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An ankryin-like protein in ascidian eggs and its role in the evolution of direct development

Published online by Cambridge University Press:  26 September 2008

William R. Jeffery  and
Billie J. Swalla
William R. Jeffery*
Affiliation:
Section of Molecular and Cellular Biology and Bodega Marine Laboratory, University of California, Davis, California, USA, and Station Biologique, Roscoff, France
Billie J. Swalla
Affiliation:
Section of Molecular and Cellular Biology and Bodega Marine Laboratory, University of California, Davis, California, USA, and Station Biologique, Roscoff, France
*
Dr. William R. Jeffery, Bodega Marine Laboratory, University of California, Davis, PO Box 247, Bodega Bay, CA 94923, USA. Fax: 1-707-875-2089.
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Summary

An erythrochyte anti-ankryin antibody was used to investigate the presence and distribution of ankryin in eggs and embryos of ascidian species with different modes of development. In eggs of the indirect developer Ascidia ceratodes anti-ankryin reacted with a 210 kDa polypeptide which has an electrophoretic mobility similar to the vertebrate ankryins. Immunofluorescence microscopy showed that the ankryin-like protein is co-distributed with the myoplasm throughout development. It is restricted to a thin layer under the plasma membrane in unfertilised eggs, undergoes ooplasmic segregation to the posterior pole of the zygote after fertilisation, and is distributed to the tail muscle cells during cleavage and embryogenesis. After gastrulation and neurulation, lower levels of the ankryin-like protein, presumably of zygotic origin, were observed in brain cells and in the apical margin of epidermal cells. The ankryin-like protein was also localised in the myoplasm in eggs and embryos of another indirect developing species, Halocynthia roretzi. The ankryin-like protein may link the cytoskeleton with the plasma membrane in ascidian eggs, as it does in vertebrate erythrocytes. In contrast to A. ceratodes and H. rorefzi, which are members of the families Ascidiidae and Pyuridae respectively, the pattern of ankryin-like protein expression was changed in five species in the family Molgulidae. These molgulid ascidians exhibit either indirect or direct development, and eggs of the direct developing species have lost or modified the myoplasm. The ankryir like protein was present in young oocytes but failed to persist during oogenesis and disappeared in mature eggs and embryos of these molgulid species. The change in ankryin-like protein expression may be a preadaptation for loss of the myoplasm and the evolution of direct development.

Keywords

AnkryinAscidian embryosEgg CytoskeletonEvolution of developmentOoplasmic segregation
Type
Review Article
Information
Zygote , Volume 1 , Issue 3 , August 1993 , pp. 197 - 208
Copyright
Copyright © Cambridge University Press 1993

