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Cell Movements During Epiboly and Gastrulation in Zebrafish

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Cell Movements During Epiboly and Gastrulation in Zebrafish Development 108,569-580(1990) 569 Printed in Great Britain © The Company of Biologists Limited 1990 Cell movements during epiboly and gastrulation in zebrafish RACHEL M. WARGA and CHARLES B. KIMMEL Institute of Neuroscience, University of Oregon, Eugene OR 97403, USA Summary Beginning during the late blastula stage in zebrafish, neighbors before gastrulation. Involuting cells eventu- cells located beneath a surface epithelial layer of the ally form endoderm and mesoderm, in an anterior- blastoderm undergo rearrangements that accompany posterior sequence according to the time of involution. major changes in shape of the embryo. We describe The epiblast is equivalent to embryonic ectoderm. three distinctive kinds of cell rearrangements. (1) Radial (3) Mediolateral cell intercalations in both the epiblast cell intercalations during epiboly mix cells located deeply and hypoblast mediate convergence and extension move- in the blastoderm among more superficial ones. These ments towards the dorsal side of the gastrula. By this rearrangements thoroughly stir the positions of deep rearrangement, cells that were initially neighboring one cells, as the blastoderm thins and spreads across the yolk another become dispersed along the anterior-posterior cell. (2) Involution at or near the blastoderm margin axis of the embryo. Epiboly, involution and convergent occurs during gastrulation. This movement folds the extension in zebrafish involve the same kinds of cellular blastoderm into two cellular layers, the epiblast and rearrangements as in amphibians, and they occur dur- hypoblast, within a ring (the germ ring) around its entire ing comparable stages of embryogenesis. circumference. Involuting cells move anteriorwards in the hypoblast relative to cells that remain in the epiblast; Key words: blastula, gastrula, morphogenetic movements, the movement shears the positions of cells that were involution, clonal analysis, cell lineage. Introduction opposite direction: deep-lying blastoderm cells spread outward towards the margin to form the hypoblast. In the zebrafish embryo, after an early developmental Ballard's view has been generally accepted, but very period of rapid cleavages, morphogenetic movements recently, involution was observed directly in the small occur that rapidly produce major changes in the appear- embryo of a teleost, the rosy barb (Wood and Timmer- ance and organization of the blastoderm. During epi- mans, 1988). boly (Trinkaus, 1984a; 19846), beginning at the late During the course of cell-lineage analyses, we have blastula stage about 4h after fertilization, the blasto- followed cell movements during epiboly and gastru- derm thins and spreads to completely cover the yolk cell lation in zebrafish. We observed cell rearrangements during the course of 6h. Gastrulation begins about an that seemed nonsensical if considered only in terms of hour after epiboly is underway. The blastoderm, a the eventual fates that the lineages produced. First, in single multilayer of cells, rearranges into a two-layered the late blastula, cells scatter chaotically (Kimmel and structure consisting of a more superficial epiblast, and Law, 1985b; Kimmel and Warga, 1986). Second, in the an inner hypoblast (Wilson, 1891). Shortly after gastru- gastrula, neighboring cells at the blastoderm margin lation begins, the embryonic axis appears and lengthens undergo anterior-posterior inversions in their positions along one side of the embryo (the dorsal side), as cells (Kimmel and Warga, 1987a). Finally, cells in either accumulate and line up specifically at that location. The ectodermal (Kimmel and Warga, 1986) or mesodermal rearrangements that occur among the cells of the (Kimmel and Warga, 1987a) lineages disperse along the blastoderm during early morphogenesis, particularly anterior-posterior axis of the embryo. with respect to their lineal relationships and their future We now show that each of these cellular rearrange- fates, are not well understood. ments are understandable if they are considered in For example, several early embryologists concluded relation to the changes in form of the blastoderm that that during gastrulation the hypoblast originates by cell occur at the same time. Studies done mostly in Xenopus involution, a streaming of cells lying at the blastoderm suggest that cells undergo specific rearrangements to margin inward and underneath their neighbors (Wilson, mediate the changes in form (Keller, 1987). We find the 1891; Morgan, 1895; Pasteels, 1936). Later, Ballard same rearrangements occur in zebrafish at the compar- (I966a,b,c) concluded that the movement was in the able stages of development. 