Development Genes and Evolution

, Volume 218, Issue 5, pp 237–251

Expression patterns of engrailed and dpp in the gastropod Lymnaea stagnalis

  • Minoru Iijima
  • Takeshi Takeuchi
  • Isao Sarashina
  • Kazuyoshi Endo
Original Article

Abstract

We isolated the full-length cDNAs of engrailed and dpp-BMP2/4 orthologues from the pond snail Lymnaea stagnalis and examined their expression patterns during development by the whole mount in situ hybridization. At the gastrula and trochophore stages, engrailed is expressed in the peripheral ectoderm of the presumptive and invaginating shell gland, corroborating its role in the shell formation that is widely conserved among molluscs. At the same stages, dpp-BMP2/4 is expressed in the right-hand side ectoderm of the shell gland and in the invaginating stomodaeum. Unlike in the gastropod Patella vulgata, our results suggested that dpp-BMP2/4 has a role in the shell formation, rather than in the regional specification and that it could be involved in the specification pathway of the left–right asymmetry of the developing shell in L. stagnalis.

Keywords

Gastropod mollusk Lymnaea stagnalis Shell formation Engrailed dpp-BMP2/4 

References

  1. Adachi J, Hasegawa M (1992) Molphy: programs for molecular phylogenetics, I.—ProtML: maximum likelihood inference of protein phylogeny (Computer Science Monographs, 27). Institute of Statistical Mathematics, TokyoGoogle Scholar
  2. Adachi J, Hasegawa M (1996) Molphy version 2.3: programs for molecular phylogenetics based on maximum likelihood. Institute of Statistical Mathematics, TokyoGoogle Scholar
  3. Aguinaldo AMA, Turbeville JM, Linford LS, Rivera MC, Garey JR, Raff RA, Lake JA (1997) Evidence for a clade of nematodes, arthropods and other moulting animals. Nature 387:489–493PubMedCrossRefGoogle Scholar
  4. Altschul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25:3389–3402PubMedCrossRefGoogle Scholar
  5. Arnolds WJA, van den Biggelaar JAM, Verdonk NH (1983) Spatial aspects of cell interactions involved in the determination of dorsoventral polarity in equally cleaving gastropods and regulative abilities of their embryos, as studied by micromere deletions in Lymnaea and Patella. Roux’s Arch Dev Biol 192:75–85Google Scholar
  6. Baratte S, Andouche A, Bonnaud L (2007) Engrailed in cephalopods: a key gene related to the emergence of morphological novelties. Dev Genes Evol 217:353–362PubMedCrossRefGoogle Scholar
  7. Brusca RC, Brusca GJ (2002) Phylum Mollusca. In: Invertebrates, 2nd edn. Sinauer Associates, Sunderland, pp 701–769Google Scholar
  8. Cheers MS, Ettensohn CA (2005) P16 is an essential regulator of skeletogenesis in the sea urchin embryo. Dev Biol 283:384–396PubMedCrossRefGoogle Scholar
  9. Croll RP (2000) Insights into early molluscan neuronal development through studies of transmitter phenotypes in embryonic pond snails. Microsc Res Tech 49:570–578PubMedCrossRefGoogle Scholar
  10. Dictus WJ, Damen P (1997) Cell-lineage and clonal-contribution map of the trochophore larva of Patella vulgata (mollusca). Mech Dev 62:213–226PubMedCrossRefGoogle Scholar
  11. Ekker M, Wegner J, Akimenko MA, Westerfield M (1992) Coordinate embryonic expression of three zebrafish engrailed genes. Development 116:1001–1010PubMedGoogle Scholar
  12. Emanuelsson O, Brunak S, von Heijne G, Nielsen H (2007) Locating proteins in the cell using TargetP, SignalP and related tools. Nat Protoc 2:953–971PubMedCrossRefGoogle Scholar
  13. Endo K, Sarashina I, Asami T (2004) Lymnaea stagnalis as a model organism for studies of calcium carbonate biomineralization. In: Kobayashi I (ed) Biomineralization: formation, diversity, evolution and application. Tokai University Press, Hadano, Japan, pp 172–175Google Scholar
