Skip to main content
Log in

Fine structure of naive and allogeneic challenged ampullae in Botrylloides subpopulation I from the Mediterranean coast of Israel

  • Research Article
  • Published:
Marine Biology Aims and scope Submit manuscript

Abstract

The external peripheral termini of vasculature in botryllid ascidians (ampullae) are important in the expression of effector mechanisms during histocompatibility reactions. We study here morphological changes to the microstructure during allorecognition in Botrylloides subpopulation I (SP1) from the Mediterranean coast of Israel, where special giant ampullae, called megaloampullae are developed hours after first allogeneic challenge. The basal part of each naive ampulla consists of a sheath of continuous squamous epithelial cells (1 μm×20 μm). At the tip of the ampullae, about 130 epithelial cells become columnar with wide apical pads (15 μm×5–10 μm), that contain electron-opaque “adhesive vesicles”. Foci of crystallizations were observed within the vesicles of some columnar cells. Ampullar epithelial cells develop internal folds that support tight attachments between circulating blood cells (most of them are pigment cells) and ampullar epithelium. During the histoincompatibility process, the tunic peripheral edge at the interaction area becomes highly convoluted. Filaments (up to 1.16 μm) accumulate in the interaction tunic matrix. Some of these filaments encircle destructed cells. Fragmented cell membranes are also found next to the reacting ampullae. The most characteristic feature of the Botrylloides SP1 rejection reaction is dilation of the ampullae. The ampullar epithelium becomes “curly” when megaloampullae are formed. Within the curly region, about 30% of the squamous epithelial cells are further stretched, up to 33 μm in length. Some additional mechanisms are suggested to explain the fast increase (up to seven times) in ampullar width that is recorded within a few hours from the first allogeneic contact.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9
Fig. 10
Fig. 11

Similar content being viewed by others

References

  • Ballarin L, Cima F, Sabbadin A (1995) Morula cells and histocompatibility in the colonial ascidian Botryllus schlosseri. Zool Sci 12:757–764

    Article  Google Scholar 

  • Cima F, Sabbadin A, Ballarin L (1995) Cellular aspects of allorecognition in the compound ascidian Botryllus schlosseri. Dev Comp Immunol 28:881–889

    Article  Google Scholar 

  • De Santo RS, Dudley PL (1969) Ultramicroscopic filaments in the ascidian Botryllus schlosseri (Pallas) and their possible role in ampullar contractions. J Ultrastruct Res 28:259–274

    Article  PubMed  Google Scholar 

  • Ermak TH (1982) The renewing cell populations of ascidians. Am Zool 22:795–805

    Article  Google Scholar 

  • Hirose E (2003) Colonial allorecognition, hemolytic rejection, and viviparity in botryllid ascidians. Zool Sci 20:387–394

    Article  Google Scholar 

  • Hirose E, Saito Y, Watanabe H (1990) Allogeneic rejection induced by cut surface contact in the compound ascidian, Botrylloides simodensis. Invertebr Reprod Dev 17:159–164

    Article  Google Scholar 

  • Katow H, Watanabe H (1978) Fine structure and possible role of ampullae on tunic supply and attachment in a compound ascidian, Botryllus primigenus Oka. J Ultrastruct Res 64:23–34

    Article  CAS  PubMed  Google Scholar 

  • Katow H, Watanabe H (1980) Fine structure of fusion reaction in compound ascidian Botryllus primigenus Oka. Dev Biol 76:1–14

    Article  CAS  PubMed  Google Scholar 

  • Kawamura K, Fujiwara S (1995) Cellular and molecular characterization of transdifferentiation in the process of morphallaxis of budding tunicates. Semin Cell Biol 6:117–126

    Article  CAS  PubMed  Google Scholar 

  • Milkman R, Byrne S (1961) Recent observations on Botryllus schlosseri. Biol Bull 121:169–221

    Google Scholar 

  • Oka H, Watanabe H (1957) Vascular budding, a new type of budding in Botryllus. Biol Bull 112:225–240

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Pérèz JM (1958) Ascidies reeoltées sur les côtes Méditerranéennes d’Israel. Bull Rec Counc Isr Sect B Zool 7:143–150

    Google Scholar 

  • Rinkevich B (2005) Rejection patterns in botryllid ascidians immunity: the first tier of allorecognition. Can J Zool 83:101–121

    Article  CAS  Google Scholar 

  • Rinkevich B, Saito Y (1992) Self-nonself recognition in the colonial protochordate Botryllus schlosseri from Mutsu Bay, Japan. Zool Sci 9:983–988

