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Stages of embryonic development of the zebrafish
Charles B. Kimmel,
William W. Ballard,
Seth R. Kimmel,
Bonnie Ullmann,
Thomas F. Schilling,
Corresponding Author
Charles B. Kimmel
Institute of Neuroscience, University of Oregon, Eugene, Oregon 97403–1254
Institute of Neuroscience, 1254 University of Oregon, Eugene, OR 97403–1254Search for more papers by this authorWilliam W. Ballard
Department of Biology, Dartmouth College, Hanover, NH 03755
Search for more papers by this authorSeth R. Kimmel
Institute of Neuroscience, University of Oregon, Eugene, Oregon 97403–1254
Search for more papers by this authorBonnie Ullmann
Institute of Neuroscience, University of Oregon, Eugene, Oregon 97403–1254
Search for more papers by this authorThomas F. Schilling
Institute of Neuroscience, University of Oregon, Eugene, Oregon 97403–1254
Search for more papers by this authorCharles B. Kimmel,
William W. Ballard,
Seth R. Kimmel,
Bonnie Ullmann,
Thomas F. Schilling,
Corresponding Author
Charles B. Kimmel
Institute of Neuroscience, University of Oregon, Eugene, Oregon 97403–1254
Institute of Neuroscience, 1254 University of Oregon, Eugene, OR 97403–1254Search for more papers by this authorWilliam W. Ballard
Department of Biology, Dartmouth College, Hanover, NH 03755
Search for more papers by this authorSeth R. Kimmel
Institute of Neuroscience, University of Oregon, Eugene, Oregon 97403–1254
Search for more papers by this authorBonnie Ullmann
Institute of Neuroscience, University of Oregon, Eugene, Oregon 97403–1254
Search for more papers by this authorThomas F. Schilling
Institute of Neuroscience, University of Oregon, Eugene, Oregon 97403–1254
Search for more papers by this authorAbstract
We describe a series of stages for development of the embryo of the zebrafish, Danio (Brachydanio) rerio. We define seven broad periods of embryogenesis—the zygote, cleavage, blastula, gastrula, segmentation, pharyngula, and hatching periods. These divisions highlight the changing spectrum of major developmental processes that occur during the first 3 days after fertilization, and we review some of what is known about morphogenesis and other significant events that occur during each of the periods. Stages subdivide the periods. Stages are named, not numbered as in most other series, providing for flexibility and continued evolution of the staging series as we learn more about development in this species. The stages, and their names, are based on morphological features, generally readily identified by examination of the live embryo with the dissecting stereomicroscope. The descriptions also fully utilize the optical transparancy of the live embryo, which provides for visibility of even very deep structures when the embryo is examined with the compound microscope and Nomarski interference contrast illumination. Photomicrographs and composite camera lucida line drawings characterize the stages pictorially. Other figures chart the development of distinctive characters used as staging aid signposts. ©1995 Wiley-Liss, Inc.
References
- Abdelilah, S., Solnica-Krezel, L., Stainier, D. Y. R., and Driever, W. (1994) The zebrafish mutation janus: implications for dorsoventral axis determination. Nature 370: 468–471.
- Akimenko, M.-A., Ekker, M., Wegner, J., and Westerfield, M., (1994) Combinatorial expression of three zebrafish genes related to distalless: part of a homeobox gene code for the head. J. Neurosci. 14: 3475–3486.
- Ballard, W. W. (1973) Morphogenetic movements in Salmo gairdneri Richardson, J. Exp. Zool. 184: 28–48.
- Ballard, W. W. (1981) Morphogenetic movements and fate maps of vertebrates. Am. Zool. 21: 391–399.
- Ballard, W. W., and Ginsberg, A. S. (1980) Morphogenetic movements in acipenserid embryos. J. Exp. Zool. 213: 69–116.
- Bennett, M. V. L., and Trinkaus, J. P. (1970) Electrical coupling between embryonic cells by way of extracellular space and specialized junctions. J. Cell Biol. 44: 592–610.
