Bmp activity gradient regulates convergent extension during zebrafish gastrulation.
During vertebrate gastrulation, a ventral to dorsal gradient of bone morphogenetic protein (Bmp) activity establishes cell fates. Concomitantly, convergent extension movements narrow germ layers mediolaterally while lengthening them anteroposteriorly. Here, by measuring movements of cell populations in vivo, we reveal the presence of three domains of convergent extension movements in zebrafish gastrula. Ventrally, convergence and extension movements are absent. Lateral cell populations converge and extend at increasing speed until they reach the dorsal domain where convergence speed slows but extension remains strong. Using dorsalized and ventralized mutants, we demonstrate that these domains are specified by the Bmp activity gradient. In vivo cell morphology and behavior analyses indicated that low levels of Bmp activity might promote extension with little convergence by allowing mediolateral cell elongation and dorsally biased intercalation. Further, single cell movement analyses revealed that the high ventral levels of Bmp activity promote epibolic migration of cells into the tailbud, increasing tail formation at the expense of head and trunk. We show that high Bmp activity limits convergence and extension by negatively regulating expression of the wnt11 (silberblick) and wnt5a (pipetail) genes, which are required for convergent extension but not cell fate specification. Therefore, during vertebrate gastrulation, a single gradient of Bmp activity, which specifies cell fates, also regulates the morphogenetic process of convergent extension.
Myers
Dina C
DC
Department of Biological Sciences, Vanderbilt University, VU Station B 351634, Nashville, Tennessee 37235-1634, USA.
Sepich
Diane S
DS
Solnica-Krezel
Lilianna
L
D000818:Animals; D019521:Body Patterning / Q000502:physiology*; D055419:Bone Morphogenetic Protein 7; D019485:Bone Morphogenetic Proteins / Q000502:physiology*; D002465:Cell Movement / Q000502:physiology; D004625:Embryo, Nonmammalian / Q000502:physiology; D005775:Gastrula / Q000502:physiology*; D018507:Gene Expression Regulation, Developmental / Q000502:physiology*; D016212:Transforming Growth Factor beta; D015027:Zebrafish / Q000196:embryology* / Q000502:physiology; D029961:Zebrafish Proteins
D055419:Bone Morphogenetic Protein 7; D019485:Bone Morphogenetic Proteins; D016212:Transforming Growth Factor beta; D029961:Zebrafish Proteins; C525826:bmp7a protein, zebrafish