Skip to main content
SpringerLink
Log in

Sensitive periods for abnormal patterning on a leg segment inDrosophila melanogaster

  • Published:
Roux's archives of developmental biology Aims and scope Submit manuscript

Summary

The development of a leg segment of the fruitflyDrosophila melanogaster was analyzed in order to determine whether the orderliness of the segment's bristle pattern originates via waves of cellular interactions, such as those that organize the retina. Fly development was perturbed at specific times by either teratogenic agents (gamma rays, heat shock, or the drug mitomycin C) or temperature-sensitive mutations (l(1)63, l(1) Notchts1, orl(1) shibire ts1), and the resulting abnormalities (e.g., missing or extra structures) were mapped within the pattern area. If bristles develop in a linear sequence across the pattern, then they should show sensitivity to perturbations in the same order, and wavefronts of cuticular defects should result. Contrary to this prediction, the maps reveal no evidence for any directional waves of sensitivity. Nevertheless, other clues were uncovered as to the nature and timing of patterning events. Chemosensory bristles show earlier sensitivities than mechanosensory bristles, and longer bristles precede shorter ones. The types and sequence of cuticular abnormalities imply the following stages of bristle pattern development: (1) scattered inception of bristle mother cells, each surrounded by an inhibitory field, (2) alignment of the mother cells into rows, (3) differential mitoses, (4) assignment of cuticular fates to the mitotic progeny, (5) polytenization of the bristle cells, (6) fine-tuning adjustments in bristle spacing, and (7) signalling from bristle cells to adjacent epidermal cells, inducing them to form “bracts”.

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

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Anderson DT (1973) Embryology and Phylogeny in Annelids and Arthropods. Pergamon Pr, New York

    Google Scholar 

  • Arora K, Rodrigues V, Joshi S, Shanbhag S, Siddiqi O (1987) A gene affecting the specificity of the chemosensory neurons ofDrosophila. Nature 330:62–63

    PubMed  Google Scholar 

  • Bainbridge SP, Bownes M (1981) Staging the metamorphosis ofDrosophila melanogaster. J Embryol Exp Morphol 66:57–80

    PubMed  Google Scholar 

  • Banerjee S, Chinya PK (1982) Effect of Mitomycin C on polytene chromosome replication ofDrosophila. Dros Info Serv 58:19–20

    Google Scholar 

  • Belote JM, Baker BS (1982) Sex determination inDrosophila melanogaster: Analysis of transformer-2, a sex-transforming locus. Proc Natl Acad Sci USA 79:1568–1572

    PubMed  Google Scholar 

  • Bodenstein D (1950) The postembryonic development ofDrosophila. In: Demerec M (ed) Biology ofDrosophila. Hafner, New York, pp 275–367

    Google Scholar 

  • Bodmer R, Barbel S, Sheperd S, Jack JW, Jan LY, Jan YN (1987) Transformation of sensory organs by mutations of thecut locus ofD. melanogaster.Cell 51:293–307

    PubMed  Google Scholar 

  • Cagan RL, Ready DF (1989a)Notch is required for successive cell decisions in the developingDrosophila retina. Genes Dev 3:1099–1112

    PubMed  Google Scholar 

  • Cagan RL, Ready DF (1989b) The emergence of order in theDrosophila pupal retina. Dev Biol 136:346–362

    PubMed  Google Scholar 

  • Chadfield CG, Sparrow JC (1985) Pupation inDrosophila melanogaster and the effect of the lethalcryptocephal mutation. Dev Gen 5:103–114

    Google Scholar 

  • Claxton JH (1974) Some quantitative features ofDrosophila sternite bristle patterns. Aust J Biol Sci 27:533–543

    PubMed  Google Scholar 

  • Claxton JH (1976) Developmental origin of even spacing between the microchaetes ofDrosophila melanogaster. Aust J Biol Sci 29:131–135

    PubMed  Google Scholar 

  • Claxton JH (1982) Temporal pattern of bristle development onDrosophila melanogaster sternites. Aust J Biol Sci 35:653–660

    Google Scholar 

  • Cooke J (1981) The problem of periodic patterns in embryos. Phil Trans R Soc Lond B 295:509–524

