Development Genes and Evolution

, Volume 214, Issue 5, pp 220–239 | Cite as

The embryonic development of the flatworm Macrostomum sp.

  • Joshua Morris
  • Ramachandra Nallur
  • Peter Ladurner
  • Bernhard Egger
  • Reinhard Rieger
  • Volker Hartenstein
Original Article

Abstract

Macrostomid flatworms represent a group of basal bilaterians with primitive developmental and morphological characteristics. The species Macrostomum sp., raised under laboratory conditions, has a short generation time of about 2–3 weeks and produces a large number of eggs year round. Using live observation, histology, electron microscopy and immunohistochemistry we have carried out a developmental analysis of Macrostomum sp. Cleavage (stages 1–2) of this species follows a modified spiral pattern and results in a solid embryonic primordium surrounded by an external yolk layer. During stage 3, cells at the anterior and lateral periphery of the embryo evolve into the somatic primordium which gives rise to the body wall and nervous system. Cells in the center form the large yolk-rich gut primordium. During stage 4, the brain primordium and the pharynx primordium appear as symmetric densities anterior-ventrally within the somatic primordium. Organ differentiation commences during stage 5 when the neurons of the brain primordium extend axons that form a central neuropile, and the outer cell layer of the somatic primordium turns into a ciliated epidermal epithelium. Cilia also appear in the lumen of the pharynx primordium, in the protonephridial system and, slightly later, in the lumen of the gut. Ultrastructurally, these differentiating cells show the hallmarks of platyhelminth epithelia, with a pronounced apical assembly of microfilaments (terminal web) inserting at the zonula adherens, and a wide band of septate junctions underneath the zonula. Terminal web and zonula adherens are particularly well observed in the epidermis. During stage 6, the somatic primordium extends around the surface dorsally and ventrally to form a complete body wall. Muscle precursors extend myofilaments that are organized into a highly regular orthogonal network of circular, diagonal and longitudinal fibers. Neurons of the brain primordium differentiate a commissural neuropile that extends a single pair of ventro-lateral nerve trunks (the main longitudinal cords) posteriorly. The primordial pharynx lumen fuses with the ventral epidermis anteriorly and the gut posteriorly, thereby generating a continuous digestive tract. The embryo adopts its final shape during stages 7 and 8, characterized by the morphallactic lengthening of the body into a U-shaped form and the condensation of the nervous system.

