult Musculature

  • Chapter
Book cover Muscle Development in Drosophila

Part of the book series: Molecular Biology Intelligence Unit ((MBIU))

Abstract

The somatic musculature of the adult fly consists of muscles that are morphologically and functionally very distinct from each other. How are these diverse muscle types generated during pupal development? This chapter summarizes the insights that have been gained into the genetic and molecular mechanisms that control different steps in patterning, differentiation and diversification of adult muscles.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 129.00
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 169.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 169.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Bate M. The mesoderm and its derivatives. In: Bate M, Martinez-Arias A, eds. The Development of Drosophila melanogaster, Vol. 2. New York: Cold Spring Harbor Laboratory Press, 1993:1013–1090.

    Google Scholar 

  2. Fernandes J, Bate M, VijayRaghavan K. Development of the indirect flight muscles of Drosophila. Development 1991; 113:67–77.

    PubMed  CAS  Google Scholar 

  3. Currie DA, Bate M. The development of adult abdominal muscles in Drosophila: Myoblasts express twist and are associated with nerves. Development 1991; 113:91–102.

    PubMed  CAS  Google Scholar 

  4. Baylies MK, Bate M. Twist: A myogenic switch in Drosophila. Science 1996; 272:1481–1484.

    Article  PubMed  CAS  Google Scholar 

  5. Baylies MK, Bate M, Ruiz-Gomez M. The specification of muscle in Drosophila. Cold Spring Harb Symp Quant Biol 1997; 62:385–93.

    PubMed  CAS  Google Scholar 

  6. Carmena A, Gisselbrecht S, Harrison J et al. Combinatorial signaling codes for the progressive determination of cell fates in the Drosophila embryonic mesoderm. Genes Dev 1998; 12:3910–3922.

    PubMed  CAS  Google Scholar 

  7. Carmena A, Bate M, Jimenez F. Lethal of scute, a proneural gene, participates in the specification of muscle progenitors during Drosophila embryogenesis. Genes Dev 1995; 9:2373–2383.

    PubMed  CAS  Google Scholar 

  8. Baylies MK, Bate M, Ruiz-Gomez M. Myogenesis: A view from Drosophila. Cell 1998; 93:921–927.

    Article  PubMed  CAS  Google Scholar 

  9. Baker R, Schubiger G. Autonomous and nonautonomous notch functions for embryonic muscle and epidermis development in Drosophila. Development 1996; 122:617–626.

    PubMed  CAS  Google Scholar 

  10. Bate M, Rushton E, Frasch M. A dual requirement for neurogenic genes in Drosophila myogenesis. Dev Suppl 1993; 149–161.

    Google Scholar 

  11. Ruiz Gomez M, Bate M. Segregation of myogenic lineages in Drosophila requires numb. Development. 1997; 124:4857–4866.

    PubMed  CAS  Google Scholar 

  12. Carmena A, Murugasu-Oei B, Menon D et al. Inscuteable and numb mediate asymmetric muscle progenitor cell divisions during Drosophila myogenesis. Genes Dev 1998; 12:304–315.

    PubMed  CAS  Google Scholar 

  13. Bate M, Rushton E, Currie DA. Cells with persistent twist expression are the embryonic precursors of adult muscles in Drosophila. Development 1991; 113:79–89.

    PubMed  CAS  Google Scholar 

  14. Broadie KS, Bate M. The development of adult muscles in Drosophila: Ablation of identified muscle precursor cells. Development 1991; 113:103–118.

    PubMed  CAS  Google Scholar 

  15. Lawrence PA. Cell lineage of the thoracic muscles of Drosophila. Cell 1982; 29:493–503.

    Article  PubMed  CAS  Google Scholar 

  16. VijayRaghavan K, Pinto L. The cell lineage of the muscles of the Drosophila head. Embryol Exp Morphol 1985; 85:285–294.

    Google Scholar 

  17. Farrell ER, Fernandes J, Keshishian H. Muscle organizers in Drosophila: The role of persistent larval fibers in adult flight muscle development. Dev Biol 1996; 176:220–229.

    Article  PubMed  CAS  Google Scholar 

  18. Roy S, VijayRaghavan K. Patterning muscles using organizers: Larval muscle templates and adult myoblasts actively interact to pattern the dorsal longitudinal flight muscles of Drosophila. J Cell Biol 1998; 141:1135–1145.

    Article  PubMed  CAS  Google Scholar 

  19. Fernandes J, VijayRaghavan K. The development of indirect flight muscle innervation in Drosoplula melanogaster. Development 1993; 118:215–227.