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References

Bennett, V. (1990). Spectrin based membrane skeleton: a multipotential adaptor between plasma membrane and cytoplasm. Physiol. Rev. 70, 1029–65.CrossRefGoogle ScholarPubMed
Berrill, N.J. (1931). Studies in tunicate development: abbreviation of development in the Molgulidae. Phil. Trans. R. Soc. Lond. [Biol]. 219, 281–346.Google Scholar
Conklin, E.G. (1905). The organization and cell lineage of the ascidian egg. J. Acad. Nat. Sci. Phila. 13, 1–119.Google Scholar
Culver, D.C. (1982). Cave Life:Ecology and Evolution. Cambridge, Mass: Harvard Universty Press.CrossRefGoogle Scholar
Debus, E., Weber, K. & Osborn, M. (1983). Monoclonal antibodies specific for glial fibrillary acidic (GFA)and each of the neurofilament triplet polypeptides. Differentiation 25, 195–203.Google Scholar
Fairbanks, G., Steck, T.L. & Wallach, D.F. (1971). Electrophoretic analysis of the major polypeptides of the human eryhrocyte membrane. Biochemistry. 10, 2606–17.Google Scholar
Jeffery, W.R. (1984 a). pattern formation by ooplasmic segregation in ascidian eggs. Biol. Bull. 166, 277–98.CrossRefGoogle Scholar
Jeffery, W.R. (1984 b). Spatial distribution of messenger RNA in the cytoskeletal framework of ascidian eggs. Dev. Biol. 103, 482–92.Google Scholar
Jeffery, W.R. (1985). Identification of proteins and mRNAs in isolated yellow crescents of ascidian eggs. J.Embryol.Exp.Morphol. 89, 275–87.Google ScholarPubMed
Jeffery, W.R. (1988). The role of cytoplasmic determinants in embryonic development. In: Developmental Biology:A Comprehensive Synthesis, Browder, L.1–53. New York: Plenum Press.Google Scholar
Jeffery, W.R. (1993). The myoplasm of ascidian eggs: a plasma membrane cytoskeleton containing spectrin and Na+ K+-ATPase which is modified during evolution Biol. Res.Google Scholar
Jeffery, W.R. & Meier, S. (1983). A yellow crescent cytoskeletal domain in ascidian eggs and its role in early development. Dev. Biol. 96, 125–43.CrossRefGoogle ScholarPubMed
Jeffery, W.R. & Meier, S. (1984). Ooplasmic segregation of the myoplasmic actin network in stratified ascidian eggs. Wilhelm Roux's Arch. Dev. Biol. 193, 257–62.Google Scholar
Jeffery, W.R. & Swalla, B.J. (1990 a). The myoplasm of ascidian eggs: a localized cytoskeletal domain with multiple roles in embryonic development, Semin. Cell Biol. 1, 373–81.Google Scholar
Jeffery, W.R. & Swalla, B.J. (1990 b). Anural development in ascidians: evolutionary modification and elimination of the tadpole larva. Semin. Dev. Biol. 1, 253–61.Google Scholar
Jeffery, W.R. & Swalla, B.J. (1991). An evolutionary change in the muscle lineage of an anural ascidian embryo is restored by interspecific hybridization with a urodele ascidian. Dev. Biol. 145, 328–37.Google Scholar
Jeffery, W.R. & Swalla, B.J. (1992). Factors necessary for restoring an evolutionary change in an anural ascidian embryo. Dev. Biol. 153, 194–205.CrossRefGoogle Scholar
Kordeli, E. & Bennett, V. (1991). Distinct ankryin isoforms at neuron cell bodies and nodes of Ranvier resolved in erythrocyte ankryin-deficient mice. J. Cell Biol. 114, 1243–59.Google Scholar
Laemmli, U.K. (1970). Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227, 680–5.Google Scholar
Nishikata, T., Mita-Miyazawa, I., Deno, T. & Satoh, N. (1987). Monoclonal antibodies against components of the myoplasm of eggs of the ascidian Ciona intestinalis partially block the development of muscle-specific acetylcholinesterase, Development 100, 577–86.Google Scholar
Nishida, H. (1992). Regionality of egg cytoplasm that promotes muscle differentiation in embryos of the ascidian Halocynthia roretzi, Development 116, 521–9.Google Scholar
Pumplin, D.W. & Bloch, R.J. (1993). The membrane skeleton. Trends Cell Biol. 3, 113–17.CrossRefGoogle ScholarPubMed
Sardet, C., Speksnijder, J.E., Inoué, S. & Jaffe, L.F. (1989). Fertilization and ooplasmic movements in the ascidian egg. Development 105, 237–49.Google Scholar
Sardet, C., Speksnider, J.E., Terasaki, M. & Chang, P. (1992). Polarity of the ascidian egg cortex before fertilization. Development 115, 221–37.CrossRefGoogle ScholarPubMed
Satoh, N., Deno, T., Nishida, H., Nishikata, T. & Makabe, K.W. (1990). Cellular and molecular mechanisms of muscle cell differentiation in ascidian embryos. Int. Rev. Cytol. 122, 221–58.Google Scholar
Sawada, T. & Osanai, K. (1981). The cortical contraction related to ooplasmic segregation Wilhelm Reuzs Arch. Dev. Biol. 190, 208–14.Google Scholar
Sawada, T. & Osanai, K. (1985). Distribution of actin thaments in fertilized eggs of the ascidian Ciena infesfinalfs. Dev. Blol. 111, 260–5.Google Scholar
Shaw, G., Debus, S. & Weber, K. (1984). The immunological relatedness of neurofilament proteins of higher vertebrates. Sue. J. Cell Biol. 34, 130–6.Google Scholar
Speksnijder, J.E., Terasaki, M., Hage, W.J., Jaffe, L.F. & Sardet, C. (1993). Polarity and reorganization of the endoplasmic reticulum during fertilization and ooplasmic segregation in the ascidian egg. J. Cell Blat. 120, 1337–46.Google Scholar
Swaila, B.J. (1992). The role of maternal factors in ascidian muscle development. Semin. Dev. Bloli. 3, 287–95.Google Scholar
Swaila, B. & Jeffery, W.R. (1990). Interspecific hybridization between an anural and urodele ascidian: differential expression of urodele features suggests multiple mechanisms control anural development. Dev. Biol. 142, 319–34.CrossRefGoogle Scholar
Swaila, B., Badgett, M.R. & Jeffery, W.R. (1991). Identification of a cytoskeletal protein localized in the myoplasm of ascidian eggs: localization is modified during anural development. Development 111, 425–36.Google Scholar
Towbin, H., Staehlin, T. & Gordon, J. (1979). Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedures and some applications. Proc. natl. Acad. Sci USA 76, 4350–4.Google Scholar
Whittaker, J.R. (1979). Development of vestigial tail muscle acetylcholinesterase in embryos of an anural ascidian species. Biol. Bull. 156, 393–407.CrossRefGoogle ScholarPubMed
Whittaker, J.R. (1980). Acetylcholinesterase development in extra cells caused by changing the distribution of myoplasm in ascidian embryos. J. Embyol. Exp. Morphol. 55, 343–54.Google Scholar