    Google Scholar 

  • Elsdale T, Pearson M, Whitehead M (1976) Abnormalities in somite segmentation following heat shock toXenopus embryos. J Embryol Exp Morphol 35:625–635

    PubMed  Google Scholar 

  • Ephrussi B, Beadle GW (1936) A technique of transplantation forDrosophila. Am Naturalist 70:218–225

    Google Scholar 

  • Fraenkel G, Bhaskaran G (1973) Pupariation and pupation in cyclorraphous flies (Diptera): Terminology and interpretation. Ann Entomol Soc Am 66:418–422

    Google Scholar 

  • Friesen H (1936) Röntgenmorphosen beiDrosophila. Roux's Arch Dev Biol 134:147–165

    Google Scholar 

  • Fristrom D (1976) The mechanism of evagination of imaginal discs ofDrosophila melanogaster. III. Evidence for cell rearrangement. Dev Biol 54:163–171

    PubMed  Google Scholar 

  • Fristrom D, Fristrom JW (1975) The mechanism of evagination of imaginal discs ofDrosophila melanogaster. I. General considerations. Dev Biol 43:1–23

    PubMed  Google Scholar 

  • Fristrom J (1965) Development of the morphological mutant cryptocephal ofDrosophila melanogaster. Genetics 52:297–318

    PubMed  Google Scholar 

  • Gloor H (1944) Phänokopie einer Letalmutante (crc) vonDrosophila melanogaster. Rev Suisse Zool 51:394–402

    Google Scholar 

  • Graves B, Schubiger G (1981) Regional differences in the developing foreleg ofDrosophila melanogaster. Dev Biol 85:334–343

    PubMed  Google Scholar 

  • Hadorn E, Gloor H (1943) Cryptocephal, ein spät wirkender Letalfaktor beiDrosophila melanogaster. Rev Suisse Zool 50:256–261

    Google Scholar 

  • Hannah-Alava A (1958) Morphology and chaetotaxy of the legs ofDrosophila melanogaster. J Morphol 103:281–310

    Google Scholar 

  • Hansen K, Hansen-Delkeskamp E (1983) The development of taste and tactile hairs in the pharate flyProtophormia terraenovae (Diptera, Calliphoridae) and in the embryonal cricketAcheta domestica (Orthopteroidea, Ensifera). Zoomorphol 102:241–259

    Google Scholar 

  • Hartenstein V (1988) Development ofDrosophila larval sensory organs: spatiotemporal pattern of sensory neurones, peripheral axonal pathways and sensilla differentiation.Development 102:869–886

    Google Scholar 

  • Hartenstein V, Posakony JW (1989) Development of adult sensilla on the wing and notum ofDrosophila melanogaster. Development 107:389–405

    PubMed  Google Scholar 

  • Held LI Jr (1979a) Pattern as a function of cell number and cell size on the second-leg basitarsus ofDrosophila. Roux's Arch Dev Biol 187:105–127

    Google Scholar 

  • Held LI Jr (1979b) A high-resolution morphogenetic map of the second-leg basitarsus inDrosophila melanogaster. Roux's Arch Dev Biol 187:129–150

    Google Scholar 

  • Held LI Jr (1990) Arrangement of bristles as a function of bristle number on a leg segment inDrosophila melanogaster. Roux's Arch Dev Biol 199:48–62

    Google Scholar 

  • Held LI Jr, Bryant PJ (1984) Cell interactions controlling the formation of bristle patterns inDrosophila. In: Malacinski GM, Bryant SV (eds) Pattern formation: a primer in developmental biology. Macmillan Pub Co, New York, pp 291–322

    Google Scholar 

  • Held LI Jr, Duarte CM, Derakhshanian K (1986) Extra tarsal joints and abnormal cuticular polarities in various mutants ofDrosophila melanogaster. Roux's Arch Dev Biol 195:145–157

    Google Scholar 

  • Held LI Jr, Pham TT (1983) Accuracy of bristle placement on a leg segment inDrosophila melanogaster. J Morphol 178:105–110

    Google Scholar 

  • Henke K, v. Finck E, Ma S-Y (1941) Über sensible Perioden für die Auslösung von Hitzemodifikationen beiDrosophila und die Beziehungen zwischen Modifikationen und Mutationen. Z Vererbgsl 79:267–316