    Google Scholar 

  20. Consoulas C, Restifo LL, Levine RB. Dendritic remodeling and growth of motoneurons during metamorphosis of Drosophila melanogaster. J Neurosci 2002; 22:4906–4917.

    PubMed  CAS  Google Scholar 

  21. Tissot M, Stocker RF. Metamorphosis in Drosophila and other insects: The rate of neurons throughout the stages. Prog Neurobiol 2000; 62:89–111.

    Article  PubMed  CAS  Google Scholar 

  22. Currie DA, Bate M. Innervation is essential for the development and differentiation of a sex-specific adult muscle in Drosophila melanogaster. Development 1995; 121:2549–2557.

    PubMed  CAS  Google Scholar 

  23. Fernandes JJ, Keshishian H. Nerve-muscle interactions during flight muscle development in Drosophila. Development 1998; 125:1769–1779.

    PubMed  CAS  Google Scholar 

  24. Lawrence PA, Johnston P. The muscle pattern of a segment of Drosophila may be determined by neurons and not by contributing myoblasts. Cell 1986; 45:505–513.

    Article  PubMed  CAS  Google Scholar 

  25. Ito H, Fujitani K, Usui K et al. Sexual orientation in Drosophila is altered by the satori mutation in the sex-determination gene fruitless that encodes a zinc finger protein with a BTB domain. Proc Natl Acad Sci USA 1996; 93:9687–9692.

    Article  PubMed  CAS  Google Scholar 

  26. Taylor BJ, Knittel LM. Sex-specific differentiation of a male-specific abdominal muscle, the muscle of lawrence, is abnormal in hydroxyurea-treated and in fruitless male flies. Development 1995; 121:3079–3088.

    PubMed  CAS  Google Scholar 

  27. Gailey DA, Taylor BJ, Hall JC. Elements of the fruitless locus regulate development of the muscle of Lawrence, a male-specific structure in the abdomen of Drosophila melanogaster adults. Development 1991; 113:879–890.

    PubMed  CAS  Google Scholar 

  28. Usui-Aoki K, Ito H, Ui-Tei K et al. Formation of the male-specific muscle in female Drosophila by ectopic fruitless expression. Nat Cell Biol 2000; 2:500–506.

    Article  PubMed  CAS  Google Scholar 

  29. Fernandes J, Celniker SE, Lewis EB et al. Muscle development in the four-winged Drosophila and the role of the Ultrabithorax gene. Curr Biol 1994; 4:957–964.

    Article  PubMed  CAS  Google Scholar 

  30. Ng M, Diaz-Benjumea FJ, Vincent JP et al. Specification of the wing by localized expression of wingless protein. Nature 1996; 381:316–318.

    Article  PubMed  CAS  Google Scholar 

  31. VijayRaghavan K, Gendre N, Stocker R. Transplanted wing and leg imaginal discs in Drosophila melanogaster demonstrates interactions between epidermis and myoblasts in muscle formation. Dev Genes Evol 1996; 206:46–53.

    Article  Google Scholar 

  32. Fernandes JJ, Celniker SE, VijayRaghavan K. Development of the indirect flight muscle attachment sites in Drosophila: Role of the PS integrins and the stripe gene. Dev Biol 1996; 176:166–184.

    Article  PubMed  CAS  Google Scholar 

  33. Volk T. Singling out Drosophila tendon cells: A dialogue between two distinct cell types. Trends Genet 1999; 15:448–453.

    Article  PubMed  CAS  Google Scholar 

  34. de la Pompa JL, Garcia JR, Ferrus A. Genetic analysis of muscle development in Drosophila melanogaster. Dev Bio 1989; 131:439–454.

    Article  Google Scholar 

  35. Costello WJ, Wyman RJ. Development of an indirect flight muscle in a muscle-specific mutant of Drosophila melanogaster. Dev Biol 1986; 118:247–258.

    Article  PubMed  CAS  Google Scholar 

  36. Sudarsan V, Anant S, Guptan P et al. Myoblast diversification and ectodermal signaling in Drosophila. Dev Cell 2001; 1:829–839.

    Article  PubMed  CAS  Google Scholar 

  37. Ghazi A, Anant S, VijayRaghavan K. Apterous mediates development of direct flight muscles autonomously and indirect flight muscles through epidermal cues. Development 2000; 127:5309–5318.

    PubMed  CAS  Google Scholar 

  38. Bernard F, Lalouette A, Gullaud M et al. Control of apterous by vestigial drives indirect flight muscle development in Drosophila. Dev Biol 2003; 260:391–403.

