Advertisement

Development Genes and Evolution

, Volume 215, Issue 3, pp 109–131 | Cite as

The embryonic development of the triclad Schmidtea polychroa

  • Albert Cardona
  • Volker Hartenstein
  • Rafael Romero
Original Article

Abstract

Triclad flatworms are well studied for their regenerative properties, yet little is known about their embryonic development. We here describe the embryonic development of the triclad Schmidtea polychroa, using histological and immunocytochemical analysis of whole-mount preparations and sections. During early cleavage (stage 1), yolk cells fuse and enclose the zygote into a syncytium. The zygote divides into blastomeres that dissociate and migrate into the syncytium. During stage 2, a subset of blastomeres differentiate into a transient embryonic epidermis that surrounds the yolk syncytium, and an embryonic pharynx. Other blastomeres divide as a scattered population of cells in the syncytium. During stage 3, the embryonic pharynx imbibes external yolk cells and a gastric cavity is formed in the center of the syncytium. The syncytial yolk and the blastomeres contained within it are compressed into a thin peripheral rind. From a location close to the embryonic pharynx, which defines the posterior pole, bilaterally symmetric ventral nerve cord pioneers extend forward. Stage 4 is characterized by massive proliferation of embryonic cells. Large yolk-filled cells lining the syncytium form the gastrodermis. During stage 5 the external syncytial yolk mantle is resorbed and the embryonic cells contained within differentiate into an irregular scaffold of muscle and nerve cells. Epidermal cells differentiate and replace the transient embryonic epidermis. Through stages 6–8, the embryo adopts its worm-like shape, and loosely scattered populations of differentiating cells consolidate into structurally defined organs. Our analysis reveals a picture of S. polychroa embryogenesis that resembles the morphogenetic events underlying regeneration.

Keywords

Flatworm Embryology Ectolecithal Morphogenesis Organogenesis 

Notes

Acknowledgements

We thank B. Sjöstrand from the UCLA CHS electron microscopy services and N. Cortadellas, A. García and A. Rivera from UB Serveis Científico-Tècnics (Microscopia Electrònica) for technical assistance in preparing and analyzing TEM samples, and the anonymous reviewers whose constructive comments greatly improved this manuscript. A.C. thanks the Hartenstein lab and the Banerjee lab at UCLA for their kind assistance in every respect, and also the Romero lab at UB for their humor, technical expertise and patience. A.C. is recipient of a FPU grant from the Ministerio de Educación, Ciencia y Deportes, Spain. This research was supported by a grant from BMC2000-0546 (to R.R.) and NSF Grant IBN-0110715 (to V.H.).