    Google Scholar 

  • Rinkevich B, Weissman IL (1992) Incidents of rejection and indifference in Fu/HC incompatible protochordate colonies. J Exp Zool 263:105–111

    Article  CAS  PubMed  Google Scholar 

  • Rinkevich B, Shlemberg Z, Lilker-Levav T, Goren M, Fishelson L (1993) Life history characteristics of Botrylloides (Tunicata) populations in Akko Bay, Mediterranean coast of Israel. Israel J Zool 39:197–212

    Google Scholar 

  • Rinkevich B, Lilker-Levav T, Goren M (1994) Allorecognition/xenorecognition responses in Botrylloides (Ascidiacea) subpopulations from the Mediterranean coast of Israel. J Exp Zool 270:302–313

    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  PubMed Central  PubMed  Google Scholar 

  • Rinkevich B, Shlemberg Z, Fishelson L (1996) Survival budding processes in the colonial tunicate Botrylloides from the Mediterranean Sea: the role of totipotent blood cells. In: Maramorosch K, Loeb MJ (eds) Invertebrate cell culture: looking towards the 21st century. In Vitro Society Press, Charlotte, NC, pp 1–9

  • Rinkevich B, Tartakover S, Gershon H (1998) Contribution of morula cells to allogeneic responses in the colonial urochordate Botryllus schlosseri. Mar Biol 131:227–236

    Article  Google Scholar 

  • Sabbadin A, Zaniolo G, Ballarin L (1992) Genetic and cytological aspects of histocompatibility in ascidians. Boll Zool 59:167–173

    Article  Google Scholar 

  • Saito Y, Hirose E, Watanabe H (1994) Allorecognition in compound ascidians. Int J Dev Biol 38:237–247

    CAS  PubMed  Google Scholar 

  • Tanaka K (1973) Allogeneic inhibition in a composed ascidian, Botryllus primigenus Oka. II. Cellular and humoral responses in “nonfusion” reaction. Cell Immunol 7:427–443

    Article  CAS  PubMed  Google Scholar 

  • Tanaka K, Watanabe H (1973) Allogeneic inhibition in a compound ascidian, Botryllus primigenus Oka. I. Processes and features of “nonfusion” reaction. Cell Immunol 7:410–426

    Article  CAS  PubMed  Google Scholar 

  • Taneda Y, Saito Y, Watanabe H (1985) Self or nonself discrimination in ascidians. Zool Sci 2:433–442

    Google Scholar 

  • Watanabe H, Taneda Y (1982) Self or non-self recognition in compound ascidians. Am Zool 22:775–782

    Article  Google Scholar 

  • Watkins MJ (1958) Regeneration of buds in Botryllus. Biol Bull 112:147–152

    Article  Google Scholar 

  • Watson JM, Scofield VL (1989) Amyloid deposits in the rejection lesions of Botrylloides leachi. J Cell Chem S13:68

    Google Scholar 

  • Weissman IL, Saito Y, Rinkevich B (1990) Allorecognition histocompatibility in a protochordate species: Is the relationship to MHC semantic or structural? Immunol Rev 113:227–241

    Article  CAS  PubMed  Google Scholar 

  • Zaniolo G (1981) Histology of the ascidian Botryllus schlosseri tunic: in particular, the test cells. Boll Zool 48:169–178

    Article  Google Scholar 

  • Zaniolo G, Ballarin L (2001) Colony specificity in Botrylloides leachi (Savigny): preliminary reports. In: Swada H, Yokosawa H, Lambert CC (eds) The biology of ascidians. Springer, Tokyo, pp 442–444

    Chapter  Google Scholar 

Download references

Acknowledgements

The study was supported by the US–Israel Binational Science Foundation and by the Israel Science Foundation (456/01). N.S.-B. was a doctoral fellow of the Charles Clore Foundation. This study is part of N.S.-B.’s PhD dissertation at Bar-Ilan University.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to N. Simon-Blecher.

Additional information

Communicated by O. Kinne, Oldendorf/Luhe

Rights and permissions

Reprints and permissions

About this article

Cite this article

Simon-Blecher, N., Hanania, J., Achituv, Y. et al. Fine structure of naive and allogeneic challenged ampullae in Botrylloides subpopulation I from the Mediterranean coast of Israel. Marine Biology 148, 987–996 (2006). https://doi.org/10.1007/s00227-005-0147-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00227-005-0147-6

Keywords

Navigation