Keywords

Platyhelminth Embryo Morphogenesis Organogenesis Differentiation 

References

  1. Ashburner M (1989) Drosophila. A laboratory manual. Cold Spring Harbor Press, Cold Spring Harbor, N.Y.Google Scholar
  2. Ax P (1961) Verwandtschaftsbeziehungen und Phylogenie der Turbellarien. Ergebn Biol 24:1–68Google Scholar
  3. Ax P (1996) Multicellular animals. A new approach to the phylogenetic order in nature. Springer, Berlin Heidelberg New YorkGoogle Scholar
  4. Ax P, Borkott H (1968a) Organisation und Fortpflanzung von Macrostomum romanicum (Turbellaria, Macrostomida). Verh Dtsch Zool Ges Innsbruck 30b:344–347Google Scholar
  5. Ax P, Borkott H (1968b) Organisation und Fortpflanzung von Macrostomum salinum (Turbellaria-Macrostomida). Inst Wiss Film C 947:1–11Google Scholar
  6. Baguñà J, Boyer BC (1990) Descriptive and experimental embryology of the Turbellaria: present knowledge, open questions and future trends. In: Marthy HJ (ed) Experimental embryology in aquatic plants and animals. Plenum Press, New York, pp 95–128Google Scholar
  7. Baguñà J, Carranza S, Paps J, Ruiz-Trillo I, Riutort M (2001) Molecular taxonomy and phylogeny of the Tricladida. In: Littlewood D, Bray RA (eds) Interrelationships of the platyhelminthes. Taylor & Francis, London, pp 49–56Google Scholar
  8. Bennazzi M, Gremigni V (1982) Developmental biology of triclad turbellarians (Planaria). In: Harrison FW, Cowden RR (eds) Developmental biology of freshwater invertebrates. Liss, New York, pp 151–211Google Scholar
  9. Bogomolow SI (1949) Zur Frage nach dem Typus der Furchung bei den Rhabdocoela. Wiss Schr Leningrader Staatl Univ Ser Biol 20:128–142Google Scholar
  10. Bogomolow SI (1960) Über die Furchung von Macrostomum rossicum Beklemichev und deren Beziehung zur Furchung der Turbellaria Coelata und Acoela. Vt Sov Can Embriol SSSR 1960:23–24Google Scholar
  11. Boyer BC, Henry JQ, Martindale MQ (1996) Dual origins of mesoderm in a basal spiralian: cell lineage analyses in the polyclad turbellarian Notoplana inquilina. Dev Biol 179:328–338CrossRefGoogle Scholar
  12. Boyer BC, Henry JJ, Martindale MQ (1998) The cell lineage of a polyclad turbellarian embryo reveals close similarity to coelomate spiralians. Dev Biol 204:111–123CrossRefPubMedGoogle Scholar
  13. Bresslau E (1904) Beitraege zur Entwicklungsgeschichte der Turbellarien. I. Die Entwicklung der Rhabdocoelen und Alloiocoelen. Z Wiss Zool 76:213–332Google Scholar
  14. Cebria F, Kobayashi C, Umesono Y, Nakazawa M, Mineta K, Ikeo K, Gojobori T, Itoh M, Taira M, Sanchez Alvarado A, Agata K (2002) FGFR-related gene nou-darake restricts brain tissues to the head region of planarians. Nature 419:620–624CrossRefPubMedGoogle Scholar
  15. Costello DP, Henley C (1976) Spiralian development: a perspective. Am Zool 16:277–291Google Scholar
  16. Curini-Galletti M (2001) The Proseriata. In: Littlewood D, Bray RA (eds) Interrelationships of the platyhelminthes. Taylor & Francis, London, pp 41–48Google Scholar
  17. Doe DA (1981) Comparative ultrastructure of the pharynx simplex in Turbellaria. Zoomorphology 97:133–192Google Scholar
  18. Ehlers U (1985) Das phylogenetische System der Platyhelminthes. Fischer, JenaGoogle Scholar
  19. Eisenman EA, Alfert M (1982) A new fixation procedure for preserving the ultrastructure of marine invertebrate tissues. J Microsc 125:117–120Google Scholar
  20. Gehlen M, Lochs A (1990) Quantification of characters from live observations in meiobenthic Turbellaria-Macrostomida. Cah Biol Mar 31:463–472Google Scholar
  21. Giesa S (1966) Die Embryonalentwicklung von Monocelis fusca Oersted (Turbellaria, Proseriata). Z Morphol Oekol Tiere 57:137–230Google Scholar
  22. Guillard R, Ryther LH (1962) Studies on marine planktonic diatoms. I. Cyclotella nana Hustedt and Detonula confervacea (Cleve). Gran Can J Microbiol 8:229–239Google Scholar
  23. Hartenstein V, Ehlers U (2000) The embryonic development of the rhabdocoel flatworm Mesostoma lingua. Dev Genes Evol 210:399–415PubMedGoogle Scholar
  24. Hartenstein V, Jones M (2003) The embryonic development of the bodywall and nervous system of the cestode flatworm Hymenolepis diminuta. Cell Tissue Res 311:427–435PubMedGoogle Scholar
  25. Henry JQ, Martindale MQ (1998) Conservation of the spiralian developmental program: cell lineage of the nemertean, Cerebratulus lacteus. Dev Biol 201:253–269PubMedGoogle Scholar
  26. Henry JQ, Martindale MQ, Boyer BC (2000) The unique developmental program of the acoel flatworm, Neochildia fusca. Dev Biol 220:285–295CrossRefPubMedGoogle Scholar