References

  1. Abeloos M (1930) Recherches expérimentales sur la croissance et la régénération chez les planaires. Bull Biol Fr Belg 64(1)Google Scholar
  2. Agata K, Watanabe K (1999) Molecular and cellular aspects of planarian regeneration. Semin Cell Dev Biol 10:377–383PubMedGoogle Scholar
  3. Ax P (1995) Multicellular animals, vol 1. Fischer, StuttgartGoogle Scholar
  4. Baguñà J (1974) A demonstration of a peripheral and a gastrodermal nervous plexus in planarians. Zool Anz 193(3/4):240–244Google Scholar
  5. Baguñà J, Boyer CB (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, New York, pp 95–128Google Scholar
  6. Baguñà J, Saló E, Auladell C (1989) Regeneration and pattern formation in planarians. III. Evidence that neoblasts are totipotent stem cells and the source of blastema cells. Development 107:77–86Google Scholar
  7. Bely A, Wray G (2001) Evolution of regeneration and fission in annelids: insights from engrailed- and orthodenticle-class gene expression. Development 128:2781–2791PubMedGoogle 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. Bresslau E (1904) Beitraege zur Entwicklungsgeschichte der Turbellarien I. Die Entwicklung der Rhabdocoelen und Alloiocoelen. Z Wiss Zool 76:213–332Google Scholar
  10. Bueno D, Fernández-Rodríguez J, Cardona A, Hernández-Hernández V, Romero R (2002) A novel invertebrate trophic factor related to invertebrate neurotrophins is involved in planarian body regional survival and asexual reproduction. Dev Biol 252:188–201PubMedGoogle Scholar
  11. Cebrià F, Vispo M, Newmark P, Bueno D, Romero R (1997) Myocyte differentiation and body wall muscle regeneration in the planarian Girardia tigrina. Dev Genes Evol 207:306–316CrossRefGoogle Scholar
  12. Cebrià F, Bueno D, Reigada S, Romero R (1999) Intercalary muscle cell renewal in planarian pharynx. Dev Genes Evol 209(4):249–253CrossRefPubMedGoogle Scholar
  13. Cebrià F, Kudome T, Nakazawa M, Mineta K, Ikeo K, Gojobori T, Agata K (2002a) The expression of neural-specific genes reveals the structural and molecular complexity of the planarian central nervous system. Mech Dev 116:199–204PubMedGoogle Scholar
  14. Cebrià F, Nakazawa M, Mineta K, Ikeo K, Gojobori T, Agata K (2002b) Dissecting planarian central nervous system regeneration by the expression of neural-specific genes. Dev Growth Differ 44(2):135–146PubMedGoogle Scholar
  15. Cebrià F, Kobayashi C, Umesono Y, Nakazawa M, Mineta K, Ikeo K, Gojobori T, Itoh M, Taira M, Sanchez Alvarado A, Agata K (2002c) FGFR-related gene nou-darake restricts brain tissues to the head region of planarians. Nature 419(6907):620–624Google Scholar
  16. Domenici L, Gremigni V (1974) Electron microscopical and cytochemical study of vitelline cells in the fresh-water triclad Dugesia lugubris sl. II. Origin and distribution of reserve materials. Cell Tissue Res 152:219–228PubMedGoogle Scholar
  17. Ehlers U (1985) Das phylogenetische System der Plathelminthes. Fischer, StuttgartGoogle Scholar
  18. Fulinski B (1916) Die Keimblätterbildung bei Dendrocoelum lacteum Oerst. Zool Anz 47:380–400Google Scholar
  19. Giesa S (1966) Die Embryonalentwicklung von Monocelis fusca Oersted (Turbellaria, Proseriata). Z Morphol Oekol Tiere 57:137–230Google Scholar
  20. González-Estévez C, Saló E (2001) GtDap-1: a molecular marker to follow apoptosis in planarian regeneration (abstract). Int J Dev Biol 45(suppl 1):S180Google Scholar
  21. Gonzalez-Estevez CM, Momose T, Gehring WJ, Salo E (2003) Transgenic planarian lines obtained by electroporation using transposon-derived vectors and an eye-specific GFP marker. Proc Natl Acad Sci USA 100(24):14046–14051PubMedGoogle Scholar