- Bernhardt, R. R., Chitnis, A. B., Lindamer, L., and Kuwada, J. Y. (1990) Identification of spinal neurons in the embryonic and larval zebrafish. J. Comp. Neurol. 302: 603–616.
- Betchaku, T., and Trinkaus, J. P. (1978) Contact relations, surface activity, and cortical microfilaments of marginal cells of the enveloping layer of the yolk syncytial and yolk cytoplasmic layers of Fundulus before and during epiboly. J. Exp. Zool. 207: 381–426.
- Brummet, A. R., and Dumont, J. N. (1978) Kupffer's vescicle in Fundulus heteroclitus. A scanning and transmission electron microscope study. Tissue Cell 10: 11–22.
- Chitnis, A. B., and Kuwada J. Y. (1990) Axonogenesis in the brain of zebrafish embryos. J. Neurosci. 10: 1892–1905.
- Dale, L. and Slack, J. M. W. (1987) Fate map for the 32-cell stage of Xenopus laevis. Development 99: 527–551.
- Eisen, J. S. (1991) Determination of primary motoneuron identity in developing zebrafish embryos. Science 252: 569–572.
- Eisen, J. S., Myers, P. Z., and Westerfield, M. (1986) Pathway selection by growth cones of identified motoneurons in live zebrafish embryos. Nature 320: 269–271.
- Eisen, J. S., Pike, S. H., and Romancier, B. (1990) An identified neuron with variable fates in embryonic zebrafish. J. Neurosci. 10: 34–43.
- Ekker, M., Wegner, J., Akimenko, M.-A., and Westerfield, M. (1992) Coordinate embryonic expression of three zebrafish engrailed genes. Development 116: 1001–1010.
- Felsenfeld, A. L., Curry, M., and Kimmel, C. B. (1991) The fub-1 mutation blocks initial myofibril formation in zebrafish muscle pioneer cells. Dev. Biol. 148: 23–30.
- Gould, S. J. (1977) “ Ontogeny and Phylogeny.” Cambridge: Harvard Univ. Press.
- Grunwald, D. J., Kimmel, C. B., Westerfield, M., and Streisinger, G. (1988) A neural degeneration mutation that spares primary neurons in the zebrafish. Dev. Biol. 126: 115–128.
- Halpern, M. E., Ho, R. K., Walker, C., and Kimmel, C. B. (1993) Induction of muscle pioneers and floor plate is distinguished by the zebrafish no tail mutation. Cell 75: 99–111.
- Hanneman, E., and Westerfield, M. (1989) Early expression of acetylcholine-sterase activity in functionally distinct neurons of the zebrafish. J. Comp. Neurol. 284: 350–361.
- Hanneman, E., Trevarrow, B., Metcalfe, W. K., Kimmel, C. B., and Westerfield, M. (1988) Segmental pattern of development of the hindbrain and spinal cord of the zebrafish embryo. Development 103: 49–58.
- Hatada, Y., and Stern, C. D. (1994) A fate map of the epiblast of the early chick embryo. Development 120: 2879–2889.
- Hatta, K., BreMiller, R. A., Westerfield, M., and Kimmel, C. B. (1991a) Diversity of expression of engrailed homeoproteins in zebrafish. Development 112: 821–832.
- Hatta, K., Kimmel, C. B., Ho, R. K., and Walker, C. (1991b) The cyclops mutation blocks specification of the floor plate of the zebrafish CNS. Nature 350: 339–341.
- Helde, K. A., Wilson, E. T., Cretekos, C. J., and Grunwald, D. J. (1994) Contribution of early cells to the fate map of the zebrafish gastrula. Science 265: 517–520.
-
Hisaoka, K. K., and
Battle, H. I.
(1958)
The normal developmental stages of the zebrafish, Brachydanio rerio (Hamilton-Buchanan).
J. Morphol.
102: 311–323.
10.1002/jmor.1051020205 Google Scholar
-
Hisaoka, K. K., and
Firlit, C. F.
(1960)
Further studies on the embryonic development of the zebrafish, Brachydanio rerio (Hamilton-Buchanan).
J. Morphol.
107: 205–225.
