Polychaete trunk neuroectoderm converges and extends by mediolateral cell intercalation

Abstract

During frog and fish development, convergent extension movements transform the spherical gastrula into an elongated neurula. Such transformation of a ball-into a worm-shaped embryo is an ancestral and fundamental feature of bilaterian development, yet this is modified or absent in the protostome model organisms Caenorhabditis or Drosophila. In the polychaete annelid Platynereis dumerilii, early embryonic and larval stages resemble a sphere that subsequently elongates into worm shape. Cellular and molecular mechanisms of polychaete body elongation are yet unknown. Our in vivo time-lapse analysis of Platynereis axis elongation reveals that the polychaete neuroectoderm converges and extends by mediolateral cell intercalation. This occurs on both sides of the neural midline, the line of fusion of the slit-like blastopore. Convergent extension moves apart mouth and anus that are both derived from the blastopore. Tissue elongation is actin-dependent but microtubule-independent. Dependence on JNK activity and spatially restricted expression of strabismus indicates involvement of the noncanonical Wnt pathway. We detect a morphogenetic boundary between the converging and extending trunk neuroectoderm and the anterior otx-expressing head neuroectoderm that does not elongate. Our comparative analysis uncovers striking similarities but also differences between convergent extension in the polychaete and in the frog (the classical vertebrate model for convergent extension). Based on these findings, we propose that convergent extension movements of the trunk neuroectoderm represent an ancestral feature of bilaterian development that triggered the separation of mouth and anus along the elongating trunk.amphistomy ͉ axis formation ͉ convergent extension ͉ gastrulation

Acoel development supports a simple planula-like urbilaterian

“…Together these studies supported the notion of a molecular 'zootype' defining a common plan for the construction of all animals (Slack et al 1993). The extension of gene expression studies to members of the third 'superclade', the Lophotrochozoa, primarily members of the Annelida, appears to confirm the notion of a morphologically complex urbilaterian (Shankland & Bruce 1998;Arendt et al 2001Arendt et al , 2002Prud'homme et al 2003;Seaver et al 2005;Frö bius & Seaver 2006;Seaver & Kaneshige 2006;Denes et al 2007;Steinmetz et al 2007). This rather complex bilaterian ancestor would have possessed serially reiterated body segments, a mesodermally lined coelomic space, a through gut with separate mouth and anus, lateral appendages, heart, eyes, epigenetic germ-cell determination (Extavour & Akam 2003;Rebscher et al 2007), a tripartite brain with a centralized nervous system and a biphasic life cycle with a feeding larvae (Arendt et al 2001;Carroll et al 2001;see figure 2).…”

Ins and outs of Spiralian gastrulation

“…5C), suggesting that this pathway could play a role in the anterior movement of the mouth; however, the expression pattern of brachyury in MAPK-inhibited embryos was not drastically different from that in controls (Koop et al, 2007). In Platynereis, homologs of Jnk pathway members are expressed in the ventral territory during elongation, and inhibiting Jnk signaling perturbed elongation (Steinmetz et al, 2007). Thus, the role of brachyury, MAPK and Jnk signaling in axial elongation should be explored further.…”

“…Careful examination in this diverse group might uncover novel mechanisms of gastrulation that can shed light on the evolution of morphogenesis. Since the techniques for live-imaging using conventional lineage tracers, membrane dyes, and fluorescentlytagged proteins already exist in several species (e.g., Steinmetz et al, 2007;Henry et al, 2010;Gline et al, 2011), we can expect to learn much more about spiralian gastrulation in the near future.…”

Wnt/β-Catenin and noncanonical Wnt signaling interact in tissue evagination in the simple eumetazoan Hydra

“…Such processes of in and evagination can be mediated by an interplay of movement, intercalation, and division of cells as well as by changes in cell polarization and shape (3,4). The molecular events underlying these cellular behaviors have been studied in a number of bilaterian model systems to some detail (5)(6)(7)(8). However, it is unknown how curvature is generated at the cellular and molecular level in more ancestral, prebilaterian animals.…”