  22. Gremigni V (1988) A comparative ultrastructural study of homocellular and heterocellular female gonads in free living Platyhelminthes-Turbellaria. Fortschr Zool 36:245–261Google Scholar
  23. Gremigni V, Nigro M, Puccinelli I (1982) Evidence of male germ cell redifferentiation into female germ cells in planarian regeneration. J Embryol Exp Morphol 70:29–36PubMedGoogle Scholar
  24. Hartenstein V, Ehlers U (2000) The embryonic development of the rhabdocoel flatworm Mesostoma lingua (Abildgaard, 1789). Dev Genes Evol 210:399–415PubMedGoogle Scholar
  25. Hase S, Kobayashi K, Koyanagi R, Hoshi M, Matsumoto M (2003) Transcriptional pattern of a novel gene, expressed specifically after the point-of-no-return during sexualization, in Planaria. Dev Genes Evol 212(12):585–592PubMedGoogle Scholar
  26. Hooge MD (2001) Evolution of body-wall musculature in Platyhelminthes (Acoelomorpha, Catenulida, Rhabditophora). J Morphol 249:171–194CrossRefPubMedGoogle Scholar
  27. Hyman LH (1951) The invertebrates: Platyhelminthes and Rhynchocoela, vol 2. McGraw-Hill, New YorkGoogle Scholar
  28. Kato K, Orii H, Watanabe K, Agata K (2001) Dorsal and ventral positional cues required for the onset of planarian regeneration may reside in differentiated cells. Dev Biol 233:109–121PubMedGoogle Scholar
  29. Koscielski B (1966) Cytological and cytochemical investigations on the embryonic development of Dendrocoelum lacteum OF Müller. Zool Pol 16(1):83–102Google Scholar
  30. Ladurner P, Rieger R (2002) Embryonic muscle development of Convoluta pulchra (Turbellaria-Acoelomorpha, Platyhelminthes). Dev Biol 222:359–375Google 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 bromodeoxyuridine analysis. Dev Biol 226:231–241CrossRefPubMedGoogle Scholar
  32. Le Moigne A (1963) Etude du développement embryonnaire de Polycelis nigra (Turbellarié, Triclade). Bull Soc Zool Fr 88:403–422Google Scholar
  33. Le Moigne A (1965) Effet des irradiations aux rayons × sur le développement embryonnaire et le pouvoir de régénération à l’éclosion, de Polycelis nigra (Turbellarié, Triclade). CR Acad Sci Paris 260:4627–4629Google Scholar
  34. Le Moigne A (1966) Etude du développement embryonnaire et recherches sur les cellules de régénération chez l’embryon de la Planaire Polycelis nigra (Turbellarié, Triclade). J Embryol Exp Morphol 15:39–60PubMedGoogle Scholar
  35. Le Moigne A (1967a) Demonstration with the electron microscope of the persistence of undifferentiated cells during embryonal development of the planarian, Polycelis nigra. CR Acad Sci 265(3):242–244Google Scholar
  36. Le Moigne A (1967b) Etude au microscope èlectronique de la différenciation des principaux types cellulaires chez l’embryon de la Planaire Polycelis nigra. Bull Soc Zool Fr 92:627–628Google Scholar
  37. Le Moigne A (1968) Etude au microscope électronique de l’évolution des structures embryonnaires de Planaires après irradiation aux rayons x. J Embryol Exp Morphol 19(2):181–192PubMedGoogle Scholar
  38. Mattiesen E (1904) Ein Beitrag zur Embryologie der Süßwasserdendrocoelen. 77:274–361Google Scholar
  39. McKanna JA (1968a) Fine structure of the protonephridial system in planaria I flame cells. Z Zellfirsch 92:509–523Google Scholar
  40. McKanna JA (1968b) Fine structure of the protonephridial system in planaria I ductules, collecting ducts, and osmoregulatory cells. Z Zellfirsch 92:524–535Google Scholar
  41. Metschnikoff E (1883) Die Embryologie von Planaria polychroa. Z Wiss Zool 38:331–354Google Scholar
  42. Morgan TH (1898) Experimental studies of the regeneration of Planaria maculata. Arch Entwicklungsmech Org 7:364–397Google Scholar
