Nodal signalling determines biradial asymmetry in Hydra

Abstract

In bilaterians, three orthogonal body axes define the animal form, with distinct anterior-posterior, dorsal-ventral and left-right asymmetries. The key signalling factors are Wnt family proteins for the anterior-posterior axis, Bmp family proteins for the dorsal-ventral axis and Nodal for the left-right axis. Cnidarians, the sister group to bilaterians, are characterized by one oral-aboral body axis, which exhibits a distinct biradiality of unknown molecular nature. Here we analysed the biradial growth pattern in the radially symmetrical cnidarian polyp Hydra, and we report evidence of Nodal in a pre-bilaterian clade. We identified a Nodal-related gene (Ndr) in Hydra magnipapillata, and this gene is essential for setting up an axial asymmetry along the main body axis. This asymmetry defines a lateral signalling centre, inducing a new body axis of a budding polyp orthogonal to the mother polyp's axis. Ndr is expressed exclusively in the lateral bud anlage and induces Pitx, which encodes an evolutionarily conserved transcription factor that functions downstream of Nodal. Reminiscent of its function in vertebrates, Nodal acts downstream of β-Catenin signalling. Our data support an evolutionary scenario in which a 'core-signalling cassette' consisting of β-Catenin, Nodal and Pitx pre-dated the cnidarian-bilaterian split. We presume that this cassette was co-opted for various modes of axial patterning: for example, for lateral branching in cnidarians and left-right patterning in bilaterians.

Ediacaran developmental biology

“…The rangeomorphs appear to have one main body axis and one lateral branching axis, an arrangement very similar to various cnidarian organisms (Watanabe et al ., 2014), with which they also share developmental similarities, i.e. a conserved form and potential positioning of the generative zone.…”

When and Why Did Brains Break Symmetry?

“…Nodal also has a role during later embryogenesis of sea urchins, where it breaks symmetry even though adult sea urchins are radially-symmetrical [40]. In fact, recent research by Watanabe et al [41] has shown that a Nodal-related gene has a role in determining a structural axis in the radially-symmetrical Cnidarian, Hydra: it establishes a body axis for a new bud distinct from that of the parent. Given these roles of Nodal in the development of structural asymmetry [42], asymmetry in invertebrates and vertebrates may have at least some homologous aspects.…”

Reconsidering regeneration in metazoans: an evo-devo approach

“…Wnt, BMP and Nodal represent the signaling pathways defining the body axes during embryonic development, at least in bilaterians. These pathways were possibly present in the most recent common ancestor of all metazoans (reviewed in Holstein et al, 2011) and their involvement in whole body or body structure re-patterning has been reported in cnidarians, acoel, platyhelminthes, and deuterostomes (Holstein et al, 2003;Yakushiji et al, 2009;Adell et al, 2010;Reddien, 2011;Srivastava et al, 2014;Watanabe et al, 2014).…”