  14. Freeman G, Lundelius JW (1982) The developmental genetics of dextrality and sinistrality in the gastropod Lymnaea peregra. Wilhelm Roux’s Arch 191:69–83CrossRefGoogle Scholar
  15. Freeman G, Lundelius JW (1992) Evolutionary implications of the mode of D quadrant specification in coelomates with spiral cleavage. J Evol Biol 5:205–247CrossRefGoogle Scholar
  16. Harada Y, Hosoiri Y, Kuroda R (2004) Isolation and evaluation of dextral-specific and dextral-enriched cDNA clones as candidates for the handedness-determining gene in a freshwater gastropod, Lymnaea stagnalis. Dev Genes Evol 214:159–169PubMedCrossRefGoogle Scholar
  17. Halanych KM, Bacheller JD, Aguinaldo AM, Liva SM, Hills DM, Lake JA (1995) Evidence from 18S ribosomal DNA that the lophophorates are protostome. Science 267:1641–1643PubMedCrossRefGoogle Scholar
  18. Hinman VF, O’Brien EK, Richards GS, Degnan BM (2003) Expression of anterior Hox genes during larval development of the gastropod Haliotis asinina. Evol Dev 5:508–521PubMedCrossRefGoogle Scholar
  19. Hogan BL (1996) Bone morphogenetic proteins: multifunctional regulators of vertebrate development. Genes Dev 10:1580–1594PubMedCrossRefGoogle Scholar
  20. Hosoiri Y, Harada Y, Kuroda R (2003) Construction of a backcross progeny collection of dextral and sinistral individuals of a freshwater gastropod, Lymnaea stagnalis. Dev Genes Evol 213:193–198PubMedGoogle Scholar
  21. Hui CC, Matsuno K, Ueno K, Suzuki Y (1992) Molecular characterization and silk gland expression of Bombyx engrailed and invected genes. Proc Natl Acad Sci U S A 89:167–171PubMedCrossRefGoogle Scholar
  22. Iijima M, Akiba N, Sarashina I, Kuratani S, Endo K (2006) Evolution of Hox genes in molluscs: a comparison among seven morphologically diverse classes. J Molluscan Stud 72:259–266CrossRefGoogle Scholar
  23. Jacobs DK, Wray CG, Wedeen CJ, Kostriken R, DeSalle R, Staton JL, Gates RD, Lindberg DR (2000) Molluscan engrailed expression, serial organization, and shell evolution. Evol Dev 2:340–347PubMedCrossRefGoogle Scholar
  24. Jones DT, Taylor WR, Thornton JM (1992) The rapid generation of mutation data matrices from protein sequences. Comput Appl Biosci 8:275–282PubMedGoogle Scholar
  25. Kniprath E (1981) Ontogeny of the Molluscan shell field: a review. Zool Scr 10:61–79CrossRefGoogle Scholar
  26. Komori T, Yagi H, Nomura S, Yamaguchi A, Sasaki K, Deguchi K, Shimizu Y, Bronson RT, Gao YH, Inada M, Sato M, Okamoto R, Kitamura Y, Yoshiki S, Kishimoto T (1997) Targeted disruption of Cbfa1 results in a complete lack of bone formation owing to maturational arrest of osteoblasts. Cell 89:755–764PubMedCrossRefGoogle Scholar
  27. Lelong C, Mathieu M, Favrel P (2000) Structure and expression of mGDF, a new member of the transforming growth factor-b superfamily in the bivalve mollusc Crassostrea gigas. Eur J Biochem 267:3986–3993PubMedCrossRefGoogle Scholar
  28. Logan C, Hanks MC, Noble-Topham S, Nallainathan D, Provart NJ, Joyner AL (1992) Cloning and sequence comparison of the mouse, human, and chicken engrailed genes reveal potential functional domains and regulatory regions. Dev Genet 13:345–358PubMedCrossRefGoogle Scholar
  29. Lydeard C, Lindberg DR (2003) Challenges and research opportunities in molluscan molecular phylogenetics. In: Lydeard C, Lindberg DR (eds) Molecular systematics and phylogeography of mollusks. Smithsonian Books, Washington London, pp 1–13Google Scholar
  30. Manzanares M, Marco R, Garesse R (1993) Genomic organization and developmental pattern of expression of the engrailed gene from the brine shrimp Artemia. Development 118:1209–1219PubMedGoogle Scholar
  31. Marin F, Luquet G (2004) Molluscan shell proteins. Comptes Rendus Palevol 3:469–492CrossRefGoogle Scholar
