Stages of embryonic development of the zebrafish

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.

[1]  Stephen W. Wilson,et al.  Regulatory gene expression boundaries demarcate sites of neuronal differentiation in the embryonic zebrafish forebrain , 1994, Neuron.

[2]  Y. Hatada,et al.  A fate map of the epiblast of the early chick embryo. , 1994, Development.

[3]  W. Driever,et al.  Microtubule arrays of the zebrafish yolk cell: organization and function during epiboly. , 1994, Development.

[4]  W. Driever,et al.  Implications for dorsoventral axis determination from the zebrafish mutation janus , 1994, Nature.

[5]  D. Grunwald,et al.  Contribution of early cells to the fate map of the zebrafish gastrula. , 1994, Science.

[6]  G. Heinrich,et al.  The fates of the blastomeres of the 16-cell zebrafish embryo. , 1994, Development.

[7]  D. V. Essen,et al.  Neural mechanisms of form and motion processing in the primate visual system , 1994, Neuron.

[8]  M. Westerfield,et al.  Combinatorial expression of three zebrafish genes related to distal- less: part of a homeobox gene code for the head , 1994, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[9]  C. Nüsslein-Volhard,et al.  no tail (ntl) is the zebrafish homologue of the mouse T (Brachyury) gene. , 1994, Development.

[10]  C. Kimmel,et al.  Segment and cell type lineage restrictions during pharyngeal arch development in the zebrafish embryo. , 1994, Development.

[11]  D. Raible,et al.  Restriction of neural crest cell fate in the trunk of the embryonic zebrafish. , 1994, Development.

[12]  C. Kimmel,et al.  Cell cycles and clonal strings during formation of the zebrafish central nervous system. , 1994, Development.

[13]  P. Ingham,et al.  A functionally conserved homolog of the Drosophila segment polarity gene hh is expressed in tissues with polarizing activity in zebrafish embryos , 1993, Cell.

[14]  J. Postlethwait,et al.  Structure of the zebrafish snail1 gene and its expression in wild-type, spadetail and no tail mutant embryos. , 1993, Development.

[15]  U. Strähle,et al.  Ultraviolet irradiation impairs epiboly in zebrafish embryos: evidence for a microtubule-dependent mechanism of epiboly. , 1993, Development.

[16]  R. Ho,et al.  Induction of muscle pioneers and floor plate is distinguished by the zebrafish no tail mutation , 1993, Cell.

[17]  D. Grunwald,et al.  Something's fishy here--rethinking cell movements and cell fate in the zebrafish embryo. , 1993, Trends in genetics : TIG.

[18]  C. Kimmel,et al.  The zebrafish midblastula transition. , 1993, Development.

[19]  M. Fishman,et al.  Cardiovascular development in the zebrafish. I. Myocardial fate map and heart tube formation. , 1993, Development.

[20]  R. Ho,et al.  Commitment of cell fate in the early zebrafish embryo. , 1993, Science.

[21]  D. Grunwald,et al.  Lithium perturbation and goosecoid expression identify a dorsal specification pathway in the pregastrula zebrafish. , 1993, Development.

[22]  E. Oxtoby,et al.  Cloning of the zebrafish krox-20 gene (krx-20) and its expression during hindbrain development. , 1993, Nucleic acids research.

[23]  W. Gilbert,et al.  A fate map for the first cleavages of the zebrafish , 1993, Nature.

[24]  T. Horder,et al.  The segmental Bauplan of the rostral zone of the head in vertebrates. , 1993, Functional and developmental morphology.

[25]  C. Kimmel,et al.  Patterning the brain of the zebrafish embryo. , 1993, Annual review of neuroscience.

[26]  C. Kimmel,et al.  Mitotic domains in the early embryo of the zebrafish , 1992, Nature.

[27]  J. Trinkaus Some Students' Perceptions about Aids: An Informal Look , 1992, Perceptual and motor skills.

[28]  R. Ho,et al.  The protein product of the zebrafish homologue of the mouse T gene is expressed in nuclei of the germ ring and the notochord of the early embryo. , 1992, Development.