10.1002/jmor.1051070206 Google Scholar
- Ho, R. K. (1992a) Cell movements and cell fate during zebrafish gastrulation. Development [Suppl]: 65–73.
- Ho, R. K. (1992b) Axis formation in the embryo of the zebrafish, Brachydanio rerio. Semin. Dev. Biol. 3: 53–64.
- Ho, R. K., and Kimmel, C. B. (1993) Commitment of cell fate in the early zebrafish embryo. Science 261: 109–111.
- Ho, R. K., Ball, E. E., and Goodman, C. S. (1984) Muscle pioneers: large mesodermal cells that erect a scaffold for developing muscles and motoneurones in grasshopper embryos. Nature 301: 66–69.
- Horder, T. J., Presley, R., and Slípka, J. (1993) The segmental bauplan of the rostral zone of the head in vertebrates. Funet. Dev. Morphol. 3: 79–89.
- Kane, D. A. (1991) Zebrafish midblastula transition: the onset of zygotic control during development. Ph.D. Disseration, Univ. of Oregon.
- Kane, D. A., and Kimmel, C. B. (1993) The zebrafish midblastula transition. Development 119: 447–456.
- Kane, D. A., Warga, R. A., and Kimmel, C. B. (1992) Mitotic domains in the early embryo of the zebrafish. Nature 360: 735–737.
- Keller, R. E. (1975) Vital dye mapping of the gastrula and neurula of Xenopus laevis. I Prospective areas and morphogenetic movements of the superficial layer. Dev. Biol. 42: 222–241.
- Keller, R. E. (1976) Vital dye mapping of the gastrula and neurula of Xenopus laevis. II. Prospective areas and morphogenetic movements in the deep region. Dev. Biol. 51: 118–137.
- Keller, R. E. (1980) The cellular basis of epiboly: an SEM study of deep cell rearrangement during gastrulation in Xenopus laevis. J. Embryol. Exp. Morphol. 60: 201–234.
- Keller, R. E., and Tibbets, P. (1989) Mediolateral cell intercalationis a property of the dorsal, axial mesoderm of Xenopus laevis. Dev. Biol. 131: 539–549.
- Kimmel, C. B. (1993) Patterning the brain of the zebrafish embryo. Annu. Rev. Neurosci. 16: 707–732.
- Kimmel, C. B., and Law, R. D. (1985a) Cell lineage of zebrafish blastomeres. I. Cleavage pattern and cytoplasmic bridges between cells. Dev. Biol. 108: 78–85.
- Kimmel, C. B., and Law, R. D. (1985b) Cell lineage of zebrafish blastomers. II. Formation of the yolk syncytial layer. Dev. Biol. 108: 86–93.
- Kimmel, C. B., and Warga, R. M. (1987) Indeterminate cell lineage of the zebrafish embryo. Dev. Biol. 124: 269–280.
- Kimmel, C. B., Kane, D. A., Walker, C., Warga, R. M., and Rothman, M. B. (1989) A mutation that changes cell movement and cell fate in the zebrafish embryo. Nature 337: 358–362.
- Kimmel, C. B., Hatta, K., and Metcalfe, W. K. (1990a) Early axonal contacts during development of an identified dendrite in the brain of the zebrafish. Neuron 4: 535–545.
- Kimmel, C. B., Warga, R. M., and Schilling, T. F. (1990b) Origin and organization of the zebrafish fate map. Development 108: 581–594.
- Kimmel, C. B., Kane, D. A., and Ho, R. K. (1991) Lineage specification during early embryonic development of the zebrafish. In: “ Cell-Cell Interactions in Early Development,” J. Gerhart (ed). New York: Wiley-Liss Inc., pp 203–225.
- Kimmel, C. B., Warga, R. M., and Kane, D. A. (1994) Cell cycles and clonal strings during formation of the zebrafish central nervous system. Development 120: 265–276.
- Krauss, S., Johansen, T., Korzh, V., and Fjose, A. (1991) Expression pattern of zebrafish pax genes suggest a role in early brain regionalization. Nature 353: 267–270.
