Roux's archives of developmental biology

, Volume 205, Issue 1–2, pp 97–101 | Cite as

Chymotrypsin mRNA expression in digestive gland amoebocytes: cell specification occurs prior to metamorphosis and gut morphogenesis in the gastropod, Haliotis rufescens

  • Bernard M. Degnan
  • Jay C. Groppe
  • Daniel E. Morse
Short Communication

Abstract

In the non-feeding larva of the marine gastropod, Haliotis rufescens, gut morphogenesis is initiated at metamorphosis. Intestine-specific chymotrypsin gene expression begins in amoebocytes located in the dorsoposterior region of the undifferentiated digestive gland prior to metamorphosis, 5 d post-fertilization. Transcript accumulates steadily in these cells over the next 6 d while the amoebocytes migrate slowly dorsally. Induction of metamorphosis dramatically accelerates the rates of chymotrypsin mRNA accumulation and amoebocyte migration, and is required for homing of the amoebocytes to the hindgut region. Induction of chymotrypsin gene expression occurs only in larvae that had developed competence to recognize an exogenous morphogenetic cue and initiate metamorphosis, with a more pronounced increase in chymotrypsin mRNA accumulation in occurring older larvae. Chymotrypsin mRNA accumulation patterns suggest that hindgut cell specification occurs prior to metamorphosis, but that completion of the morphogenetic program requires signaling events associated with metamorphosis.

Key words

Chymotrypsin Larva Metamorphosis Mollusc In situ hybridization 

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References

  1. Barlow LA (1990) Electrophysiological and behavioral responses of larvae of the red abalone (Haliotis rufescens) to settlement-inducing substances. Bull Mar Sci 46:537–554Google Scholar
  2. Barlow LA, Truman JW (1992) Patterns of serotonin and SCP immunoreactivity during metamorphosis of the nervous system of the red abalone, Haliotis rufescens. J Neurobiol 23:829–844Google Scholar
  3. Crofts DR (1929) Haliotis. L.M.B.C. Memoirs XXIX, University Press of Liverpool, LiverpoolGoogle Scholar
  4. Crofts DR (1937) The development of Haliotis tuberculata, with special reference to organogenesis during torsion. Phil Trans Royal Soc London 22813:219–268Google Scholar
  5. Degnan BM, Morse DE (1993) Identification of eight homeoboxcontaining transcripts expressed during larval development and at metamorphosis in the gastropod mollusc Haliotis rufescens. Mol Mar Biol Biotech 2:1–9Google Scholar
  6. Degnan BM, Morse DE (1995) Developmental and morphogenetic gene regulation in Haliotis rufescens larvae at metamorphosis. Amer Zool (in press)Google Scholar
  7. Fretter V, Graham A (1962) British Prosbranch Molluscs. Their Functional Anatomy and Ecology. Ray Society, LondonGoogle Scholar
  8. Groppe JC, Morse DE (1993) Molluscan chymotrypsin-like chymotrypsin: structure, localization, and substrate specificity. Arch Biochem Biophys 305:159–169Google Scholar
  9. Groppe JC, Morse DE (1995) Sequence-independent detection of gene family homologs: Identification of a transcript encoding a molluscan serine protease homologous to the pancreatic enzymes of vertebrates. Comp Biochem Physiol 110:75–82Google Scholar
  10. Harkey MA, Whiteley HR, Whiteley AH (1992) Differential expression of the msp130 gene among skeletal lineage cells in the sea urchin embryo: a three dimensional in situ hybridization analysis. Mech Dev 37:173–184Google Scholar
  11. Moor B (1983) Organogenesis. In: Verdonk NH, van den Biggelar, JAM, Tompa, AS (eds) The mollusca, vol 3. Academic Press, New York, pp 123–178Google Scholar
  12. Morse DE (1990) Recent progress in larval settlement and metamorphosis: closing the gap between molecular biology and ecology. Bull Mar Sci 46:465–483Google Scholar
  13. Morse DE (1992) Molecular mechanisms controlling metamorphosis and recruitment in abalone larvae. In: Shepherd SA, Tegner MJ, Guzman del Proo s (SA) Abalone of the World: ecology, fisheries and culture. Blackwell, Oxford, pp 107–119Google Scholar
  14. Morse DE, Duncan H, Hooker N, Morse A (1977) Hydrogen peroxide induces spawning in molluscs, with activation of prostaglandin endoperoxide synthetase. Science 196:298–300Google Scholar
  15. Morse DE, Hooker N, Duncan H, Jensen L (1979) γ-aminobutryric acid, a neurotransmitter, induces planktonic abalone larvae to settle and begin metamorphosis. Science 204:407–410Google Scholar
  16. Morse DE, Duncan H, Hooker N, Baloun A, Young G (1980) GABA induces behavioral and developmental metamorphosis in planktonic molluscan larvae. Fed Proc 39:3237–3241Google Scholar
  17. Pipe RK (1990) Hydrolytic enzymes associated with the granular haemocytes of the marine mussel, Mytilus edulis. Histochem J 22:595–603Google Scholar
  18. Raven CP (1966) Morphogenesis: the analysis of molluscan development. Pergamon Press, New YorkGoogle Scholar
  19. Salvesen G, Farley D, Shuman J, Przybyla A, Reilly C, Travis J (1987) Molecular cloning of human cathepsin G: Structural similarity to mast cell and cytotoxic T lymphocyte proteases. Biochemistry 26:2289–2293Google Scholar
  20. Spaulding DC, Morse DE (1991) Purification and characterization of sulfatases from Haliotis rufescens: evidence for changes in synthesis and heterogeneity during development. J Comp Physiol B 161:498–515Google Scholar
  21. Tautz D, Pfeifle C (1989) A non-radioactive in situ hybridization method for the localization of specific RNAs in Drosophila embryos reveals translational control of the segmentation gene hunchback. Chromosoma 98:81–85Google Scholar
  22. Trapido-Rosenthal HG, Morse DE (1986) Availability of chemosensory receptors is down regulated by habituation of larvae to a morphometric signal. Proc Natl Acad Sci USA 83:7658–7662Google Scholar
  23. Weissman IL (1994) Developmental switches in the immune system. Cell 76:207–218Google Scholar

Copyright information

© Springer-Verlag 1995

Authors and Affiliations

  • Bernard M. Degnan
    • 1
  • Jay C. Groppe
    • 1
  • Daniel E. Morse
    • 1
  1. 1.Marine Biotechnology Center and Department of MolecularCellular and Developmental Biology University of CaliforniaSanta BarbaraUSA
  2. 2.Department of ZoologyUniversity of QueenslandBrisbaneAustralia
  3. 3.Department of Cell BiologyBiozentrumBaselSwitzerland

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