Transformation of external sensilla to chordotonal sensilla in the cut mutant of Drosophila assessed by single-cell marking in the embryo and larva

Microscopy Research and Technique

Volumn 39, Issue 6, 1997, Pages 492-505

  Merritt, David John ^a,b  

^a UNIVERSITY OF NEW ENGLAND   (Australia)

^b UNIVERSITY OF QUEENSLAND   (Australia)

Author keywords

DiI; Fluorescent tracers; Insect sense organs; Proneural genes

Indexed keywords

CYTOLOGY; FLUORESCENCE; MOLECULAR BIOLOGY;

DII; DROSOPHILLA; DROSOPHILLA MELANOGASTER; EXTERNAL SENSE; FLUORESCENT TRACERS; INSECT SENSE ORGAN; PRONEURAL GENE; SENSE ORGANS; SENSILLAE; SINGLE CELLS;

GENES;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; DROSOPHILA; EMBRYO; GENE MUTATION; IMMUNOHISTOCHEMISTRY; LARVAL DEVELOPMENT; MICROSCOPY; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; PHYLOGENY; PRIORITY JOURNAL; SENSE ORGAN;

ANIMALIA; ARTHROPODA; CRUSTACEA; DROSOPHILA MELANOGASTER; INSECTA; MELANOGASTER;

EID: 0031470658     PISSN: 1059910X     EISSN: None     Source Type: Journal    
DOI: 10.1002/(SICI)1097-0029(19971215)39:6<492::AID-JEMT4>3.0.CO;2-G     Document Type: Article

References (87)