    Google Scholar 

  • Hollingsworth MJ (1964) Sex-combs of intersexes and the arrangement of the chaetae on the legs ofDrosophila. J Morphol 115:35–51

    Google Scholar 

  • Huxley JS, De Beer GR (1934) The Elements of experimental embryology. Cambridge University Press, London

    Google Scholar 

  • Jacobson AG (1988) Somitomeres: mesodermal segments of vertebrate embryos.Development [Suppl] 104:209–220

    Google Scholar 

  • Keil TA, Steinbrecht RA (1984) Mechanosensitive and olfactory sensilla of insects. In: King RC, Akai H (eds) Insect ultrastructure, vol 2. Plenum Press, New York, pp 477–516

    Google Scholar 

  • Köhler W, Feldotto W (1935) Experimentelle Untersuchungen über die Modifikabilität der Flügelzeichnung, ihrer Systeme und Elemente in den sensiblen Perioden vonVanessa urticae L., nebst einigen Beobachtungen anVanessa io L. Arch J Klaus-Stiftung 10:313–453

    Google Scholar 

  • Krishnakumaran A, Berry SJ, Oberlander H, Schneiderman HA (1967) Nucleic acid synthesis during insect development — II. Control of DNA synthesis in the Cecropia silkworm and other saturniid moths. J Insect Physiol 13:1–57

    Google Scholar 

  • Landauer W (1958) On phenocopies, their developmental physiology and genetic meaning. Am Nat 92:201–213

    Google Scholar 

  • Lawrence PA (1966) Development and determination of hairs and bristles in the milkweed bug,Oncopeltus fasciatus (Lygaeidae, Hemiptera). J Cell Sci 1:475–498

    PubMed  Google Scholar 

  • Lawrence PA (1969) Cellular differentiation and pattern formation during metamorphosis of the milkweed bugOncopeltus. Dev Biol 19:12–40

    PubMed  Google Scholar 

  • Lawrence PA, Struhl G, Morata G (1979) Bristle patterns and compartment boundaries in the tarsi ofDrosophila. J Embryol Exp Morphol 51:195–208

    PubMed  Google Scholar 

  • Lee L-W, Gerhart JC (1973) Dependence of transdetermination frequency on the developmental stage of cultured imaginal discs ofDrosophila melanogaster. Dev Biol 35:62–82

    PubMed  Google Scholar 

  • Lees AD, Waddington CH (1942) The development of the bristles in normal and some mutant types ofDrosophila melanogaster. Proc Roy Soc Lond B 131:87–110

    Google Scholar 

  • Lehmann R, Jiménez F, Dietrich U, Campos-Ortega JA (1983) On the phenotype and development of mutants of early neurogenesis inDrosophila melanogaster. Roux's Arch Dev Biol 192:62–74

    Google Scholar 

  • Lienhard MC, Stocker RF (1987) Sensory projection patterns of supernumerary legs and aristae inD. melanogaster. J Exp Zool 244:187–201

    Google Scholar 

  • Lifschytz E (1978) Uncoupling of gonial and spermatocyte stages by means of conditional lethal mutations inDrosophila melanogaster. Dev Biol 66:571–578

    PubMed  Google Scholar 

  • Lindquist S (1986) The heat-shock response. Ann Rev Biochem 55:1151–1191

    PubMed  Google Scholar 

  • Lindsley DE, Poodry CA (1977) A reversible temperature-induced developmental arrest inDrosophila. Dev Biol 56:213–218

    PubMed  Google Scholar 

  • Lindsley DL, Grell EH (1968) Genetic Variations ofDrosophila melanogaster. Carnegie Inst. of Washington Publ. No. 627, Washington DC

  • Linsenmayer TF (1972) Control of integumentary patterns in the chick. Dev Biol 27:244–271

    PubMed  Google Scholar 

  • Ma S-Y (1943) Experimentelle Untersuchungen über Hitzemodifikationen des Flügels vonDrosophila melanogaster. Roux's Arch Dev Biol 142:508–618