    Article  PubMed  CAS  Google Scholar 

  39. Bourgouin C, Lundgren SE, Thomas JB. Apterous is a Drosophila LIM domain gene required for the development of a subset of embryonic muscles. Neuron 1992; 9:549–561.

    Article  PubMed  CAS  Google Scholar 

  40. Phillips RG, Whittle JR. Wingless expression mediates determination of peripheral nervous system elements in late stages of Drosophila wing disc development. Development 1993; 118:427–438.

    PubMed  CAS  Google Scholar 

  41. Ruiz-Gomez M, Coutts N, Price A et al. Drosophila dumbfounded: A myoblast attractant essential for fusion. Cell 2000; 102:189–198.

    Article  PubMed  CAS  Google Scholar 

  42. Luo L, Liao YJ, Jan LY et al. Distinct morphogenetic functions of similar small GTPases: Drosophila Drac1 is involved in axonal outgrowth and myoblast fusion. Genes Dev 1994; 8:1787–1802.

    PubMed  CAS  Google Scholar 

  43. Dworak HA, Sink H. Myoblast fusion in Drosophila. BioEssays 2002; 24:591–601.

    Article  PubMed  CAS  Google Scholar 

  44. Taylor MV. Muscle differentiation: How two cells become one. Curr Biol 2002; 12:R224–8.

    Article  PubMed  CAS  Google Scholar 

  45. Anant S, Roy S, VijayRaghavan K. Twist and notch negatively regulate adult muscle differentiation in Drosophila. Development 1998; 125:1361–1369.

    PubMed  CAS  Google Scholar 

  46. Spicer DB, Rhee J, Cheung WL et al. Inhibition of myogenic bHLH and MEF2 transcription factors by the bHLH protein Twist. Science 1996; 272:1476–1480.

    Article  PubMed  CAS  Google Scholar 

  47. Hebrok M, Wertz K, Fuchtbauer EM. M-twist is an inhibitor of muscle differentiation. Dev Biol 1994; 165:537–544.

    Article  PubMed  CAS  Google Scholar 

  48. Lin MH, Bour BA, Abmayr SM et al. Ectopic expression of MEF2 in the epidermis induces epidermal expression of muscle genes and abnormal muscle development in Drosophila. Dev Biol 1997; 182:240–255.

    Article  PubMed  CAS  Google Scholar 

  49. Bour BA, O’Brien MA, Lockwood WL et al. Drosophila MEF2, a transcription factor that is essential for myogenesis. Genes Dev 1995; 9:730–741.

    PubMed  CAS  Google Scholar 

  50. Lilly B, Zhao B, Ranganayakulu G et al. Requirement of MADS domain transcription factor D-MEF2 for muscle formation in Drosophila. Science 1995; 267:688–693.

    Article  PubMed  CAS  Google Scholar 

  51. Olson EN, Perry M, Schulz RA. Regulation of muscle differentiation by the MEF2 family of MADS box transcription factors. Dev Biol 1995; 172:2–14.

    Article  PubMed  CAS  Google Scholar 

  52. Cripps RM, Black BL, Zhao B et al. The myogenic regulatory gene Mef2 is a direct target for transcriptional activation by twist during Drosophila myogenesis. Genes Dev 1998; 12:422–434.

    PubMed  CAS  Google Scholar 

  53. Ranganayakulu G, Zhao B, Dokidis A et al. A series of mutations in the D-MEF2 transcription factor reveal multiple functions in larval and adult myogenesis in Drosophila. Dev Biol 1995; 171:169–181.

    Article  PubMed  CAS  Google Scholar 

  54. Michelson AM. Muscle pattern diversification in Drosophila is determined by the autonomous function of homeotic genes in the embryonic mesoderm. Development 1994; 120:755–768.

    PubMed  CAS  Google Scholar 

  55. Hooper J. Homeotic gene expression in muscles of Drosophila larvae. EMBO J 1986; 5:2321–2329.

    PubMed  Google Scholar 

  56. Volk T, VijayRaghavan K. A central role for epidermal segment border cells in the induction of muscle patterning in the Drosophila embryo. Development 1994; 120:59–70.

    PubMed  CAS  Google Scholar 

  57. Rivlin PK, Gong A, Schneiderman AM et al. The role of Ultrabithorax in the patterning of adult thoracic muscles in Drosophila melanogaster. Dev Genes Evol 2001; 211(2):55–66.

    Article  PubMed  CAS  Google Scholar 

  58. Greig S, Akam M. Homeotic genes autonomously specify one aspect of pattern in the Drosophila mesoderm. Nature 1993; 362:630–632.