1. Altner, H., and Thies, G. (1984) Internal proprioceptive organs of the distal antennal segments in Allacma fusca (L.) (Collembola: Sminthurindae): Proprioceptors phylogenetically derived from sensillum-bound exteroceptors. Int. J. Insect Morphol. Embryol., 13:315-330.
2. Altner, H., Tichy, H., and Altner, I. (1978) Lamellated outer dendritic segments of a sensory cell within a poreless thermo- and hygroreceptive sensillum of the insect Carausius morosus. Cell Tissue Res., 191:287-304.
3. Altner, I., Hatt, H., and Altner, H. (1983) Structural properties of bimodal chemo- and mechanosensitive setae on the pereiopod chelae of the crayfish, Austropotamobius torrentium. Cell Tissue Res., 228:357-374.
4. Averof, M., and Akam, M. (1995) Insect-crustacean relationships: Insights from comparative developmental and molecular studies. Philos. Trans. R. Soc. Lond. [Biol.], 347:293-303.
5. Ballard, J.W.O., Olsen, G.J., Faith, D.P., Odgers, W.A., Rowell, D.M., and Atkinson, P.W. (1992) Evidence from 12S ribosomal RNA sequences that onychophorans are modified arthropods. Science, 258:1345-1348.
6. Bate, C.M. (1978) Development of sensory systems in arthropods. In: Handbook of Sensory Physiology. Development of Sensory Systems, Vol. 9. M. Jacobson, ed. Springer Verlag, Berlin, pp. 1-53.
7. Blöchl, R., and Selzer, R. (1988) Embryogenesis of the connective chordotonal organ in the pedicel of the American cockroach: Cell lineage and morphological differentiation. Cell Tissue Res., 252:669-678.
8. Blochlinger, K., Bodmer, R., Jack, J., Jan, L.Y., and Jan, Y.N. (1988) Primary structure and expression of a product from cut, a locus involved in specifying sensory organ identity in Drosophila. Nature, 333:629-635.
9. Blochlinger, K., Bodmer, R., Jan, L.Y., and Jan, Y.N. (1990) Patterns of expression of Cut, a protein required for external sensory organ development in wild-type and cut mutant Drosophila embryos. Genes Dev., 4:1322-1331.
10. Blochlinger, K., Jan, L.Y., and Jan, Y.N. (1991) Transformation of sensory organ identity by ectopic expression of cut in Drosophila. Genes Dev., 5:1124-1135.
11. Bloom, J.W., Zacharuk, R.Y, and Holodniuk, A.E. (1982) Ultrastructure of the larval antenna of Tenebrio molitor L. (Coleoptera: Tenebrionidae): Structure of the blunt-tipped peg and papillate sensilla. Can. J. Zool., 60:1545-1556.
12. Bodmer, R., Barbel, S., Sheperd, S., Jack, J.W., Jan, L.Y, and Jan, Y.N. (1987) Transformation of sensory organs by mutations of the cut locus of D. melanogaster. Cell, 51:293-307.
13. Bodmer, R., Caretto, R., and Jan, Y.N. (1989) Neurogenesis of the peripheral nervous system in Drosophila embryos: DNA replication patterns and cell lineages. Neuron, 3:21-32.
14. Boo, K.S., and Richards, A.G. (1975) Fine structure of the scolopidia in the Johnston's organ of male Aedes aegypti (L.) (Diptera: Culicidae). Int. J. Insect Morphol. Embryol., 4:549-566.
15. Boyan, G.S. (1993) Another look at insect audition: The tympanic receptors as an evolutionary specialization of the chordotonal system. J. Insect Physiol., 39:187-200.
16. Brewster, R. and Bodner, R. (1995) Origin and specification of type II sensory neurons in Drosophila. Development. 121:2923-2936.
17. Cagan, R.L., and Ready, D.F. (1989) The emergence of order in the Drosophila pupal retina. Dev. Biol., 136:346-362.
18. Campos-Ortega, J.A., and Hartenstein, V. (1985) The Embryonic Development of Drosophila melanogaster. Springer, Berlin, 227 pp.
19. Campuzano, S., and Modolell, J. (1992) Patterning of the Drosophila nervous system: The achaete-scute gene complex. Trends Genet., 8:202-208.
20. Chu-Wang, I., and Axtell, R. (1971) Fine structure of the dorsal organ of the house fly larva, Musca domestica L. Z. Zellforsch., 117:17-34.
21. Chu-Wang, I., and Axtell, R.C. (1972a) Fine structure of the ventral organ of the house fly larva, Musca domestica L. Z. Zellforsch., 130:489-495.
22. Chu-Wang, I., and Axtell, R.C. (1972b) Fine structure of the terminal organ of the house fly larva, Musca domestica L. Z. Zellforsch., 127:287-305.
