Nodal and planar cell polarity signaling cooperate to regulate zebrafish convergence and extension gastrulation movements.

Margot Lk Williams,Lilianna Solnica-Krezel

doi:10.7554/elife.54445

Abstract

During vertebrate gastrulation, convergence and extension (C and E) of the primary anteroposterior (AP) embryonic axis is driven by polarized mediolateral (ML) cell intercalations and is influenced by AP axial patterning. Nodal signaling is essential for patterning of the AP axis while planar cell polarity (PCP) signaling polarizes cells with respect to this axis, but how these two signaling systems interact during C and E is unclear. We find that the neuroectoderm of Nodal-deficient zebrafish gastrulae exhibits reduced C and E cell behaviors, which require Nodal signaling in both cell- and non-autonomous fashions. PCP signaling is partially active in Nodal-deficient embryos and its inhibition exacerbates their C and E defects. Within otherwise naïve zebrafish blastoderm explants, however, Nodal induces C and E in a largely PCP-dependent manner, arguing that Nodal acts both upstream of and in parallel with PCP during gastrulation to regulate embryonic axis extension cooperatively.

Highlights

The embryonic body plan first emerges during gastrulation, when the three primordial germ layers — ectoderm, mesoderm, and endoderm — are formed and shaped, and embryonic axes are morphologically manifest
Ninomiya et al, 2004 reported that Xenopus gastrula explants with different AP positional values extend when apposed ex vivo, whereas those with the same positional identity do not. These positional values could be recapitulated in explants by different doses of the TGFb ligand Activin (Ninomiya et al, 2004), which signals largely via the Nodal signaling pathway during early vertebrate embryogenesis (Pauklin and Vallier, 2015). These results demonstrate that AP patterning is required for axial extension ex vivo and implies a crucial role for Nodal signaling at this intersection of tissue patterning and morphogenesis in vivo
These cells moved along swirling paths, which contrasted with the direct anterior, posterior, and medial-ward movement of WT cells, and were seen to cross the dorsal midline, which was not observed in WT embryos (Figure 1B; Concha and Adams, 1998)

Summary

Introduction

The embryonic body plan first emerges during gastrulation, when the three primordial germ layers — ectoderm, mesoderm, and endoderm — are formed and shaped, and embryonic axes are morphologically manifest. These positional values could be recapitulated in explants by different doses of the TGFb ligand Activin (Ninomiya et al, 2004), which signals largely via the Nodal signaling pathway during early vertebrate embryogenesis (Pauklin and Vallier, 2015) These results demonstrate that AP patterning is required for axial extension ex vivo and implies a crucial role for Nodal signaling at this intersection of tissue patterning and morphogenesis in vivo. Treatment of explants with a Nodal inhibitor revealed a continuous requirement for Nodal signaling in ex vivo extension after mesoderm was specified and even in the absence of mesoderm, implying a primary, mesoderm-independent role for Nodal in C and E Together, these data support a model in which Nodal signaling promotes ML cell polarity and C and E, both upstream and independent of PCP signaling, and predicts additional AP patterning mechanisms that instruct the PCP compass during vertebrate gastrulation

Results

Discussion

Materials and methods

Funding Funder National Institutes of Health