Gene expression analysis reveals that Delta/Notch signalling is not involved in onychophoran segmentation

Abstract

Delta/Notch (Dl/N) signalling is involved in the gene regulatory network underlying the segmentation process in vertebrates and possibly also in annelids and arthropods, leading to the hypothesis that segmentation may have evolved in the last common ancestor of bilaterian animals. Because of seemingly contradicting results within the well-studied arthropods, however, the role and origin of Dl/N signalling in segmentation generally is still unclear. In this study, we investigate core components of Dl/N signalling by means of gene expression analysis in the onychophoran Euperipatoides kanangrensis, a close relative to the arthropods. We find that neither Delta or Notch nor any other investigated components of its signalling pathway are likely to be involved in segment addition in onychophorans. We instead suggest that Dl/N signalling may be involved in posterior elongation, another conserved function of these genes. We suggest further that the posterior elongation network, rather than classic Dl/N signalling, may be in the control of the highly conserved segment polarity gene network and the lower-level pair-rule gene network in onychophorans. Consequently, we believe that the pair-rule gene network and its interaction with Dl/N signalling may have evolved within the arthropod lineage and that Dl/N signalling has thus likely been recruited independently for segment addition in different phyla.Electronic supplementary materialThe online version of this article (doi:10.1007/s00427-016-0529-4) contains supplementary material, which is available to authorized users.

Untangling posterior growth and segmentation by analyzing mechanisms of axis elongation in hemichordates

“…Our data suggest that, similar to vertebrates, a Wnt-Brachyury feedback loop may regulate PAE, which would establish this key regulatory interaction as an ancestral feature of deuterostomes. We further show that Notch signaling interacts with Wnt/Brachyury during PAE of S. kowalevskii, supporting the idea that Notch signaling was an ancestral component of the bilaterian PAE network (7,10,22,23) and that the role of Notch in segmentation may have evolved later independently in different lineages. Alternatively, hemichordates may have secondarily lost segmentation, but ultimately it is only through broader phylogenetic sampling, representing a wider range of trunk morphologies,…”

“…To test whether posterior Notch signaling is also needed for posterior Wnt signaling in S. kowalevskii, as shown for some protostomes and vertebrates (6,7,10,22,23), we combined treatments of DAPT and 1-azakenpaullone ( Fig. 4E, gray bars) and compared them to individual treatments of DAPT (Fig.…”

“…Knockdown of Notch signaling in representatives of both lineages leads to strong posterior truncation that is due to either a failure to properly form the PAE network (6,7,10,22) or a failure of segmentation (4,6,9,10,13,22,23). However, since these two mechanisms are tightly coupled in segmented phyla, it is difficult to determine whether the ancestral role of posterior Notch signaling in bilaterians was in posterior growth and/or segmentation (4,5,23). Examining the role of Notch during PAE in unsegmented taxa like enteropneusts is essential for testing between these alternatives.…”

Embryonic expression of a Long Toll (Loto) gene in the onychophorans Euperipatoides kanangrensis and Cephalofovea clandestina

“…2 (a, b)), tissue that likely contributes to the brain (cf. expression of Notch , Delta and achaete-scute (Eriksson and Stollewerk 2010; Janssen and Budd 2016)). This latter expression is in the form of a salt and pepper pattern.…”

Dynamic Paleontology

“…Note that this hypothesis proposes that the virus can reconfigure the entire kernel; this is not just a modification of Hox or Ubx genes (Martin et al 2016) to alter limb structure nor Delta/Notch signaling to modify segmentation (Janssen and Budd 2016), but something much more profound. It then went extinct shortly after having caused the Cambrian Explosion.…”