  43. Morita M, Best JB (1974) Electron microscopic studies of planarian regeneration. II. Changes in epidermis during regeneration. J Exp Zool 187(3):345–73PubMedGoogle Scholar
  44. Morita M, Best JB, Noel J (1969) Electronic microscopic studies of planarian regeneration. I. Fine structure of neoblasts in Dugesia dorotocepha. J Ultrastr Res 27:7–23Google Scholar
  45. Morris J, Ramachandra N, Ladurner P, Egger B, Rieger R, Hartenstein V (2004) The embryonic development of the flatworm Macrostomum sp. Dev Genes Evol 214:220–239CrossRefPubMedGoogle Scholar
  46. Newmark PA, Sánchez-Alvarado A (2000) Bromodeoxyuridine specifically labels the regenerative stem cells of planarians. Dev Biol 220:142–153CrossRefPubMedGoogle Scholar
  47. Newmark PA, Sánchez-Alvarado A (2002) Not your father planarian: a classic model enters the era of functional genomics. Nature 2002(3):210Google Scholar
  48. Nimeth T, Mahlknecht M, Mezzanato A, Peter R, Rieger R, Ladurner P (2004) Stem cell dynamics during growth, feeding and starvation in the basal flatworm Macrostomum sp (Platyhelminthes). Dev Dyn 230:91–99CrossRefPubMedGoogle Scholar
  49. Ogawa K, Kobayashi C, Hayashi T, Orii F, Watanabe K, Agata K (2002) Planarian fibroblast growth factor receptor homologs expressed in stem cells and cephalic ganglions. Dev Growth Differ 44:191–204PubMedGoogle Scholar
  50. Orii H, Mochii M, Watanabe K (2003) A simple “soaking method” for RNA interference in the planarian Dugesia japonica. Dev Genes Evol 213(3):138–141PubMedGoogle Scholar
  51. 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(9):4525–4529PubMedGoogle Scholar
  52. Plunket JA, Simmons RB, Walthall WW (1996) Dynamic interactions between nerve and muscle in Caenorhabditis elegans. Dev Biol 175:154–165PubMedGoogle Scholar
  53. Rasband WS (1997–2004) ImageJ. National Institutes of Health, Bethesda, Maryland, USA. http://rsb.info.nih.gov/ij/
  54. Reddien PW, Sánchez-Alvarado A (2004) Fundamentals of planarian regeneration. An Rev Cell Dev Biol 20:725–757Google Scholar
  55. Reiter D, Boyer B, Ladurner P (1996) Differentiation of the body wall musculature in Macrostomum hystricinum marinum and Hoploplana inquilina (Platyhelminthes) as models for muscle development in lower Spiralia. Roux’s Arch Dev Biol 205(7–8):410–423Google Scholar
  56. Reuter M, Palmberg I (1989) Development and differentiation of neuronal subsets in asexually reproducing Microstomum lineare. Immunocytochemistry of 5-HT, RF-amide and SCPB. Histochemistry 91(2):123–131PubMedGoogle Scholar
  57. Reuter M, Gustafsson MK, Sahlgren C, Halton DW, Maule AG, Shaw C (1995a) The nervous system of Tricladida. I. Neuroanatomy of Procerodes littoralis (Maricola, Procerodidae): an immunocytochemical study. Invertebr Neurosci 1(2):113–122Google Scholar
  58. Reuter M, Gustafsson MKS, Sheiman I M, Terenina N, Halton DW, Maule AG, Shaw C (1995b) The nervous system of Tricladida. II. Neuroanatomy of Dugesia tigrina (Paludicola, Dugesiidae): an immunocytochemical study. Invertebr Neurosci 1:133–143Google Scholar
  59. Reuter M, Gustafsson MKS, Mäntylä K, Grimmelikhuijzen CJP (1996) The nervous system of Tricladida III. Neuroanatomy of Dendrocoelum lacteum and Polycelis tenuis (Plathelminthes, Paludicola): an immunocytochemical study. Zoomorphology 116:111–122Google Scholar
  60. Rieger RM, Tyler S, Smith JPS III, Rieger GE (1991a) Platyhelminthes: Turbellaria. In: Harrison FW, Bogitsh BJ (eds) Microscopic anatomy of invertebrates. Vol 3, Platyhelminthes and Nemertinea. Wiley-Liss, New York, pp 7–140Google Scholar