  32. Meshcheryakov VN (1990) The common pond snail Lymanaea stagnalis. In: Dettlaff TA, Vassetzky SG (eds) Animal species for developmental studies. Consultants Bureau, New York, pp 69–132Google Scholar
  33. Monsoro-Burq A, Le Douarin N (2000) Left–right asymmetry in BMP4 signalling pathway during chick gastrulation. Mech Dev 97:105–108PubMedCrossRefGoogle Scholar
  34. Morill JB (1982) Development of the pulmonate gastropod, “Lymnaea”. In: Harrison FW, Cowden RR (eds) Developmental biology of fresh water invertebrates. Alan R. Liss Inc., New York, pp 399–483Google Scholar
  35. Moshel SM, Levine M, Collier JR (1998) Shell differentiation and engrailed expression in the Ilyanassa embryo. Dev Genes Evol 208:135–141PubMedCrossRefGoogle Scholar
  36. Nederbragt AJ, van Loon AE, Dictus W (2002) Expression of Patella vulgata orthologs of engrailed and dpp-BMP2/4 in adjacent domains during molluscan shell development suggests a conserved compartment boundary mechanism. Dev Biol 246:341–355PubMedCrossRefGoogle Scholar
  37. Patel NH, Martin-Blanco E, Coleman KG, Poole SJ, Ellis MC, Kornberg TB, Goodman CS (1989) Expression of engrailed proteins in arthropods, annelids and chordates. Cell 58:955–968PubMedCrossRefGoogle Scholar
  38. Runnegar B (1996) Early evolution of the Mollusca: the fossil record. In: Taylor J (ed) Origin and evolutionary radiation of the Mollusca. Oxford University Press, London, pp 77–87Google Scholar
  39. Runnegar B, Pojeta J (1985) Origin and diversification of the Mollusca. In: Treuman ER, Clarke MR (eds) The Mollusca, vol 10. Academic Press, London, pp 1–57Google Scholar
  40. Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425PubMedGoogle Scholar
  41. Salvini-Plawen L, Steiner G (1996) Synapomorphies and plesiomorphies in higher classification of mollusc. In: Taylor J (ed) Origin and evolutionary radiation of the Mollusca. The Malacological Society of London, London, pp 29–51Google Scholar
  42. Sarashina I, Endo K (2006) Skeletal matrix proteins of invertebrate animals: comparative analysis of their amino acid sequences. Paleontol Res 10:311–336CrossRefGoogle Scholar
  43. Sarashina I, Yamaguchi H, Haga T, Iijima M, Chiba S, Endo K (2006) Molecular evolution and functionally important structures of molluscan Dermatopontin: implications for the origins of molluscan shell matrix proteins. J Mol Evol 62:307–318PubMedCrossRefGoogle Scholar
  44. Shibazaki Y, Shimizu M, Kuroda R (2004) Body handedness is directed by genetically determined cytoskeletal dynamics in the early embryo. Curr Biol 14:1462–1467PubMedCrossRefGoogle Scholar
  45. Shigeno S, Sasaki T, Moritaki T, Kasugai T, Vecchione M, Agata K (2008) Evolution of the cephalopod head complex by assembly of multiple molluscan body parts: evidence from Nautilus embryonic development. J Morphol 269:1–17PubMedCrossRefGoogle Scholar
  46. Ueshima R, Asami T (2003) Evolution: single-gene speciation by left–right reversal. Nature 425:679 16PubMedCrossRefGoogle Scholar
  47. Voronezhskaya EE, Elekes K (2003) Expression of FMRFamide gene encoded peptides by identified neurons in embryos and juveniles of the pulmonate snail Lymnaea stagnalis. Cell Tissue Res 314:297–313PubMedCrossRefGoogle Scholar
  48. Wanninger A, Haszprunar G (2001) The expression of an engrailed protein during embryonic shell formation in the tuskshell Antalis entalis (Mollusca, Scaphopoda). Evol Dev 3:312–321PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2008

Authors and Affiliations

  • Minoru Iijima
    • 1
  • Takeshi Takeuchi
    • 1
  • Isao Sarashina
    • 1
  • Kazuyoshi Endo
    • 1
  1. 1.Department of Earth Evolution Sciences, Graduate School of Life and Environmental SciencesUniversity of TsukubaTsukubaJapan

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