[29]  M. Westerfield,et al.  Coordinate embryonic expression of three zebrafish engrailed genes. , 1992, Development.

[30]  D. Raible,et al.  Segregation and early dispersal of neural crest cells in the embryonic zebrafish , 1992, Developmental dynamics : an official publication of the American Association of Anatomists.

[31]  R. Ho Cell movements and cell fate during zebrafish gastrulation. , 1992, Development (Cambridge, England). Supplement.

[32]  J. Trinkaus,et al.  The midblastula transition, the YSL transition and the onset of gastrulation in Fundulus. , 1992, Development (Cambridge, England). Supplement.

[33]  C. Kimmel,et al.  The fub-1 mutation blocks initial myofibril formation in zebrafish muscle pioneer cells. , 1991, Developmental biology.

[34]  R. Pedersen,et al.  Clonal analysis of epiblast fate during germ layer formation in the mouse embryo. , 1991, Development.

[35]  Terje Johansen,et al.  Expression pattern of zebrafish pax genes suggests a role in early brain regionalization , 1991, Nature.

[36]  M. Westerfield,et al.  Diversity of expression of engrailed-like antigens in zebrafish. , 1991, Development.

[37]  Stephen W. Wilson,et al.  Stereotyped pathway selection by growth cones of early epiphysial neurons in the embryonic zebrafish. , 1991, Development.

[38]  J. Eisen Determination of primary motoneuron identity in developing zebrafish embryos. , 1991, Science.

[39]  R. Ho,et al.  The cyclops mutation blocks specification of the floor plate of the zebrafish central nervous system , 1991, Nature.

[40]  J. Gerhart Cell-cell interactions in early development , 1991 .

[41]  J. Y. Kuwada,et al.  Identification of spinal neurons in the embryonic and larval zebrafish , 1990, The Journal of comparative neurology.

[42]  W. K. Metcalfe,et al.  Primary neurons that express the L2/HNK-1 carbohydrate during early development in the zebrafish. , 1990, Development.

[43]  A. Chitnis,et al.  Axonogenesis in the brain of zebrafish embryos , 1990, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[44]  C. Kimmel,et al.  Organization of hindbrain segments in the zebrafish embryo , 1990, Neuron.

[45]  W. K. Metcalfe,et al.  Early axonal contacts during development of an identified dendrite in the brain of the zebrafish , 1990, Neuron.

[46]  C. Kimmel,et al.  Origin and organization of the zebrafish fate map. , 1990, Development.

[47]  C. Kimmel,et al.  Cell movements during epiboly and gastrulation in zebrafish. , 1990, Development.

[48]  S. Pike,et al.  An identified motoneuron with variable fates in embryonic zebrafish , 1990, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[49]  Stephen W. Wilson,et al.  The development of a simple scaffold of axon tracts in the brain of the embryonic zebrafish, Brachydanio rerio. , 1990, Development.

[50]  M. Westerfield,et al.  Early expression of acetylcholinesterase activity in functionally distinct neurons of the zebrafish , 1989, The Journal of comparative neurology.

[51]  P. Tibbetts,et al.  Mediolateral cell intercalation in the dorsal, axial mesoderm of Xenopus laevis. , 1989, Developmental biology.

[52]  C. Kimmel,et al.  A mutation that changes cell movement and cell fate in the zebrafish embryo , 1989, Nature.

[53]  M. Westerfield,et al.  Segmental pattern of development of the hindbrain and spinal cord of the zebrafish embryo. , 1988, Development.

[54]  A. Wood,et al.  Teleost epibolie: a reassesment of deep cell movement in the germ ring. , 1988 .

[55]  M. Westerfield,et al.  A neural degeneration mutation that spares primary neurons in the zebrafish. , 1988, Developmental biology.

[56]  C. Kimmel,et al.  Indeterminate cell lineage of the zebrafish embryo. , 1987, Developmental biology.

[57]  M. Martindale,et al.  Mesodermal metamerism in the teleost, oryzias latipes (the medaka) , 1987, Journal of morphology.

