No tail co-operates with non-canonical Wnt signaling to regulate posterior body morphogenesis in zebrafish.
The vertebrate posterior body is formed by a combination of the gastrulation movements that shape the head and anterior trunk and posterior specific cell behaviors. Here, we investigated whether genes that regulate cell movements during gastrulation [no tail (ntl)/brachyury, knypek (kny) and pipetail (ppt)/wnt5] interact to regulate posterior body morphogenesis. Both kny;ntl and ppt;ntl double mutant embryos exhibit synergistic trunk and tail shortening by early segmentation. Gene expression analysis in the compound mutants indicates that anteroposterior germ-layer patterning is largely normal and that the tail elongation defects are not due to failure to specify or maintain posterior tissues. Moreover, ntl interacts with ppt and kny to synergistically regulate the posterior expression of the gene encoding bone morphogenetic protein 4 (bmp4) but not of other known T-box genes, fibroblast growth factor genes or caudal genes. Examination of mitotic and apoptotic cells indicates that impaired tail elongation is not simply due to decreased cell proliferation or increased cell death. Cell tracing in ppt;ntl and kny;ntl mutants demonstrates that the ventral derived posterior tailbud progenitors move into the tailbud. However, gastrulation-like convergence and extension movements and cell movements within the posterior tailbud are impaired. Furthermore, subduction movements of cells into the mesendoderm are reduced in kny;ntl and ppt;ntl mutants. We propose that Ntl and the non-canonical Wnt pathway components Ppt and Kny function in parallel, partially redundant pathways to regulate posterior body development. Our work initiates the genetic dissection of posterior body morphogenesis and links genes to specific tail-forming movements. Moreover, we provide genetic evidence for the notion that tail development entails a continuation of mechanisms regulating gastrulation together with mechanisms unique to the posterior body.
Marlow
Florence
F
Department of Biological Sciences, Vanderbilt University, Nashville, TN 37235, USA.
Gonzalez
Encina M
EM
Yin
Chunyue
C
Rojo
Concepcion
C
Solnica-Krezel
Lilianna
L
D000818:Animals; D019521:Body Patterning / Q000502:physiology; D004625:Embryo, Nonmammalian / Q000502:physiology*; D005775:Gastrula / Q000502:physiology*; D018507:Gene Expression Regulation, Developmental / Q000235:genetics*; D005838:Genotype; D009024:Morphogenesis / Q000502:physiology*; D009068:Movement / Q000502:physiology; D009154:Mutation; D010641:Phenotype; D011518:Proto-Oncogene Proteins / Q000502:physiology*; D015398:Signal Transduction; D013623:Tail / Q000002:abnormalities / Q000196:embryology*; D051153:Wnt Proteins; D015027:Zebrafish / Q000196:embryology* / Q000235:genetics; D029961:Zebrafish Proteins
D011518:Proto-Oncogene Proteins; D051153:Wnt Proteins; D029961:Zebrafish Proteins; C094522:wnt8b protein, zebrafish