23. Crouau, Y., Bauby, A., and Deharveng, L. (1987) Fine structure of the tibiotarsal and pretarsal sensory organs in Monobella grassei banyulensis (Collembola: Neanuridae). Int. J. Insect Morphol. Embryol., 16:245-261.
24. Dambly-Chaudière, C., and Ghysen, A. (1987) Independent subpatterns of sense organs require independent genes of the achaete-scute complex in Drosophila larvae. Genes Dev., 1:297-306.
25. Dambly-Chaudière, C., Jamet, E., Burri, M., Bopp, D., Basler, K., Hafen, E., Dumont, N., Spielmann, P., Ghysen, A., and Noll, M. (1992) The paired box gene pox neuro: A determinant of poly-innervated sense organs in Drosophila. Cell, 69:159-172.
26. De Kramer, J.J., and Van Der Molen, L.G. (1984) Development of labellar taste hairs in the blowfly, Calliphora vicina (Insecta, Diptera). Zoomorphology, 104:1-10.
27. Foelix, R.F. (1985) Mechano- and chemoreceptive sensilla. In: Neurobiology of the Arachnids. F. Barth, ed. Springer, Berlin, pp. 118-137.
28. Ghysen, A., and Dambly-Chaudière, C. (1992) Development of the peripheral nervous system in Drosophila. In: Determinants of Neuronal Identity. M. Shankland and E.R. Macagno, eds. Academic Press, San Diego, pp. 225-292.
29. Ghysen, A., and Dambly-Chaudière, C. (1993) The specification of sensory neuron identity in Drosophila. Bioessays, 15:293-298.
30. Ghysen, A., Dambly-Chaudière, C., Aceves, E., Jan, L.Y., and Jan, Y.N. (1986) Sensory neurons and peripheral pathways in Drosophila embryos. Roux Arch. Dev. Biol., 195:281-289.
31. Ghysen, A., Dambly-Chaudière, C., Jan, L.Y., and Jan, Y.N. (1993) Cell interactions and gene interactions in peripheral neurogenesis. Genes Dev., 7:723-733.
32. Guse, G.-W. (1978) Antennal sensilla of Neomysis integer (Leach). Protoplasma, 95:145-161.
33. Hallberg, E. (1984) Paracrystalline inclusions in the cilia of the sensory cells in Johnston's organ of Calliphora erythrocephala Meigen (Diptera: Calliphoridae). Int. J. Insect Morphol. Embryol., 13:77-79.
34. Hansen, K., and Hansen-Delkeskamp, E. (1983) The development of taste and tactile hairs in the pharate fly Protophormia terraenovae (Diptera, Calliphoridae) and in the embryonal cricket Acheta domestica (Orthopteroidea, Ensifera). Zoomorphology, 102:241-259.
35. Hartenstein, V. (1988) Development of Drosophila larval sensory organs: Spatiotemporal pattern of sensory neurones, peripheral axonal pathways and sensilla differentiation. Development, 102:869-886.
36. Jan, Y.N., and Jan, L.Y. (1993) The peripheral nervous system. In: The Development of Drosophila melanogaster, Vol. 2. M. Bate and A. Martinez-Arias, eds. Cold Spring Harbor Laboratory Press, Plainview, pp. 1207-1244.
37. Jan, Y.N., and Jan, L.Y. (1994) Genetic control of cell fate specification in Drosophila peripheral nervous system. Annu. Rev. Genet., 28:373-393.
38. Jarman, A.P., Grau, Y., Jan, L.Y., and Jan, Y.N. (1993) atonal is a proneural gene that directs chordotonal organ formation in the Drosophila peripheral nervous system. Cell, 73:1307-1321.
39. Keil, T.A. (1978) Die Makrochaeten auf dem Thorax von Calliphora vicina Robineau-Desvoidy (Calliphoridae, Diptera). Zoomorphologie, 90:151-180.
40. Keil, T.A., and Steiner, C. (1991) Morphogenesis of the antenna of the male silkmoth, Antheraea polyphemus. III. Development of olfactory sensilla and the properties of hair-forming cells. Tissue Cell, 23:821-851.
41. Kouyama, N., and Shimozawa, T. (1982) The structure of a hair mechanoreceptor in the antennule of crayfish (Crustacea). Cell Tissue Res., 226:565-578.
42. Kuhbandner, B. (1984) Ultrastructure and ontogeny of the hair sensilla on the funicle of Calliphora erythrocephala (Insecta, Diptera). I. The basiconical sensilla. Zoomorphology, 104:373-385.
43. Kuhbandner, B. (1985) Ultrastructure and ontogeny of the double-walled sensilla on the funicle of Calliphora erythrocephala Meigen (Diptera: Calliphoridae). Int. J. Insect Morphol. Embryol., 14:227-242.
44. Kutsch, W., and Breidbach, O. (1994) Homologous structures in the nervous systems of Arthropoda. Adv. Insect Physiol., 24:1-113.