- Krauss, S., Concordet, J.-P., and Ingham, P. W. (1993) A functionally conserved homolog of the Drosophila segment polarity gene hh is expressed in tissues with polarizing activity in zebrafish embryos. Cell 75: 1431–1444.
- Lawson, K. A., Meneses, J. J., and Pedersen, R. A. (1991) Clonal analysis of epiblast fate during germ layer formation in the mouse embryo. Development 113: 891–911.
- Macdonald, R., Xu, Q., Barth, K. A., Mikkola, I., Holder, N., Fjose, A., Krauss, S., and Wilson, S. W. (1994) Regulatory gene expression boundaries demarcate sites of neuronal differentiation in the embryonic zebrafish forebrain. Neuron 13: 1–20.
- Martindale, M. Q., Meier, S., and Jacobson, A. G. (1987) Mesodermal metamerism in the teleost, Oryzias latipes (the Medaka). J. Morphol. 193: 241–252.
- Melby, A. E., Ho, R. K., and Kimmel, C. B. (1993) An identifiable domain of tail-forming cells in the zebrafish gastrula. Soc. Neurosci. Abstr. 19: 445.
- Mendelson, B. (1986) Development of reticulospinal neurons of the zebrafish. I. Time of origin. J. Comp. Neurol. 251: 160–171.
- Metcalfe, W. K. (1985) Sensory neuronal growth cones comigrate with posterior lateral line primordial cells in zebrafish. J. Comp. Neurol. 238: 218–224.
- Metcalfe, W. K. Myers, P. Z., Trevarrow, B., Bass, M., and Kimmel, C. B. (1990) Primary neurons that express the L2/HNK-1 carbohydrate during early development in the zebrafish. Development 110: 491–504.
- Milos, N., and Dingle, A. D. (1978) Dynamics of pigment formation in the zebrafish, Brachydanio rerio. I. Establishment and regulation of the lateral line melanophore stripe during the first eight days of development. J. Exp. Zool. 205: 205–216.
- Myers, P. Z., Eisen, J. S., and Westerfield, M. (1986) Development and axonal outgrowth of identified motoneurons in the zebrafish. J. Neurosci. 6: 2278–2289.
- Newport, J., and Kirshner, M. (1982a) A major developmental transition in early Xenopus embryos: I. Characterization and timing of cellular changes at the midblastula stage. Cell 30: 675–686.
- Newport, J., and Kirshner, M. (1982b) A major developmental transition in early Xenopus embryos: II. Control of the onset of transcription. Cell 30: 687–696.
- Oxtoby, E., and Jowett, T. (1993) Cloning of the zebrafish krox-20 gene (krx-20) and its expression during hindbrain development. Nucleic Acid Res. 21: 1087–1095.
- Papan, C., and Campos-Ortega, J. (1994) On the formation of the neural keel and neural tube in the zebrafish Danio (Brachydanio) rerio. Rouxs Arch. Dev. Biol. 203: 178–186.
- Raible, D. W., and Eisen, J. S. (1994) Restriction of neural crest cell fate in the trunk of the embryonic zebrafish. Development 120: 495–503.
- Raible, D. W., Wood, A., Hodsdon, W., Henion, P. D., Weston, J. A., and Eisen, J. S. (1992) Segregation and early dispersal of neural crest cells in the embryonic zebrafish. Dev. Dyn. 195: 29–42.
- Reib, J. P. (1973) La circulation sanguine chez l'embryon de Brachydanio rerio. Ann. Embryol. Morphol. 6: 43–54.
- Schilling, T. F., and Kimmel, C. B. (1994) Segment and cell type lineage restrictions during pharyngeal arch development in the zebrafish embryo. Development 120: 483–494.
- Schirone, R. C., and Gross, L. (1968) Effect of temperature on early embryological development of the zebra fish, Brachydanio rerio. J. Exp. Zool. 169: 43–52.
- Schmitz, B., and J. A. Campos-Ortega (1994) Dorso-ventral polarity of the zebrafish embryo is distinguishable prior to the onset of gastrulation. Rouxs Arch. Dev. Biol. 203: 374–380.
