Hostname: page-component-77c89778f8-vsgnj Total loading time: 0 Render date: 2024-07-24T06:34:19.446Z Has data issue: false hasContentIssue false

A model for ascidian development and developmental modifications during evolution

Published online by Cambridge University Press:  11 May 2009

William R. Jeffery
Affiliation:
Section of Molecular & Cellular Biology and Bodega Marine Laboratory, University of California, Davis, PO Box 247, Bodega Bay, CA 94923, USA

Extract

Ascidian development is reviewed and a model is presented for specification of the larval body plan and cell fate during embryogenesis. The model involves the combined activity of determinants inherited from the egg and inductive cell interactions in the embryo. It is suggested that there are four determinant systems in the egg which are segregated to different blastomeres during cleavage. The ectodermal, endodermal, and muscle determinants specify cell fate autonomously, while the axial determinants initiate cell-shape changes at gastrulation and generate a cascade of inductive activities establishing the larval body plan. In the proposed signalling cascade, the endoderm induces notochord by generating a planar inductive signal late during the cleavage phase, and the notochord cells in turn induce the nervous system by generating a vertical inductive signal in the overlying ectoderm during gastrulation. Ultraviolet (UV) irradiation experiments are described which suggest that axial and muscle determinants exhibit UV-sensitive components resembling nucleic acids and proteins, respectively. The model is evaluated in terms of developmental changes during the evolutionary transition from indirect to direct development. This transition can be explained according to the model by loss or inactivation of the muscle determinants and modification of the inductive activities generated by the axial determinants. These changes are supported by recent studies of embryogenesis in direct-developing ascidians.

Type
Research Article
Copyright
Copyright © Marine Biological Association of the United Kingdom 1994