45. Lakes-Harlan, R., Pollack, G.S., and Merritt, D.J. (1991) From embryo to adult: Anatomy and development of a leg sensory organ in Phormia regina Meigen (Insecta: Diptera). I. Anatomy and physiology of a larval "leg" sensory organ. J. Comp. Neurol., 308:188-199.
46. Lee, J.-K., and Altner, H. (1985) Sensory cell degeneration in the ontogeny of the chemosensitive sensilla in the labial palp-pit organ of the butterfly, Pieris rapae L. (Insecta, Lepidoptera). Cell Tissue Res., 242:279-288.
47. Matthews, K.A., Miller, D.F.B., and Kaufman, T.C. (1990) Functional implications of the unusual spatial distribution of a minor α-tubulin isotype in Drosophila: A common thread among chordotonal ligaments, developing muscle, and testis cyst cells. Dev. Biol., 137:171-183.
48. McGinnis, W., and Krumlauf, R. (1992) Homeobox genes and axial patterning. Cell, 68:283-302.
49. McIver, S.B. (1985) Mechanoreception. In: Comprehensive Insect Physiology, Biochemistry, and Pharmacology, Vol. 6. G. Kerkut and L. Gilbert, eds. Pergamon, Oxford, pp. 71-132.
50. Meier, T., and Reichert, H. (1995) Developmental mechanisms, homology and evolution of the insect peripheral nervous system. In: The Nervous Systems of Invertebrates: An Evolutionary and Comparative Approach. O. Breidbach and W. Kutsch, eds. Birkhäuser Verlag, Basel, pp. 249-271.
51. Meier, T., Chabaud, F., and Reichert, H. (1991) Homologous patterns in the embryonic development of the peripheral nervous system in the grasshopper Schistocerca gregaria and the fly Drosophila melanogaster. Development, 112:241-253.
52. Merritt, D.J. (1987) The cereal sensilla of the blowfly Lucilia cuprina. I. Structure of the sockets and distal dendritic regions. Tissue Cell 19:287-299.
53. Merritt, D.J. (1989) The cereal sensilla of the blowfly, Lucilia cuprina. II. Structure of the enveloping cells and basal regions of the sensory dendrites. Tissue Cell, 21:281-298.
54. Merritt, D.J., and Whitington, P.M. (1995) Central projections of sensory neurons in the Drosophila embryo correlate with sensory modality, soma position and proneural gene function. J. Neurosci., 15:1755-1767.
55. Merritt, D.J., Hawken, A., and Whitington, P.M. (1993) The role of the cut gene in the specification of central projections by sensory axons in Drosophila. Neuron, 10:741-752.
56. Moulins, M. (1976) Ultrastructure of chordotonal organs. In: Structure and Function of Proprioceptors in the Invertebrates. P. Mill, ed. Chapman and Hall, London, pp. 387-426.
57. Nayak, S.V., and Singh, R.N. (1983) Sensilla on the tarsal segments and mouthparts of adult Drosophila melanogaster Meigen (Diptera: Drosophilidae). Int. J. Insect Morphol. Embryol., 12:273-291.
58. Nottebohm, E., Dambfy-Chaudière, C., and Ghysen, A. (1992) Connectivity of chemosensory neurons is controlled by the gene poxn in Drosophila. Nature, 359:829-832.
59. Osorio, D., and Bacon, J.P. (1994) A good eye for arthropod evolution. Bioessays, 16:419-424.
60. Pappas, L.G., and Larsen, J.R. (1976) Labellar chordotonal organs of the mosquito, Culiseta inornata (Williston) (Diptera: Culicidae). Int. J. Insect Morphol. Embryol., 5:145-150.
61. Posakony, J.W. (1994) Nature versus nurture: Asymmetric cell divisions in Drosophila bristle development. Cell, 76:415-418.
62. Rice, M.J. (1975) Insect mechanoreceptor mechanisms. In: Sensory Physiology and Behavior. R. Galun, P. Hillman, I. Parnas, and R. Werman, eds. Plenum, New York, pp. 135-165.
63. Rodríguez, I., Hernández, R., Modolell, J., and Ruiz-Gómez, M. (1990) Competence to develop sensory organs is temporally and spatially regulated in Drosophila epidermal primordia. EMBO J., 9:3583-3592.
64. Schmidt, K. (1969) Der Feinbau der stiftführenden Sinnesorgane im Pedicellus def Florfliege Chrysopa Leach (Chrysopidae, Planipennia). Z. Zellforsch., 99:357-388.
65. Schmidt, M., and Gnatzy, W. (1984) Are the funnel-canal organs the "campaniform sensilla" of the shore crab, Carcinus maenas (Decapoda, Crustacea)? II. Ultrastructure. Cell Tissue Res., 237:81-93.