    Article  PubMed  CAS  Google Scholar 

  59. Roy S, Shashidhara LS, VijayRaghavan K. Muscles in the Drosophila second thoracic segment are patterned independently of autonomous homeotic gene function. Curr Biol 1997; 7:222–227.

    Article  PubMed  CAS  Google Scholar 

  60. Roy S, VijayRaghavan K. Homeotic genes and the regulation of myoblast migration, fusion, and fibre-specific gene expression during adult myogenesis in Drosophila. Development 1997; 124:3333–3341.

    PubMed  CAS  Google Scholar 

  61. Lawrence PA, Brower DL. Myoblasts from Drosophila wing discs can contribute to developing muscles throughout the fly. Nature 1982; 295:55–57.

    Article  Google Scholar 

  62. Kozopas KM, Nusse R. Direct flight muscles in Drosophila develop from cells with characteristics of founders and depend on DWnt-2 for their correct patterning. Dev Biol 2002; 243:312–325.

    Article  PubMed  CAS  Google Scholar 

  63. Glicksman MA, Brower DL. Expression of the sex combs reduced protein in Drosophila larvae. Dev Biol 1988; 127:113–118.

    Article  PubMed  CAS  Google Scholar 

  64. Lee JC, VijayRaghavan K, Celniker SE et al. Identification of a Drosophila muscle development gene with structural homology to mammalian early growth response transcription factors. Proc Natl Acad Sci USA 1995; 92:10344–10348.

    Article  PubMed  CAS  Google Scholar 

  65. Ghazi A, Paul L, VijayRaghavan K. Prepattern genes and signaling molecules regulate stripe expression to specify Drosophila flight muscle attachment sites. Mech Dev 2003; 120:519–528.

    Article  PubMed  CAS  Google Scholar 

  66. Sandstrom DJ, Restifo LL. Epidermal tendon cells require broad complex function for correct attachment of the indirect flight muscles in Drosophila melanogaster. J Cell Sci 1999; 112:4051–4065.

    PubMed  CAS  Google Scholar 

  67. Sandstrom DJ, Bayer CA, Fristrom JW et al. Broad-complex transcription factors regulate thoracic muscle attachment in Drosophila. Dev Biol 1997; 181:168–185.

    Article  PubMed  CAS  Google Scholar 

  68. Restifo LL, White K. Mutations in a steroid hormone-regulated gene disrupt the metamorphosis of internal tissues in Drosophila: Salivary glands, muscle and gut. Roux’s Arch Dev Biol 1992; 201:221–234.

    Article  CAS  Google Scholar 

  69. Becker S, Pasca G, Strumpf D et al. Reciprocal signaling between Drosophila epidermal muscle attachment cells and their corresponding muscles. Development 1997; 124:2615–2622.

    PubMed  CAS  Google Scholar 

  70. Frommer G, Vorbruggen G, Pasca G et al. Epidermal egr-like zinc finger protein of Drosophila participates in myotube guidance. EMBO J 1996; 15:1642–1649.

    PubMed  CAS  Google Scholar 

  71. Roy S, VijayRaghavan K. Muscle pattern diversification in Drosophila: The story of imaginal myogenesis. BioEssays 1999; 21:486–498.

    Article  PubMed  CAS  Google Scholar 

  72. Lawrence PA, Johnston P. The genetic specification of pattern in a Drosophila muscle. Cell 1984; 36:775–782.

    Article  PubMed  CAS  Google Scholar 

  73. Rivlin PK, Schneiderman AM, Booker R. Imaginal pioneers prefigure the formation of adult thoracic muscles in Drosophila melanogaster. Dev Biol 2000; 222:450–459.

    Article  PubMed  CAS  Google Scholar 

  74. Dutta D, Anant S, Ruiz-Gomez M et al. Founder myoblasts and fibre number during adult myogenesis in Drosophila. Development 2004; 131:3761–3772.

    Article  PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. National Centre for Biological Sciences, Tata Institute of Fundamental Research, Bangalore, 560065, India

    Devkanya Dutta & K. VijayRaghavan

Authors
  1. Devkanya Dutta
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. K. VijayRaghavan
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to K. VijayRaghavan .

Rights and permissions

Reprints and permissions

Copyright information

© 2006 Eurekah.com and Springer Science+Business Media

About this chapter

Cite this chapter

Dutta, D., VijayRaghavan, K. (2006). Metamorphosis and the Formation of the Adult Musculature. In: Muscle Development in Drosophila. Molecular Biology Intelligence Unit. Springer, New York, NY. https://doi.org/10.1007/0-387-32963-3_11

Download citation

Publish with us

Policies and ethics

Search

Navigation