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Bates, W.R. & Jeffery, W.R., 1987. Localization of axial determinants in the vegetal pole region of ascidian eggs. Developmental Biology, 124, 6576.CrossRefGoogle Scholar
Berrill, N.J., 1931. Studies in tunicate development. II. Abbreviation of development in the Molgulidae. Philosophical Transactions of the Royal Society of London (B), 219, 281346.Google Scholar
Conklin, E.G., 1905. The organization and cell lineage of the ascidian egg. Journal of the Academy of Natural Sciences of Philadelphia, 13, 1119.Google Scholar
Deno, T., Nishida, H. & Satoh, N., 1984. Autonomous muscle cell differentiation in partial embryos according to the newly-verified cell lineages. Developmental Biology, 104, 322328.CrossRefGoogle Scholar
Jeffery, W.R., 1984. Pattern formation by ooplasmic segregation in ascidian eggs. Biological Bulletin. Marine Biological Laboratory, Woods Hole, 166, 277298.CrossRefGoogle Scholar
Jeffery, W.R., 1990a. Ultraviolet irradiation during ooplasmic segregation prevents gastrulation, sensory cell induction, and axis formation in the ascidian embryo. Developmental Biology, 140, 388400.CrossRefGoogle ScholarPubMed
Jeffery, W.R., 1990b. An ultraviolet-sensitive maternal mRNA encoding a cytoskeletal protein may be involved in axis determination in the ascidian embryo. Developmental Biology, 141, 141148.CrossRefGoogle ScholarPubMed
Jeffery, W.R., 1992. A gastrulation center in the ascidian egg. Development, supplement 1992, 5363.CrossRefGoogle Scholar
Jeffery, W.R., 1993. Role of cell interactions in ascidian muscle and pigment cell specification. Wilhelm Roux's Archives of Developmental Biology, 202, 103111.CrossRefGoogle ScholarPubMed
Jeffery, W.R. & Capco, D.G., 1978. Differential accumulation and localization of maternal poly (A)-containing RNA during early development of the ascidian, Styela. Developmental Biology, 67, 152166.CrossRefGoogle ScholarPubMed
Jeffery, W.R. & Swalla, B.J., 1990. Anural development in ascidians: evolutionary modification and elimination of the tadpole larva. Seminars in Developmental Biology, 1, 253261.Google Scholar
Jeffery, W.R. & Swalla, B.J., 1992. Factors necessary for restoring an evolutionary change in an anural ascidian embryo. Developmental Biology, 153, 194205.CrossRefGoogle Scholar
Jeffery, W.R. & Swalla, B.J., 1993. An ankryin-like protein in ascidian eggs and its role in the evolution of direct development. Zygote, 1, in press.CrossRefGoogle Scholar
Kovilur, S., Jacobson, J.W., Beach, R.L., Jeffery, W.R. & Tomlinson, C.R., 1993. Evolution of the chordate muscle actin gene. Journal of Molecular Evolution, 36, 361368.CrossRefGoogle ScholarPubMed
Nishida, H., 1987. Cell lineage analysis in ascidian embryos by intracellular injection of a tracer enzyme. III. Up to the tissue restricted stage. Developmental Biology, 121, 526541.CrossRefGoogle Scholar
Nishida, H., 1990. Determinative mechanisms in secondary muscle lineages of ascidian embryos: development of muscle specific features in isolated muscle progenitor cells. Development, 108, 559568.CrossRefGoogle ScholarPubMed
Nishida, H., 1991. Induction of brain and sensory pigment cells in the ascidian embryo analysed by experiments with isolated blastomeres. Development, 112, 389395.CrossRefGoogle Scholar
Nishida, H., 1992a. Determination of developmental fates of blastomeres in ascidian embryos. Development, Growth and Differentiation, 34, 253262.CrossRefGoogle ScholarPubMed
Nishida, H., 1992b. Developmental potential for tissue differentiation of fully dissociated cells of the ascidian embryo. Wilhelm Roux's Archives of Developmental Biology, 201, 8187.CrossRefGoogle ScholarPubMed
Nishida, H., 1992c. Regionality of egg cytoplasm that promotes muscle differentiation in embryos of the ascidian Halocynthia roretzi. Development, 116, 521529.CrossRefGoogle Scholar
Nishida, H. & Satoh, N., 1983. Cell lineage analysis in ascidian embryos by intracellular injection of a tracer enzyme. I. Up to the eight-cell stage. Developmental Biology, 99, 382394.CrossRefGoogle Scholar
Nishida, H. & Satoh, N., 1985. Cell lineage analysis in ascidian embryos by intracellular injection of a tracer enzyme. II. The 16- and 32-cell stages. Developmental Biology, 110, 440454.CrossRefGoogle ScholarPubMed
Nishida, H. & Satoh, N., 1989. Determination and regulation in the pigment cell lineage of the ascidian embryo. Developmental Biology, 132, 355367.CrossRefGoogle ScholarPubMed
Nishikata, T., Mita-Miyazawa, I., Deno, T., Takamura, K. & Satoh, N., 1987. Expression of epidermis-specific antigens during embryogenesis of the ascidian, Halocynthia roretzi. Developmental Biology, 121, 408416.CrossRefGoogle ScholarPubMed
Reverberi, G., Ortolani, G. & Farinella-Ferruzza, N., 1960. The causal formation of the brain in the ascidian larva. Ada Embryologiae et Morphologiae Experimentalis, 3, 296336.Google Scholar
Rose, S.M., 1939. Embryonic induction in the Ascidia. Biological Bulletin. Marine Biological Laboratory, Woods Hole, 77, 216232.CrossRefGoogle Scholar
Sardet, C., Speksnijder, J.E., Inoué, S. & Jaffe, L.F., 1989. Fertilization and ooplasmic movements in the ascidian egg. Development, 105, 237249.CrossRefGoogle ScholarPubMed
Swalla, B.J. 1992. The role of maternal factors in ascidian muscle development. Seminars in Developmental Biology, 3, 287295.Google Scholar
Swalla, B.J., 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, 425436.CrossRefGoogle ScholarPubMed
Swalla, B.J. & Jeffery, W.R., 1990. Interspecific hybridization between an anural and urodele ascidian: differential expression of urodele features suggests multiple mechanisms control anural development. Developmental Biology, 142, 319334.CrossRefGoogle ScholarPubMed
Swalla, B.J., Makabe, K.W., Satoh, N. & Jeffery, W.R. 1993. Novel genes expressed differentially in ascidians with alternate modes of development. Development, 119, 307318.CrossRefGoogle ScholarPubMed
Whittaker, J.R., 1973. Segregation during ascidian embryogenesis of egg cytoplasmic information for tissue specific enzyme development. Proceedings of the National Academy of Sciences of the United States of America, 70, 20962100.CrossRefGoogle ScholarPubMed
Whittaker, J.R., 1980. Acetylcholinesterase development in extra cells caused by changing the distribution of myoplasm in ascidian embryos. Journal of Embryology and Experimental Morphology, 55, 343354.Google ScholarPubMed
Whittaker, J.R., 1990. Determination of alkaline phosphatase expression in endodermal cell lineages of an ascidian embryo. Biological Bulletin. Marine Biological Laboratory, Woods Hole, 178, 222230.CrossRefGoogle ScholarPubMed