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

  • William R. Jeffery (a1) and Billie J. Swalla (a1)


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.


Corresponding author

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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Bennett, V. (1990). Spectrin based membrane skeleton: a multipotential adaptor between plasma membrane and cytoplasm. Physiol. Rev. 70, 1029–65.
Berrill, N.J. (1931). Studies in tunicate development: abbreviation of development in the Molgulidae. Phil. Trans. R. Soc. Lond. [Biol]. 219, 281346.
Conklin, E.G. (1905). The organization and cell lineage of the ascidian egg. J. Acad. Nat. Sci. Phila. 13, 1119.
Culver, D.C. (1982). Cave Life:Ecology and Evolution. Cambridge, Mass: Harvard Universty Press.
Debus, E., Weber, K. & Osborn, M. (1983). Monoclonal antibodies specific for glial fibrillary acidic (GFA)and each of the neurofilament triplet polypeptides. Differentiation 25, 195203.
Fairbanks, G., Steck, T.L. & Wallach, D.F. (1971). Electrophoretic analysis of the major polypeptides of the human eryhrocyte membrane. Biochemistry. 10, 2606–17.
Jeffery, W.R. (1984 a). pattern formation by ooplasmic segregation in ascidian eggs. Biol. Bull. 166, 277–98.
Jeffery, W.R. (1984 b). Spatial distribution of messenger RNA in the cytoskeletal framework of ascidian eggs. Dev. Biol. 103, 482–92.
Jeffery, W.R. (1985). Identification of proteins and mRNAs in isolated yellow crescents of ascidian eggs. J.Embryol.Exp.Morphol. 89, 275–87.
Jeffery, W.R. (1988). The role of cytoplasmic determinants in embryonic development. In: Developmental Biology:A Comprehensive Synthesis, Browder, L.153. New York: Plenum Press.
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.
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.
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.
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.
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.
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.
Jeffery, W.R. & Swalla, B.J. (1992). Factors necessary for restoring an evolutionary change in an anural ascidian embryo. Dev. Biol. 153, 194205.
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.
Laemmli, U.K. (1970). Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227, 680–5.
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.
Nishida, H. (1992). Regionality of egg cytoplasm that promotes muscle differentiation in embryos of the ascidian Halocynthia roretzi, Development 116, 521–9.
Pumplin, D.W. & Bloch, R.J. (1993). The membrane skeleton. Trends Cell Biol. 3, 113–17.
Sardet, C., Speksnijder, J.E., Inoué, S. & Jaffe, L.F. (1989). Fertilization and ooplasmic movements in the ascidian egg. Development 105, 237–49.
Sardet, C., Speksnider, J.E., Terasaki, M. & Chang, P. (1992). Polarity of the ascidian egg cortex before fertilization. Development 115, 221–37.
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.
Sawada, T. & Osanai, K. (1981). The cortical contraction related to ooplasmic segregation Wilhelm Reuzs Arch. Dev. Biol. 190, 208–14.
Sawada, T. & Osanai, K. (1985). Distribution of actin thaments in fertilized eggs of the ascidian Ciena infesfinalfs. Dev. Blol. 111, 260–5.
Shaw, G., Debus, S. & Weber, K. (1984). The immunological relatedness of neurofilament proteins of higher vertebrates. Sue. J. Cell Biol. 34, 130–6.
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.
Swaila, B.J. (1992). The role of maternal factors in ascidian muscle development. Semin. Dev. Bloli. 3, 287–95.
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.
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.
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.
Whittaker, J.R. (1979). Development of vestigial tail muscle acetylcholinesterase in embryos of an anural ascidian species. Biol. Bull. 156, 393407.
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.


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

  • William R. Jeffery (a1) and Billie J. Swalla (a1)


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