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Stem Cells in Marine Organisms pp 267–280Cite as

Stem Cells in Sexual and Asexual Reproduction of Botryllus schlosseri (Ascidiacea, Tunicata): An Overview

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Abstract

Botryllus schlosseri, a colonial ascidian reproducing both sexually and asexually, is an excellent model for the study of adult stem cells, since budding blastozooids are derived from a disc of stem cells at the parental atrial chamber and the overlying epidermis. At the colony level, adult zooids undergo cyclical generation changes during which the adults die, are resorbed and then replaced by their buds which reach functional maturity and start filtering. At the same time, blood cell renewal takes place thanks to a new haemopoietic wave. Several experimental manipulations were used to evaluate the behaviour of stem cells during bud morphogenesis under different developmental constraints. When all zooids and buds of a colony are extirpated, new developed zooids are derived from totipotent blood cells which aggregate on the walls of the blood vessels of the tunic. Stem cells can also be transferred from one colony to another through vasculature during fusion of allogeneic compatible colonies. Germ stem cells persist in a host colony so that heterochtonous offspring can be collected after many blastogenetic generations. The persistence of somatic stem cells alters the fusibility pattern of the colony. Pluripotent stem cells are also involved in the embryonic development of larval and juvenile organs; these embryonic cells were analysed and compared with bud stem cells for their potentials and gene expression.

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References

  • Ballarin L, Cima F (2005) Cytochemical properties of Botryllus schlosseri haemocytes: Indica-tions for morpho-functional characterisation. Eur J Histochem 49:255–264

    CAS  Google Scholar 

  • Ballarin L, Menin A, Tallandini L, Matozzo V, Burighel P, Basso G, Fortunato E, Cima F (2008) Haemocytes and blastogenetic cycle in the colonial ascidian Botryllus schlosseri: A matter of life and death. Cell Tissue Res 331:555–564

    Google Scholar 

  • Berrill NJ (1941) The development of the bud in Botryllus. Biol Bull 80:169–184

    Article  Google Scholar 

  • Brien P (1948) Morphologie et reproduction des tuniciers. In: Grassé PP (ed) Traité de Zoologie, vol 11. Masson, Paris, pp 553–1040

    Google Scholar 

  • Brown FD, Swalla BJ (2007) Vasa expression in a colonial ascidian, Botrylloides violaceus. Evol Dev 9:165–177

    CAS  Google Scholar 

  • Burighel P (1970) Sviluppo e differenziamento del tubo digerente nel blastozooide dell'ascidia coloniale Botryllus schlosseri (Pallas). Boll Zool 37:177–192

    Google Scholar 

  • Burighel P, Brunetti R (1971) The circulatory system in the blastozooid of the colonial ascidian Botryllus schlosseri (Pallas). Boll Zool 38:273–289

    Google Scholar 

  • Burighel P, Brunetti R, Zaniolo G (1976) Hibernation of the colonial ascidian Botrylloides leachi (Savigny): Histological observations. Boll Zool 43:293–301

    Google Scholar 

  • Burighel P, Lane NJ, Zaniolo G, Manni L (1998) Neurogenic role of the neural gland in the development of the ascidian, Botryllus schlosseri (Tunicata, Urochordata). J Comp Neurol 394:230–241

    Article  CAS  Google Scholar 

  • Buss L (1987) The evolution of individuality. Princeton University Press, Princeton

    Google Scholar 

  • Casagrande L, Martinucci GB, Burighel P (1993) Origin and differentiation of branchial stigmata in the compound ascidian Botryllus schlosseri (Tunicata). Animal Biol 2:111–121

    Google Scholar 

  • Cima F, Basso G, Ballarin L (2003) Apoptosis and phosphatidylserine-mediated recognition dur-ing the take-over phase of the colonial life-cycle in the ascidian Botryllus schlosseri. Cell Tissue Res 312:369–376

    Article  Google Scholar 

  • De Tomaso AW (2006) Allorecognition polymorphism versus parasitic stem cells. Trends Gen 22:485–490

    Article  Google Scholar 

  • Freeman G (1964) The role of blood cells in the process of asexual reproduction in the tunicate Perophora viridis. J Exp Zool 156:157–184

    Article  CAS  Google Scholar 

  • Kawamura K, Nakauchi M (1986) Mitosis and body patterning during morphallactic development of palleal buds in ascidians. Dev Biol 116:39–50

    Article  Google Scholar 

  • Kawamura K, Nakauchi M (1991) Homeostatic integration of stem cell dynamics during palleal budding of ascidians. Zool Sci 8:11–22

    Google Scholar 

  • Kawamura K, Hashimoto K, Nakauchi M (1995) Development of irradiated tunicate buds: Is cell division required for morphallaxis? Dev Growth Diff 37:487–496

