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Expression of a cell surface protein during morphogenesis of the reproductive system in Manduca sexta embryos

Both moths and mammals have an indifferent stage of genital differentiation

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Abstract

New antibody markers have allowed more refined examinations of embryogenesis. Features are being found that were overlooked in whole and sectioned embryos stained with traditional histochemical labels. Two monoclonal antibodies that recognize two different cell surface proteins in Manduca sexta label cells of the developing reproductive system. These specific immunolabels reveal that during a brief period of Manduca embryogenesis, rudiments of both male and female genital ducts are present in a single embryo. This transient phase of genital differentiation parallels the transient indifferent stage known to occur during development of reproductive systems in many vertebrate embryos. At the end of this indifferent stage, one of the two pairs of genital ducts retracts and degenerates. The dynamic expression of the two surface proteins on cells involved in morphogenesis of both the female and male reproductive systems also suggests that these proteins are important in orchestrating the specific cellular interactions that occur between mesodermal cells of the genital ducts and the nearby ventral ectoderm.

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References

  • Anderson DT (1972a) The development of holometabolous insects. In: Counce SJ, Waddington CH (eds) Developmental systems: insects. Academic Press, London New York, pp 165–242

    Google Scholar 

  • Anderson DT (1972b) The development of hemimetabolous insects. In: Counce SJ, Waddington CH (eds) Developmental systems: insects. Academic Press, London New York, pp 95–163

    Google Scholar 

  • Bate M (1993) The mesoderm and its derivatives. In: Bate, M. Martinez Arias A (eds) The development of Drosophila melanogaster. Cold Spring Harbor Laboratory Press, pp 1013–1090

  • Bieber AJ, Snow PM, Hortsch M, Patel NH, Jacobs JR, Traquina ZR, Schilling J, Goodman CS (1989) Drosophila neuroglian: A member of the immunoglobulin superfamily with extensive homology to the vertebrate neural adhesion molecule L1. Cell 59:447–460

    Google Scholar 

  • Broadie KS, Bate M, Tublitz NJ (1991) Quantitative staging of embryonic development of the tobacco hawkmoth, Manduca sexta. Roux's Arch Dev Biol 199:327–334

    Google Scholar 

  • Brookman JJ, Toosy AT, Shashidhara LS, White RAH (1992) The 412 retrotransposon and the development of gonadal mesoderm in Drosophila. Development 116:1185–1182

    Google Scholar 

  • Carr JN, Taghert PH (1988) Formation of the transverse nerve in moth embryos. I. A scaffold of nonneuronal cells prefigures the nerve. Dev Biol 130:487–499

    Google Scholar 

  • Cohen SM (1993) Imaginal disc development. In: Bate M, Martinez Arias A (eds) The development of Drosophila melanogaster. Cold Spring Harbor Laboratory Press, pp 747–841

  • Copenhaver PF, Taghert PH (1989) Development of the enteric nervous system is the moth. I. Diversity of cell types and the embryonic expression of FRMF amide related neuropeptides. Dev Biol 131:70–84

    Google Scholar 

  • Demerec M (1965) Biology of Drosophila. Hafner, New York and London

    Google Scholar 

  • Epper F, Nöthiger R (1982) Genetic and developmental evidence for a repressed genital primordium in Drosophila melanogaster. Dev Biol 94:163–175

    Google Scholar 

  • Gilbert SF (1994) Developmental biology, Sinauer, Sunderland, MA, USA

    Google Scholar 

  • Grenningloh G, Rehm EJ, Goodman CS (1991) Genetic analysis of growth cone guidance in Drosophila: fasciclin II functions as a neuronal recognition molecule. Cell 67:45–57

    Google Scholar 

  • Gruenwald P (1952) Development of the excretory system. Ann NY Acad Sci 55:142–146

    Google Scholar 

  • Harrelson AL, Goodman CS (1988) Growth cone guidance in insects: fasciclin II is a member of the immunoglobulin superfamily. Science 242:700–708

    Google Scholar 

  • Horsfall WR, Anderson JF (1961) Suppression of male characteristics of mosquitoes by thermal means. Science 133:1830

    Google Scholar 

  • Horsfall WR, Ronquillo MC, Patterson WH (1972) Genesis of the reproductive system of mosquitoes IV: thermal modification of Aedes stimulans. Israel J Entomol 7:73–84

    Google Scholar 

  • Lawrence PA, Johnston P (1986) Observations on cell lineage of internal organs of Drosophila. J Embryol Exp Morphol 91:251–266

    Google Scholar 

  • Lewis EB (1978) A gene complex controlling segmentation in Drosophila. Nature 276:565–570

    Google Scholar 

  • Matsuda R (1976) Morphology and evolution of the insect abdomen. Pergamon Press, Oxford

    Google Scholar 

  • Nardi JB (1990) Expression of a surface epitope on cells that link branches in the tracheal network of Manduca sexta. Development 110:682–688

    Google Scholar 

  • Nardi JB (1992) Dynamic expression of a cell surface protein during rearrangement of epithelial cells in the Manduca wing monolayer. Dev Biol 152:161–171

    Google Scholar 

  • Nardi JB (1993) Modulated expression of a surface epitope on migrating germ cells of Manduca sexta embryos. Development 118:967–975

    Google Scholar 

  • Poole TJ, Steinberg MS (1982) Evidence for the guidance of pronephric duct migration by a craniocaudally traveling adhesive gradient. Dev Biol 92:144–158

    Google Scholar 

  • Snodgrass RE (1935) Principles of insect morphology. McGraw-Hill, New York London

    Google Scholar 

  • Sommer RJ, Steinberg PW (1994) Changes of induction and competence during the evolution of vulva development in nematodes. Science 265:114–118

    Google Scholar 

  • Wheeler WM (1893) A contribution to insect embryology. J Morphol 8:1–160

    Google Scholar 

  • Wieschaus E, Nöthiger R (1982) The role of the transformer genes in the development of genitalia and analia of Drosophila melanogaster. Dev Biol 90:320–334

    Google Scholar 

  • Zackson SL, Steinberg MS (1987) Chemotaxis or adhesion gradient? Pronephric duct elongation does not depend on distant sources of guidance information. Dev Biol 124:418–422

    Google Scholar 

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Nardi, J.B., Cattani, E.G. Expression of a cell surface protein during morphogenesis of the reproductive system in Manduca sexta embryos. Roux's Arch Dev Biol 205, 21–30 (1995). https://doi.org/10.1007/BF00188840

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  • DOI: https://doi.org/10.1007/BF00188840

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