570 R. M. Warga and C. B. Kimmel Materials and methods was advanced through the intact EVL. It was technically more difficult to specifically inject single DEL cells than EVL cells, Embryos and stages even under visual control. As an aid, we monitored voltage through the injection pipette. We observed that successful Zebrafish embryos were obtained from natural spawnings and passage of the pipette through the EVL was accompanied by a staged by cell number during early cleavage. They were rise in voltage of up to 40 mV; the extracellular space dechorionated with watchmaker's forceps and kept at 28.5°C surrounding DEL cells is at a positive potential relative to the in an incubation medium of 14mM NaCl, 0.6mM KC1, 1.3mM bath (Bennett and Trinkaus, 1970). Upon intracellular pen- CaCl2, lmM MgSO4, and 0.07mM sodium-potassium phos- etration of a DEL cell, we then observed the expected shift to phate buffer (pH7.2). In some experiments, we used embryos negative potential, reflecting the membrane potential of the homozygous for the gol-1 (golden) mutation (Streisinger et al. cell. 1981), because they are lightly pigmented relative to the wild type, and fluorescently labeled cells in their bodies can be observed more clearly in whole-mount preparations after Observations of fluorescent cells in live embryos pigment cells differentiate. For short-term viewing of labeled cells, embryos were usually Developmental time usually was determined from the positioned as desired in a gel of 3 % methyl cellulose made in morphological features of the embryo, and Table 1 gives a the aqueous incubation medium described above and viewed staging series for the period of development of interest, from without a coverglass. Alternatively, embryos in incubation midblastula period until somites begin to form. We use the medium were sandwiched between two micro cover glasses letter h to mean hours after fertilization at 28.5°C. A that were spaced apart with three pairs of cover glasses (each previously published series, although less complete, includes 0.13-0.17mm thick). For longer term viewing and for time- useful sets of photographs (Hisaoka and Battle, 1958; lapse recordings, the embryos were held stationary in such Hisaoka and Firlit, 1960). In our series, names in common chambers in a gel of 0.1 % agarose made in the same medium, usage in embryology denote major periods of development and the chamber was then sealed with Vaseline to prevent (e.g. midblastula, gastrula), and the stages subdivide these evaporation. Observations were made using a Zeiss micro- periods. We name rather than number the stages, which scope with illumination from both a transmitted and an epi- seems to help one to remember them, and is more flexible. light source (Zeiss filter set 48-77-14), which permitted simultaneous imaging of labeled and unlabeled cells. The Blastomere injections fluorescent image was amplified with a Silicon-Intensified- Single blastomeres were injected (Kimmel and Law, 1985a), Target (SIT) video camera (Dage) to prevent light-induced in mid- and late blastula embryos with the lineage tracer dye damage to the labeled cells. In some experiments, the depths tetramethylrhodamine-isothiocyanate dextran (Molecular of fluorescent cells were determined with a digital shaft 3 encoder fitted to the fine-focus knob of the microscope. Probes, Eugene, OR; lOxlO Afr, diluted to 5 % (wt./vol.) in 0.2 M KC1). The second dye for double-label experiments was For time-lapse recordings, single-frame images were taken fluorescein-dextran (Sigma), dissolved the same way. Injec- with a Gyre video recorder at 4 s intervals. The epi-light tions were made by pressure, usually over the course of a few source was controlled by a shutter that illuminated the seconds, either into a cell in the surface enveloping layer embryo for only 60 ms during each exposure, in order to (EVL), or, in other cases, into a cell in the deep layer (DEL) minimize light-induced damage to the labeled cells. Frequent of the blastoderm. To inject a DEL cell, the injection pipette refocusing of the image was required during the recording Table 1. Series of normal stages for 3-10.5 h of development Stage h1 HBb Description 1 k-cell 3 10 Midblastula; yolk syncytial layer present; cell cycles of blastoderm cells fairly synchronous, determined by presence or absence of interphase nuclei 2k-cell 3.2 Single row of yolk syncytial layer nuclei; cell cycles of blastoderm cells highly asynchronous High 3.5 Blastoderm perched high upon the yolk cell, giving the embryo a dumbbell shape; yolk syncytial layer nuclei in two rows Oblong 3.7 11 Flattening of the blastoderm over the yolk cell produces a single smooth contoured outline, elongated along the animal-vegetal axis; multiple rows of yolk syncytial layer nuclei Sphere 12 Late blastula; embryo has assumed a spherical shape; at a deep plane of focus the yolk cell-blastoderm interface is flat Dome 4.3 13 Yolk cell bulging (doming) towards animal pole as blastoderm rapidly thins by epiboly 30%-epiboly 4.7 14 Blastoderm shaped as an inverted cup of uniform thickness and covers 30% of the yolk cell 50%-epiboly 5.2 Gastrula; 50% of the yolk cell is covered by the blastoderm Germ-ring 5.5 Germ ring visible from animal pole; 50%-epiboly Shield 6 15 Embryonic shield visible from animal pole, 50%-epiboly 75%-epiboly 8 16 The blastoderm continues to spread over the yolk cell at a rate of 15 %-epiboly per hour 100%-epiboly 9.5 17 Yolk plug closed.
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