    Article  Google Scholar 

  • Kawamura K, Kouki T, Kawahara G, Kikuyama S (2002) Hypophyseal development in vertebrates from amphibians to mammals. Gen Comp Endocrinol 126:130–135

    Article  CAS  Google Scholar 

  • Kawamura K, Sugino Y, Sunanaga T, Fujiwara S (2008) Multipotent epithelial cells in the process of regeneration and asexual reproduction in colonial tunicates. Dev Growth Diff 50:1–10

    Google Scholar 

  • Laird DJ, De Tomaso AW, Weissman IL (2005) Stem cells are units of natural selection in a co-lonial ascidian. Cell 123:1351–1360

    Article  CAS  Google Scholar 

  • Lauzon RJ, Ishizuka KJ, Weissman IL (1992) A cyclical, developmentally-regulated death phe-nomenon in a colonial urochordate. Dev Dyn 194:71–83

    CAS  Google Scholar 

  • Mackie GO (1995) On the 'visceral nervous system' of Ciona. J Mar Biol Ass UK 75:141–151

    Article  Google Scholar 

  • Mackie GO, Burighel P (2005) The nervous system in adult tunicates: Current research directions. Canad J Zool 83:151–183

    Article  CAS  Google Scholar 

  • Majone F (1977) Regeneration of isolated bud fragments of Botryllus schlosseri. Acta Embryol Exp 1:11–19

    Google Scholar 

  • Manni L, Burighel P (2006) Common and divergent pathways in alternative developmental processes of ascidians. BioEssays 28:902–912

    Article  Google Scholar 

  • Manni L, Lane NJ, Sorrentino M, Zaniolo G, Burighel P (1999) Mechanism of neurogenesis dur-ing the embryonic development of a tunicate. J Comp Neurol 412:527–541

    Article  CAS  Google Scholar 

  • Manni L, Lane NJ, Zaniolo G, Burighel P (2002) Cell reorganisation during epithelial fusion and perforation: The case of ascidian branchial fissures. Dev Dyn 224:303–313

    Article  Google Scholar 

  • Manni L, Zaniolo G, Cima F, Burighel P, Ballarin L (2007) Botryllus schlosseri: A model ascidian for the study of asexual reproduction. Dev Dyn 236:335–352

    Article  CAS  Google Scholar 

  • Nyholm SV, Passegue E, Ludington WB, Voskoboynik A, Mitchel K, Weissman IL, De Tomaso AW (2006) Fester, a candidate allorecognition receptor from a primitive chordate. Immunity 25:163–173

    Article  CAS  Google Scholar 

  • Nunzi MG, Burighel P, Schiaffino S (1979) Muscle cell differentiation in the ascidian heart. Devel Biol 68:371–380

    Article  CAS  Google Scholar 

  • Oka H, Watanabe H (1959) Vascular budding in Botrylloides. Biol Bull 117:340–346

    Article  Google Scholar 

  • Rinkevich B, Shapira M (1999) Multi-partner urochordate chimeras outperform two-partner chimerical entities. Oikos 87:315–320

    Article  Google Scholar 

  • Rinkevich B, Shlemberg Z, Fishelson L (1995) Whole-body protochordate regeneration from totipotent blood cells. Proc Natl Acad Sci USA 92:7695–7699

    Article  CAS  Google Scholar 

  • Rinkevich B, Weissman IL, De Tomaso AW (1998) Transplantation of Fu/HC incompatible zooids in Botryllus schlosseri results in chimerism. Biol Bull 195:98–106

    Article  CAS  Google Scholar 

  • Rinkevich Y, Paz G, Rinkevich B, Reshef R (2007) Systemic bud induction and retinoic acid signaling underlie whole body regeneration in the urochordate Botrylloides leachi. PLoS Biol 5:e71. doi:10.1371/journal.pbio.0050071

    Article  Google Scholar 

  • Takamura K, Fujimura M, Yamaguchi Y (2002) Primordial germ cells originate from the endo-dermal strand cells in the ascidian Ciona intestinalis. Dev Genes Evol 212:11–18

    Article  CAS  Google Scholar 

  • Tiozzo S, Christiaen L, Deyts C, Manni L, Joly JS, Burighel P (2004) Embryonic versus blasto-genetic development in the compound ascidian Botryllus schlosseri: Insights from Pitx ex-pression patterns. Dev Dyn 232:468–478

    Article  Google Scholar 

  • Tiozzo S, Ballarin L, Burighel P, Zaniolo G (2006) Programmed cell death in vegetative devel-opment: Apoptosis during the colonial life-cycle of the ascidian Botryllus schlosseri. Tissue Cell 38:193–201