  27. Hooge MD (2001) Evolution of body-wall musculature in the Platyhelminthes (Acoelomorpha, Catenulida, Rhabditophora). J Morphol 249:171–194CrossRefPubMedGoogle Scholar
  28. Jondelius U, Norén M, Hendelberg J (2001) The Prolecithophora. In: Littlewood D, Bray RA (eds) Interrelationships of the platyhelminthes. Taylor & Francis, London, pp 74–80Google Scholar
  29. Jondelius U, Ruiz-Trillo I, Baguñà J, Riutort M (2002) The nemertodermatid flatworms are basal bilaterians and not members of the Platyhelminthes. Zool Scripta 31:201–215CrossRefGoogle Scholar
  30. Ladurner P, Rieger R (2000) Embryonic muscle development of Convoluta pulchra (Turbellaria-Acoelomorpha, Platyhelminthes). Dev Biol 222:359–375CrossRefPubMedGoogle Scholar
  31. Ladurner P, Rieger R, Baguñà J (2000) Spatial distribution and differentiation potential of stem cells in hatchlings and adults in the marine platyhelminth Macrostomum sp.: a bromodeoxyridine analysis. Dev Biol 226:231–241CrossRefPubMedGoogle Scholar
  32. Ladurner P, Schärer L, Salvenmoser W, Rieger R (2004) A new species of the genus Macrostomum (Rhabditophora, Macrostomorpha) from the northern Adriatic: a new model system for the lower Bilateria. Zool Scripta (in press)Google Scholar
  33. Littlewood DT, Olson PD (2001) Small subunit rDNA and the Platyhelminthes: signal, noise, conflict and compromise. In: Littlewood DT, Bray RA (eds)Interrelationships of the platyhelminthes. Taylor & Francis, London, pp 262–278Google Scholar
  34. Littlewood DT, Olson PD, Telford MJ, Herniou EA, Riutort M (2001) Elongation factor 1-alpha sequences alone do not assist in revolving the position of the acoela within the Metazoa. Mol Biol Evol 18:437–442PubMedGoogle Scholar
  35. Luther A (1960) Die Turbellarien Ostfennoskandiens. I. Acoela, Catenulida, Macrostomida, Lecithoepitheliata, Prolecithophora und Proseriata. Fauna Fenn 7:1–155 Google Scholar
  36. Ogawa K, Ishihara S, Saito Y, Mineta K, Nakazawa M, Ikeo K, Gojobori T, Watanabe K, Agata K (2002) Induction of a noggin-like gene by ectopic DV interaction during planarian regeneration. Dev Biol 250:59–70CrossRefPubMedGoogle Scholar
  37. Papi F (1953) Beitraege zur Kenntnis der Macrostomiden (Turbellarien). Acta Zool Fenn 78:1–32Google Scholar
  38. Peter R, Ladurner P, Rieger R (2001) The role of stem cell strategies in coping with environmental stress and choosing between alternative reproductive modes: Turbellaria rely on a single cell type to maintain individual life and propagate species. Mar Ecol 22:35–45CrossRefGoogle Scholar
  39. Peter R, Gschwentner R, Schürmann W, Rieger R, Ladurner P (2004) The significance of stem cells in free-living flatworms: one common source for all cells in the adult. J Appl Biomed 2:21–35Google Scholar
  40. Pineda D, Gonzalez J, Callaerts P, Ikeo K, Gehring WJ, Salo E (2000) Searching for the prototypic eye genetic network: sine oculis is essential for eye regeneration in planarians. Proc Natl Acad Sci USA 97:4525–4529CrossRefPubMedGoogle Scholar
  41. Pineda D, Rossi L, Batistoni R, Salvetti A, Marsal M, Gremigni V, Falleni A, Gonzalez-Linares J, Deri P, Salo E (2002) The genetic network of prototypic planarian eye regeneration is Pax6 independent. Development 129:1423–1434PubMedGoogle Scholar
  42. Ramachandra NB, Gates R, Ladurner P, Jacobs D, Hartenstein V (2002) Neurogenesis in the primitive bilaterian Neochildia. I. Normal development and isolation of genes controlling neural fate. Dev Genes Evol 212:55–69CrossRefPubMedGoogle Scholar
  43. Reisinger E (1923) Turbellaria. In: Schulze (ed) Biologie der Tiere Deutschlands. pp 1–64Google Scholar
  44. Reisinger E, Cichocki I, Erlach R, Szyskowitz T (1974a) Ontogenetische Studien an Turbellarien: ein Beitrag zur Evolution der Dotterverarbeitung im ektolezithalen Ei, 1. Teil 1. Z Zool Syst Evolutionsforsch 12:161–195Google Scholar
  45. Reisinger E, Cichocki I, Erlach R, Szyskowitz T (1974b) Ontogenetische Studien an Turbellarien: ein Beitrag zur Evolution der Dotterverarbeitung im ektolezithalen Ei, 2. Teil 1. Z Zool Syst Evolutionsforsch 12:241–278Google Scholar
  46. Reiter D, Boyer B, Ladurner P, Mair G, Salvenmoser W, Rieger R (1996) Differentiation of the bodywall musculature in Macrostomum hystricinum marinum and Hoploplana inquilina (Platyhelminthes), as models for muscle development in lower Spiralia. Roux’s Arch Dev Biol 205:410–423Google Scholar
  47. Reuter M, Halton DW (2001) Comparative neurobiology of Platyhelminthes. In: Littlewood D, Bray RA (eds) Interrelationships of the platyhelminthes. Taylor & Francis, London, pp 231–238Google Scholar
