Abstract

Gastrulation is a key event in animal embryogenesis during which germ layer precursors are rearranged and the embryonic axes are established. Cell polarization is essential during gastrulation, driving asymmetric cell division, cell movements, and cell shape changes. The furry (fry) gene encodes an evolutionarily conserved protein with a wide variety of cellular functions, including cell polarization and morphogenesis in invertebrates. However, little is known about its function in vertebrate development. Here, we show that in Xenopus, Fry plays a role in morphogenetic processes during gastrulation, in addition to its previously described function in the regulation of dorsal mesoderm gene expression. Using morpholino knock-down, we demonstrate a distinct role for Fry in blastopore closure and dorsal axis elongation. Loss of Fry function drastically affects the movement and morphological polarization of cells during gastrulation and disrupts dorsal mesoderm convergent extension, responsible for head-to-tail elongation. Finally, we evaluate a functional interaction between Fry and NDR1 kinase, providing evidence of an evolutionarily conserved complex required for morphogenesis.

Highlights

  • Gastrulation is a key event in animal embryogenesis during which germ layer precursors are rearranged and the embryonic axes are established

  • Since we were not able to detect the endogenous protein with available antibodies, we investigated Fry cellular localization in dorsal marginal zone (DMZ) explants from fry-GFP mRNA injected embryos at a dose that did not cause an axis phenotype

  • We found that Fry loss-of-function consistently affects the movements and spatial configuration of the superficial and deep involuting marginal zone (IMZ) cells

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Summary

Introduction

Gastrulation is a key event in animal embryogenesis during which germ layer precursors are rearranged and the embryonic axes are established. The furry (fry) gene encodes an evolutionarily conserved protein with a wide variety of cellular functions, including cell polarization and morphogenesis in invertebrates. We show that in Xenopus, Fry plays a role in morphogenetic processes during gastrulation, in addition to its previously described function in the regulation of dorsal mesoderm gene expression. Loss of Fry function drastically affects the movement and morphological polarization of cells during gastrulation and disrupts dorsal mesoderm convergent extension, responsible for head-to-tail elongation. In fission and budding yeasts, the phenotypes associated with loss-of-function mutants of Fry orthologs, including Drosophila Fry, C. elegans Sax[2], S. pombe Mor2p and S. cerevisiae Tao3p, implicate this protein in the control of cell division, transcriptional asymmetry, cell polarization, and ­morphogenesis[13,14,15,16,17,18,19,20]. Neither the function of Xenopus ortholog of NDR1 nor its physical and functional interaction with Fry have been investigated

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