66. Seidl, S. (1991) Structure and differentiation of the sensilla of the ventral sensory field on the maxillary palps of Periplaneta americana (Insecta, Blattodea), paying special attention to the ciliogenesis of the sensory cells. Zoomorphology, 111:35-47.
67. Seifert, P., and Heinzeller, T. (1989) Mechanical, sensory and glandular structures in the tarsal unguitractor apparatus of Chironomus riparius (Diptera, Chironomidae). Zoomorphology, 109:71-78.
68. Shanbhag, S.R., Singh, K., and Singh, R.N. (1992) Ultrastructure of the femoral chordotonal organs and their novel synaptic organization in the legs of Drosophila melanogaster Meigen (Diptera, Drosophilidae). Int. J. Insect Morphol. Embryol., 21:311-322.
69. Singh, R.N., and Nayak, S.V. (1985) Fine structure and primary sensory projections of sensilla on the maxillary palp of Drosophila melanogaster Meigen (Diptera: Drosophilidae). Int. J. Insect Morphol. Embryol., 14:291-306.
70. Singh, R.N., and Singh, K. (1984) Fine structure of the sensory organs of Drosophila melanogaster Meigen larva (Diptera: Drosophilidae). Int. J. Insect Morphol. Embryol., 13:255-273.
71. Skeath, J.B., and Carroll, S.B. (1991) Regulation of achaete-scute gene expression and sensory organ pattern formation in the Drosophila wing. Genes Dev., 5:984-995.
72. Sugawara T. (1996) Chordotonal sensilla embedded in the epidermis of the soft integument of the cricket, Teleogryllus commodus. Cell Tiss. Res., 284:125-142.
73. Uga, S., and Kuwabara, M. (1965) On the fine structure of the chordotonal sensillum in antenna of Drosophila melanogaster. J. Electron Microsc. (Tokyo), 14:173-181.
74. Warren, R.W., Nagy, L., Selegue, J., Gates, J., and Carroll, S. (1994) Evolution of homeotic gene regulation and function in flies and butterflies. Nature, 372:458-461.
75. Whitington, P.M. (1995) Conservation versus change in early axonogenesis in arthropod embryos: A comparison between myriapods, crustaceans and insects. In: The Nervous Systems of Invertebrates: An Evolutionary and Comparative Approach. O. Breidbach and W. Kutsch, eds. Birkhäuser Verlag, Basel, pp. 181-219.
76. Wolfrum, U. (1990) Actin filaments: The main components of the scolopale in insect sensilla. Cell Tissue Res., 261:85-96.
77. Wolfrum, U. (1991a) Tropomyosin is co-localized with the actin filaments of the scolopale in insect sensilla. Cell Tissue Res., 265:11-17.
78. Wolfrum, U. (1991b) Centrin-like and α-actinin-like immunoreactivity in the ciliary rootlets of insect sensilla. Cell Tissue Res., 266:231-238.
79. Wright, K.A. (1980) Nematode sense organs. In: Nematodes as Biological Models, Vol. 2. B. Zuckerman, ed. Academic Press, New York, pp. 237-295.
80. Wright, K.A. (1992) Peripheral sensilla of some lower invertebrates: The Platyhelminthes and Nematoda. Microsc. Res. Tech., 22:285-297.
81. Yack, J.E., and Roots, B.I. (1992) The metathoracic wing-hinge chordotonal organ of an atympanate moth, Actias luna (Lepidoptera, Saturniidae): A light-microscopic and electron-microscopic study. Cell Tissue Res., 267:455-471.
82. Yang, X.H., Yeo, S.L., Dick, T., and Chia, W. (1993) The role of a Drosophila POU homeo domain gene in the specification of neural precursor cell identity in the developing embryonic central nervous system. Genes Dev., 7:504-516.
83. Yokohari, F. (1981) The sensillum capitulum, an antennal hygro- and thermoreceptive sensillum of the cockroach, Periplaneta americana. Cell Tissue Res., 216:525-543.
84. Zacharuk, R.Y. (1985) Antennae and sensilla. In: Comprehensive Insect Physiology, Biochemistry, and Pharmacology, Vol. 6. G. Kerkut and L. Gilbert, eds. Pergamon, Oxford, pp. 1-69.
85. Zawarzin, A. (1912) Histologische Studien über Insekten. III. Über das sensible Nervensystem der Larven von Melolontha vulgaris. Z. Wiss. Zool., 100:447-458.
86. Zhao, C., and Emmons, S.W. (1995) A transcription factor controlling development of peripheral sense organs in C. elegans. Nature, 373:74-78.
87. Zimmermann, B. (1991) Differentiation of the thermo-/hygrosensitive (no-pore) sensilla on the antenna of Antheraea pernyi (Lepidoptera, Saturniidae): A study of cryofixed material. Cell Tissue Res., 266:427-440.