[58]  J M Slack,et al.  Fate map for the 32-cell stage of Xenopus laevis. , 1987, Development.

[59]  B. Mendelson Development of reticulospinal neurons of the zebrafish. I. Time of origin , 1986, The Journal of comparative neurology.

[60]  M. Westerfield,et al.  Development and axonal outgrowth of identified motoneurons in the zebrafish , 1986, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[61]  M. Westerfield,et al.  Pathway selection by growth cones of identified motoneurones in live zebra fish embryos , 1986, Nature.

[62]  W. K. Metcalfe Sensory neuron growth cones comigrate with posterior lateral line primordial cells in zebrafish , 1985, The Journal of comparative neurology.

[63]  C. Kimmel,et al.  Cell lineage of zebrafish blastomeres: II. Formation of the yolk syncytial layer , 1985 .

[64]  C. Kimmel,et al.  Cell lineage of zebrafish blastomeres. I. Cleavage pattern and cytoplasmic bridges between cells. , 1985, Developmental biology.

[65]  J. Trinkaus Mechanism of Fundulus Epiboly—A Current View , 1984 .

[66]  R. Ho,et al.  Muscle pioneers: large mesodermal cells that erect a scaffold for developing muscles and motoneurones in grasshopper embryos , 1983, Nature.

[67]  M. Kirschner,et al.  A major developmental transition in early xenopus embryos: I. characterization and timing of cellular changes at the midblastula stage , 1982, Cell.

[68]  M. Kirschner,et al.  A major developmental transition in early xenopus embryos: II. control of the onset of transcription , 1982, Cell.

[69]  G. Streisinger,et al.  Production of clones of homozygous diploid zebra fish (Brachydanio rerio) , 1981, Nature.

[70]  W. W. Ballard Morphogenetic Movements and Fate Maps of Vertebrates , 1981 .

[71]  R. Keller,et al.  The cellular basis of epiboly: an SEM study of deep-cell rearrangement during gastrulation in Xenopus laevis. , 1980, Journal of embryology and experimental morphology.

[72]  W. W. Ballard,et al.  Morphogenetic movements in acipenserid embryos , 1980 .

[73]  J. Trinkaus,et al.  Contact relations, surface activity, and cortical microfilaments of marginal cells of the enveloping layer and of the yolk syncytial and yolk cytoplasmic layers of fundulus before and during epiboly. , 1978, The Journal of experimental zoology.

[74]  A. D. Dingle,et al.  Dynamics of pigment pattern formation in the zebrafish, Brachydanio rerio. I. Establishment and regulation of the lateral line melanophore stripe during the first eight days of development , 1978 .

[75]  J. Dumont,et al.  Kupffer's vesicle in Fundulus heteroclitus: a scanning and transmission electron microscope study. , 1978, Tissue & cell.

[76]  S. Gould,et al.  Ontogeny and Phylogeny , 1978 .

[77]  R. Keller,et al.  Vital dye mapping of the gastrula and neurula of Xenopus laevis: I. Prospective areas and morphogenetic movements of the superficial layer , 1976 .

[78]  R. Keller,et al.  Vital Dye Mapping of the Gastrula and Neurula of Xenopus Laevis , 1975 .

[79]  W. W. Ballard Morphogenetic movements in Salmo gairdneri Richardson , 1973 .

[80]  M. Bennett,et al.  ELECTRICAL COUPLING BETWEEN EMBRYONIC CELLS BY WAY OF EXTRACELLULAR SPACE AND SPECIALIZED JUNCTIONS , 1970, The Journal of cell biology.

[81]  Robert C. Schirone,et al.  Effect of temperature on early embryological development of the zebra fish, Brachydanio rerio† , 1968 .

[82]  C. Firlit,et al.  Further studies on the embryonic development of the zebrafish, Brachydanio rerio (Hamilton‐Buchanan) , 1960 .

[83]  K. K. Hisaoka,et al.  The normal developmental stages of the zebrafish, brachydanio rerio (hamilton‐buchanan) , 1958 .