  48. Rieger RM (1977) The relationship of character variability and morphological complexity in copulatory structures of Turbellaria-Macrostomida and -Haplopharyngida. Mikrofauna Meeresbd 61:197–216Google Scholar
  49. Rieger RM (1998) 100 Years of research on Turbellaria. Hydrobiologia 383:1–27CrossRefGoogle Scholar
  50. Rieger RM (2001) Phylogenetic systematics of the Macrostomorpha. In: Littlewood D, Bray RA (eds) Interrelationships of the platyhelminthes. Taylor & Francis, London, pp 28–38Google Scholar
  51. Rieger RM, Tyler S, Smith JPS III, Rieger GE (1991) Platyhelminthes: Turbellaria. In: Harrison FW, Bogitsh BJ (eds) Microscopic anatomy of invertebrates, vol 3. Wiley-Liss, New YorkGoogle Scholar
  52. Rieger RM, Salvenmoser W, Legniti A, Tyler S (1994) Phalloidin-rhodamine preparations of Macrostomum hystricinum marinum (Platyhelminthes); morphology and postembryonic development of the musculature. Zoomorphology 114:133–147Google Scholar
  53. Rohde K (2001) Protonephridia as phylogenetic characters. In: Littlewood D, Bray RA (eds) Interrelationships of the Platyhelminthes. Taylor & Francis, London, pp 203–216Google Scholar
  54. Salo E, Pineda D, Marsal M, Gonzalez J, Gremigni V, Batistoni R (2002) Genetic network of the eye in Platyhelminthes: expression and functional analysis of some players during planarian regeneration. Gene 287:67–74CrossRefPubMedGoogle Scholar
  55. Sanchez-Alvarado A, Newmark PA (1999) Double-stranded RNA specifically disrupts gene expression during planarian regeneration. Proc Natl Acad Sci USA 96:5049–5054CrossRefPubMedGoogle Scholar
  56. Sanchez-Alvarado A, Newmark PA, Robb SM, Juste R (2002) The Schmidtea mediterranea database as a molecular resource for studying platyhelminthes, stem cells and regeneration. Development 129:5659–5665CrossRefPubMedGoogle Scholar
  57. Seilern-Aspang F (1957) Die Entwicklung von Macrostomum appendiculatum (Fabricius). Zool Jahrb Anat 76:311–330Google Scholar
  58. Surface FM (1908) The early development of a polyclad, Planocera inquilina Wh. Proc Acad Nat Sci Philadelphia 59:514–559Google Scholar
  59. Thomas MB (1986) Embryology of the Turbellaria and its phylogenetic significance. Hydrobiologia 132:105–115Google Scholar
  60. Tyler S (1981) Development of cilia in embryos of the turbellarian Macrostomum. Hydrobiologia 84:231–239Google Scholar
  61. Tyler S (1984) Turbellarian platyhelminths. In: Bereiter-Hahn J, Matoltsy AG, Richards KS (eds) Biology of the integument. Springer, Berlin Heidelberg New York, pp 112–113Google Scholar
  62. Tyler S (1988) The role of function in determination of homology and convergence—examples from invertebrate adhesive organs. Fortschr Zool 36:331–347Google Scholar
  63. Tyler S (2001) The early worm—origins and relationships of the lower flatworms. In: Littlewood D, Bray RA (eds) Interrelationships of the platyhelminthes. Taylor & Francis, London, pp 3–12Google Scholar
  64. Verdonk NH, van den Biggelaar JAM (1983) Early development and the formation of the germ layers. In: Verdonk NH, van den Biggelaar J, Tompa AS (eds) The Mollusca. Academic, New York, pp 91–122Google Scholar
  65. Xylander W (2004) Neodermata. In: Westheide W, Rieger R (eds) Spezielle Zoologie. Spektrum Akademischer Verlag, Heidelberg, pp 230–258Google Scholar
  66. Younossi-Hartenstein A, Hartenstein V (2000a) Comparative approach to developmental analysis: the case of the dalyellid flatworm, Gieysztoria superba. Int J Dev Biol 44:499–506PubMedGoogle Scholar
  67. Younossi-Hartenstein A, Hartenstein V (2000b) The embryonic development of the polyclad flatworm Imgogine mcgrathi. Dev Genes Evol 210:383–398PubMedGoogle Scholar
  68. Younossi-Hartenstein A, Hartenstein V (2001) The embryonic development of the temnocephalid flatworms Craspedella pedum and Diceratocephala sp. Cell Tissue Res 304:295–310PubMedGoogle Scholar
  69. Younossi-Hartenstein A, Ehlers U, Hartenstein V (2000) Embryonic development of the nervous system of the rhabdocoel flatworm Mesostoma lingua (Abildgaard, 1789). J Comp Neurol 416:461–476CrossRefPubMedGoogle Scholar
  70. Zalokar M, Erk I (1977) Phase-partition fixation and staining of Drosophila eggs. Stain Technol 52:89–95PubMedGoogle Scholar

Copyright information

© Springer-Verlag 2004

Authors and Affiliations

  • Joshua Morris
    • 1
  • Ramachandra Nallur
    • 1
  • Peter Ladurner
    • 2
  • Bernhard Egger
    • 2
  • Reinhard Rieger
    • 2
  • Volker Hartenstein
    • 1
  1. 1.Department of Molecular, Cell and Developmental BiologyUniversity of CaliforniaLos AngelesUSA
  2. 2.Institute of Zoology and LimnologyUniversity of InnsbruckInnsbruckAustria

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