    Google Scholar 

  • McIver SB (1985) Mechanoreception. In: Kerkut GA, Gilbert LI (eds) Comprehensive insect physiology, biochemistry, and pharmacology, vol 6. Pergamon Press, New York, pp 71–132

    Google Scholar 

  • Mee JE, French V (1986) Disruption of segmentation in a short germ insect embryo. I. The location of abnormalities induced by heat shock. J Embryol Exp Morphol 96:245–266

    PubMed  Google Scholar 

  • Mglinets VA, Kostina IV (1978) Genetic control of bristle length inDrosophila. Genetika 14:285–293

    Google Scholar 

  • Mitchell HK, Lipps LS (1978) Heat shock and phenocopy induction inDrosophila. Cell 15:907–918

    PubMed  Google Scholar 

  • Mitchell HK, Petersen NS (1982) Developmental abnormalities inDrosophila induced by heat shock. Dev Genet 3:91–102

    Google Scholar 

  • Nardi JB, Magee-Adams SM (1986) Formation of scale spacing patterns in a moth wing. I. Epithelial feet may mediate cell rearrangement. Dev Biol 116:278–290

    Google Scholar 

  • Nayak SV, Singh RN (1983) Sensilla on the tarsal segments and mouthparts of adultDrosophila melanogaster Meigen (Diptera: Drosophilidae). Int J Insect Morphol Embryol 12:273–291

    Google Scholar 

  • Palka J, Malone MA, Ellison RL, Wigston DJ (1986) Central projections of identifiedDrosophila sensory neurons in relation to their time of development. J Neurosci 6:182–1830

    Google Scholar 

  • Petersen NS, Young P (1989) Effects of heat shock on protein processing and turnover in developingDrosophila wings. Dev Gen 10:11–15

    Google Scholar 

  • Poodry CA (1975) A temporal pattern in the development of sensory bristles inDrosophila. Roux's Arch Dev Biol 178:203–213

    Google Scholar 

  • Poodry CA (1980) Epidermis: morphology and development. In: Ashburner M, Wright TRF (eds) The Genetics and Biology ofDrosophila, vol. 2d. Academic Press, New York, pp 443–497

    Google Scholar 

  • Poodry CA, Hall L, Suzuki DT (1973) Developmental properties ofshibire ts: A pleiotropic mutation affecting larval and adult locomotion and development. Dev Biol 32:373–386

    PubMed  Google Scholar 

  • Poodry CA, Schneiderman HA (1970) The ultrastructure of the developing leg ofDrosophila melanogaster. Roux's Arch Dev Biol 166:1–44

    Google Scholar 

  • Powsner L (1935) The effects of temperature on the durations of the developmental stages ofDrosophila melanogaster. Physiol Zool 8:474–520

    Google Scholar 

  • Primmett DRN, Stern CD, Keynes RJ (1988) Heat shock causes repeated segmental anomalies in the chick embryo. Development 104:331–339

    PubMed  Google Scholar 

  • Ready DF, Hanson TE, Benzer S (1976) Development of theDrosophila retina, a neurocrystalline lattice. Dev Biol 53:217–240

    PubMed  Google Scholar 

  • Reed CT, Murphy C, Fristrom D (1975) The ultrastructure of the differentiating pupal leg ofDrosophila melanogaster. Roux's Arch Dev Biol 178:285–302

    Google Scholar 

  • Ripoll P, El Messal M, Laran E, Simpson P (1988) A gradient of affinities for sensory bristles across the wing blade ofDrosophila melanogaster.Development 103:757–767

    Google Scholar 

  • Rizki MTM (1960) The effects of glucosamine hydrochloride on the development ofDrosophila melanogaster. Biol Bull 118:308–314

    Google Scholar 

  • Robertson CW (1936) The metamorphosis ofDrosophila melanogaster, including an accurately timed account of the principal morphological changes. J Morphol 59:351–391

    Google Scholar 

  • Rushlow CA, Hogan A, Pinchin SM, Howe KM, Lardelli M, Ish-Horowicz D (1989) TheDrosophila hairy protein acts in both segmentation and bristle patterning and shows homology to N-myc. EMBO J 8:3095–3103

    PubMed  Google Scholar 

  • Sanes JR, Hildebrand JG (1976) Origin and morphogenesis of sensory neurons in an insect antenna. Dev Biol 51:300–319