  61. Rieger R, Salvenmoser W, Legniti A, Reindl S, Adam H, Simonsberger P, Tyler S (1991b) Organization and differentiation of the body-wall musculature in Macrostomum (Turbellaria, Macrostomidae). Hydrobiologia 227:119–129Google Scholar
  62. Romero R, Baguñà J (1991) Quantitative cellular analysis of growth and reproduction in freshwater planarians (Turbellaria; Tricladida). I. A cellular description of the intact organism. Invertebr Rep Dev 19:157–165Google Scholar
  63. Saló 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(1–2):67–74PubMedGoogle Scholar
  64. Sánchez Alvarado A, Newmark PA (1999) Double-stranded RNA specifically disrupts gene expression during planarian regeneration. Proc Natl Acad Sci USA 96:5049–5054PubMedGoogle Scholar
  65. Sánchez 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(24):5659–5665PubMedGoogle Scholar
  66. Sánchez Alvarado A, Reddien PW, Newmark PA, Nusbaum C (2003) Proposal for the sequencing of a new target genome: white paper for a Planarian Genome Project. The Schmidtea mediterranea Sequencing ConsortiumGoogle Scholar
  67. Seilern-Aspang F (1958) Entwicklungsgeschichtliche studien an paludicolen tricladen. Roux’ Arch Entwicklungsmech 150:S425–S480Google Scholar
  68. Skaer RJ (1965) The origin and continuous replacement of epidermal cells in the planarian Plycelis tenuis (Ijima). J Embryol Exp Morphol 13(1):129–139PubMedGoogle Scholar
  69. Stevens M (1904) On the germ cells and the embryology of Planaria simplissima. Proc Natl Acad Sci Philadelphia 56:208–220Google Scholar
  70. Thomas MB (1986) Embryology of the Turbellaria and its phylogenetic significance. Hydrobiologia 132:105–115Google Scholar
  71. Umesono Y, Watanabe K, Agata K (1997) A planarian orthopedia homolog is specifically expressed in the branch region of both mature and regenerating brain. Dev Growth Differ 39(6):723–727PubMedGoogle Scholar
  72. Umesono Y, Watanabe K, Agata K (1999) Distinct structural domains in the planarian brain defined by the expression of evolutionarily conserved homeobox genes. Dev Genes Evol 209(1):31–39PubMedGoogle Scholar
  73. Watt FM, Hogan BLM (2000) Out of Eden: stem cells and their niches. Science 25:1427–1430Google Scholar
  74. Wolff E (1962) Recent researches on the regeneration of planaria. In: Rudnick D (ed.) Regeneration: 20th growth symposium. Ronald Press, New York, pp. 53-84Google Scholar
  75. Wray AG (2000) The evolution of embryonic patterning mechanisms in animals. Sem Cell Dev Biol 11:385–393Google Scholar
  76. Younossi-Hartenstein A, Hartenstein V (2000a) Comparative approach to developmental analysis: the case of the dalyellid flatworm, Gieysztoria superba. Int J Dev Biol 44(5):499–506PubMedGoogle Scholar
  77. Younossi-Hartenstein A, Hartenstein V (2000b) The embryonic development of the polyclad flatworm Imogine mcgrathi. Dev Genes Evol 210(8–9):383–398PubMedGoogle Scholar
  78. Younossi-Hartenstein A, Hartenstein V (2001) The embryonic development of the temnocephalid flatworms Craspedella pedum and Diceratocephala boschmai. Cell Tissue Res 304(2):295–310PubMedGoogle Scholar
  79. Younossi-Hartenstein A, Ehlers U, Hartenstein V (2000) Embryonic development of the nervous system of the rhabdocoel flatworm Mesostoma lingua (Abilgaard, 1789). J Comp Neurol 416(4):461–474PubMedGoogle Scholar

Copyright information

© Springer-Verlag 2004

Authors and Affiliations

  • Albert Cardona
    • 1
  • Volker Hartenstein
    • 2
  • Rafael Romero
    • 1
  1. 1.Department of Genetics, Faculty of BiologyUniversity of BarcelonaBarcelonaSpain
  2. 2.Department Molecular, Cell and Developmental BiologyUniversity of California Los AngelesLos AngelesUSA

Personalised recommendations