    Article  CAS  Google Scholar 

  • Sabbadin A (1955) Osservazioni sullo sviluppo, l'accrescimento e la riproduzione di Botryllus schlosseri (Pallas), in condizioni di laboratorio. Boll Zool 22:243–263

    Google Scholar 

  • Sabbadin A (1956) Situs inversus viscerum provocato sperimentalmente in Botryllus schlosseri (Pallas) Ascidiacea. Rendiconti Accademia Nazionale Lincei 20:659–666

    Google Scholar 

  • Sabbadin A (1958) Analisi sperimentale dello sviluppo delle colonie di Botryllus schlosseri (Pal-las) [Ascidiacea]. Arch Ital Anat Embr 63:178–221

    CAS  Google Scholar 

  • Sabbadin A (1962) Le basi genetiche della capacità di fusione fra colonie in Botryllus schlosseri (Ascidiacea). Rendiconti Accademia Nazionale Lincei, 32:1031–1035

    Google Scholar 

  • Sabbadin A (1982) Formal genetics of ascidians. Am Zool 22:765–773

    Google Scholar 

  • Sabbadin A (1994) Coloniality in ascidians and its adaptive value, with special reference to Bot-ryllus schlosseri. Animal Biol 3:157–163

    Google Scholar 

  • Sabbadin A, Astorri C (1988) Chimeras and histocompatibility in the colonial ascidian Botryllus schlosseri. Dev Comp Immunol 12:737–747

    Article  CAS  Google Scholar 

  • Sabbadin A, Ballarin L (1990) The reaction of the colonial ascidian Botryllus schlosseri to al-logeneic blood. Preliminary results. Acta Embryol Morphol Exp ns 11:211–212

    Google Scholar 

  • Sabbadin A, Zaniolo G (1979) Sexual differentiation and germ cell transfer in the colonial ascidian Botryllus schlosseri. J Exp Zool 207:289–304

    Article  Google Scholar 

  • Sabbadin A, Zaniolo G, Majone F (1975) Determination of polarity and bilateral asymmetry in palleal and vascular buds of the ascidian Botryllus schlosseri. Dev Biol 46:79–87

    Article  CAS  Google Scholar 

  • Sabbadin A, Burighel P, Zaniolo G (1991) Studies on the colonial ascidian Botryllus schlosseri. A review of some lines of research. Acta Embryol Morphol Exp ns 12:259–279

    Google Scholar 

  • Sala M (1973) Differenziamento in vitro di cellule della linea sanguigna da elementi mesenchi-mali di larva di Botryllus schlosseri. Atti Memorie Accademia Patavina Scienze Lettere Arti 85:275–293

    Google Scholar 

  • Stoner DS, Rinkevich B, Weissman IL (1999) Heritable germ and somatic cell lineage competi-tions in chimeric colonial protochordates. Proc Natl Acad Sci USA 96:9148–9153

    Article  CAS  Google Scholar 

  • Sunanaga T, Saito Y, Kawamura K (2006) Postembryonic epigenesis of Vasa-positive germ cells from aggregated hemoblasts in the colonial ascidian, Botryllus primigenus. Dev Growth Diff 48:87–100

    Article  Google Scholar 

  • Voskoboynik A, Simon-Blecher N, Soen Y, Rinkevich B, De Tomaso AW, Ishizuka KJ, Weiss-man IL (2007) Striving for normality: Whole body regeneration through a series of abnormal generations. FASEB J 21:1335–1344

    Article  CAS  Google Scholar 

  • Weissman IL (2000) Stem cells: Units of development, units of regeneration, and units in evolution. Cell 100:157–168

    Article  CAS  Google Scholar 

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Acknowledgments

Grant information: grants from the Ministero della Università e Ricerca Scientifica e Tecnologica to L.B. and L.M.

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Authors and Affiliations

  1. Department of Biology, University of Padova, via U. Bassi 58/B, 35131, Padova, Italy

    Loriano Ballarin & Lucia Manni

Authors
  1. Loriano Ballarin
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  2. Lucia Manni
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Correspondence to Loriano Ballarin .

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Editors and Affiliations

  1. Limnological Research, Israel Oceanographic & , Haifa, 31 080, Israel

    Baruch Rinkevich

  2. Istituto di Biomedicina e Immunologia, CNR Palermo, Via La Malfa 153, Palermo, 90146, Italy

    Valeria Matranga

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Ballarin, L., Manni, L. (2009). Stem Cells in Sexual and Asexual Reproduction of Botryllus schlosseri (Ascidiacea, Tunicata): An Overview. In: Rinkevich, B., Matranga, V. (eds) Stem Cells in Marine Organisms. Springer, Dordrecht. https://doi.org/10.1007/978-90-481-2767-2_11

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