    PubMed  Google Scholar 

  • Schaerer HR (1976) The action of Mitomycin C on the bristleforming apparatus of Phormia regina. Roux's Arch Dev Biol 179:145–158

    Google Scholar 

  • Shellenbarger DL, Mohler JD (1978) Temperature-sensitive periods and autonomy of pleiotropic effects ofl(1)N ts1, a conditional Notch lethal inDrosophila. Dev Biol 62:432–446

    PubMed  Google Scholar 

  • Smolka H (1958) Untersuchungen an Kleinorganen im Integument der Mehlmotte. Biol Zbl 77:437–478

    Google Scholar 

  • Sybalski W, Iyer VN (1964) Crosslinking of DNA by enzymatically or chemically activated mitomycins and porfiromycins, bifunctionally “alkylating” antibiotics. Fed Proc 23:946–957

    PubMed  Google Scholar 

  • Teugels E, Ghysen A (1983) Two mechanisms for the establishment of sensory projections inDrosophila. Prog Brain Res 58:305–312

    PubMed  Google Scholar 

  • Thomasz M, Lipman R, Chowdary D, Pawlak J, Verdine GL, Nakanishi K (1987) Isolation and structure of a covalent crosslink adduct between Mitomycin C and DNA. Science 235:1204–1208

    PubMed  Google Scholar 

  • Tobler H (1969) Beeinflussung der Borstendifferenzierung und Musterbildung durch Mitomycin beiDrosophila melanogaster. Experientia 25:213–214

    PubMed  Google Scholar 

  • Tobler H, Burckhardt H (1971) Determination of the sensitive phase for bristle organ modifications upon injection of Mitomycin C into larvae and pupae ofDrosophila melanogaster. Experientia 27:189–191

    PubMed  Google Scholar 

  • Tobler H, Rothenbuhler V, Nothiger R (1973) A study of the differentiation of bracts inDrosophila melanogaster using two mutations,H 2 andsv de. Experientia 29:370–371

    PubMed  Google Scholar 

  • Tokunaga C (1962) Cell lineage and differentiation on the male foreleg ofDrosophila melanogaster. Dev Biol 4:489–516

    PubMed  Google Scholar 

  • Tokunaga C, Gerhart JC (1976) The effect of growth and joint formation on bristle pattern inD. melanogaster. J Exp Zool 198:79–96

    PubMed  Google Scholar 

  • Tomlinson A, Ready DF (1986)Sevenless: A cell-specific homeotic mutation of theDrosophila eye. Science 231:400–402

    Google Scholar 

  • Uemura T, Shepherd S, Ackerman L, Jan LY, Jan YN (1989)numb, a gene required in determination of cell fate during sensory organ formation inDrosophila embryos. Cell 58:349–360

    PubMed  Google Scholar 

  • Waddington CH (1942a) Some developmental effects of X-rays inDrosophila. J Exp Biol 19:101–117

    Google Scholar 

  • Waddington CH (1942b) The pupal contraction as an epigenetic crisis inDrosophila. Proc Zool Soc Lond Ser A, 111:181–188

    Google Scholar 

  • Walt H, Tobler H (1978) Ultrastructural analysis of differentiating bristle organs in wild-type,shaven-depilate and Mitomycin Ctreated larvae ofDrosophila melanogaster. Biol Cell 32:291–298

    Google Scholar 

  • Welshons WJ (1965) Analysis of a gene inDrosophila. Science 150:1122–1129

    PubMed  Google Scholar 

Download references

Author information

Author notes

  1. Lewis I. Held Jr.

    Present address: Department of Biological Sciences, Texas Tech University, 79409, Lubbock, Texas, USA

Authors and Affiliations

  1. Developmental Biology Center, University of California, 92717, Irvine, CA, USA

    Lewis I. Held Jr.

Authors
  1. Lewis I. Held Jr.
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Held, L.I. Sensitive periods for abnormal patterning on a leg segment inDrosophila melanogaster . Roux's Arch Dev Biol 199, 31–47 (1990). https://doi.org/10.1007/BF01681531

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF01681531

Key words

Search

Navigation