- Schmitz, B., Papan, C., and Campos-Ortega, J. A. (1993) Neurulation in the anterior trunk region of the zebrafish Brachydanio rerio. Rouxs Arch. Dev. Biol. 202: 250–259.
- Schulte-Merker, S., Ho, R. K., Herrmann, B. G., and Nüsslein-Volhard, C. (1992) The proteinproduct of the zebrafish homologue of the mouse T gene is expressed in nuclei of the germ ring and the notochord of the early embryo. Development 116: 1021–1032.
- Schulte-Merker, S., van Eeden, F. J. M., Halpern, M. E., Kimmel, C. B., and Nüsslein-Volhard, C. (1994) no tail (ntl) is the zebrafish homologue of the mouse T (Brachyury) gene. Development 120: 1009–1015.
- Solnica-Krezel, L., and Driever, W. (1994) Microtubule arrays of the zebrafish yolk cell: organization and function during epiboly. Development 120: 2443–2455.
- Stachel, S. E., Grunwald, D. J., and Myers, P. Z. (1993) Lithium perturbation and goosecoid expression identify a dorsal specification pathway in the pregastrula zebrafish. Development 117: 1261–1274.
- Stainier, D. Y. R., Lee, R. K., and Fishman, M. C. (1993) Cardiovascular development in the zebrafish. I. Myocardial fate map and heart tube formation. Development 119: 31–40.
- Strähle, U., and Jesuthasan, S. (1993) Ultraviolet irradiation imparis epiboly in zebrafish embryos: evidence for a microtubule-dependent mechanism of epiboly. Development 119: 909–919.
- Strehlow, D., and Gilbert, W. (1993) A fate map for the first cleavages of the zebrafish. Nature 361: 451–453.
- Strehlow, D., Heinrich, G., and Gilbert, W. (1994) The fates of the blastomers of the 16-cell zebrafish embryo. Development 120: 1791–1798.
- Streisinger, G., Walker, C., Dower, N., Knauber, D., and Singer, F. (1981) Production of clones of homozygous diploid zebra fish (Brachydanio rerio). Nature 291: 293–296.
- Thisse, C., Thisse, B., Schilling, T. F., and Postlethwait, J. H. (1993) Structure of the zebrafish snail1 gene and its expression in wildtype, spadetail and no tail mutant embryos. Development 119: 1203–1215.
- Trevarrow, B., Marks, D. L., and Kimmel, C. B. (1990) Organization of hindbrain segments in the zebrafish embryo. Neuron 4: 669–679.
- Trinkaus, J. P. (1984) Mechanism of Fundulus epiboly—a current view. Am. Zool. 24: 673–688.
- Trinkaus, J. P. (1992) The midblastula transition, the YSL transition and the onset of gastrulation in Fundulus. Development [Suppl]: 75–80.
- Warga, R. M., and Kimmel, C. B. (1990) Cell movements during epiboly and gastrulation in zebrafish. Development 108: 569–580.
- Westerfield, M. (1994) “ The Zebrafish Book,” Edition 2.1 Eugene, OR: Univ. Oregon Press.
- Wilson, H. V. (1889) The embryology of the sea bass. Bull. U.S. Fish Comm. 9: 209–277.
- Wilson, S. W., and Easter, S. S., Jr., (1991) Sterotyped pathway selection by growth cones of early epiphysial neurons in the embryonic zebrafish. Development 112: 723–746.
- Wilson, S. W., Ross, L. S., Parrett, T., and Easter, S. S., Jr., (1990) The development of a simple scaffold of axon tracts in the brain of the embryonic zebrafish, Brachydanio rerio. Development 108: 121–145.
- Wilson, E. T., Helde, K. A., and Grunwald, D. J. (1993) Something's fishy here—rethinking cell movements and cell fate in the zebrafish embryo. TIG 9: 348–352.
- Wood, A., and Timmermans, L. P. M. (1988) Teleost epiboly: reassessment of deep cell movement in the germ ring. Development 102: 575–585.
