Editorial: MorphoEvoDevo: a multilevel approach to elucidate the evolution of metazoan organ systems

Editorial on the Research Topic MorphoEvoDevo: a multilevel approach to elucidate the evolution of metazoan organ systems

Expression of the pair-rule gene homologs runt, Pax3/7, even-skipped-1 and even-skipped-2 during larval and juvenile development of the polychaete annelid Capitella teleta does not support a role in segmentation

<p>Abstract</p> <p>Background</p> <p>Annelids and arthropods each possess a segmented body. Whether this similarity represents an evolutionary convergence or inheritance from a common segmented ancestor is the subject of ongoing investigation.</p> <p>Methods</p> <p>To investigate whether annelids and arthropods share molecular components that control segmentation, we isolated orthologs of the <it>Drosophila melanogaster </it>pair-rule genes, <it>runt</it>, <it>paired </it>(<it>Pax3/7</it>) and <it>eve</it>, from the polychaete annelid <it>Capitella teleta </it>and used whole mount <it>in situ </it>hybridization to characterize their expression patterns.</p> <p>Results</p> <p>When segments first appear, expression of the single <it>C. teleta runt </it>ortholog is only detected in the brain. Later, <it>Ct-runt </it>is expressed in the ventral nerve cord, foregut and hindgut. Analysis of <it>Pax </it>genes in the <it>C. teleta </it>genome reveals the presence of a single <it>Pax3/7 </it>ortholog. <it>Ct-Pax3/7 </it>is initially detected in the mid-body prior to segmentation, but is restricted to two longitudinal bands in the ventral ectoderm. Each of the two <it>C. teleta eve </it>orthologs has a unique and complex expression pattern, although there is partial overlap in several tissues. Prior to and during segment formation, <it>Ct-eve1 </it>and <it>Ct-eve2 </it>are both expressed in the bilaterial pair of mesoteloblasts, while <it>Ct-eve1 </it>is expressed in the descendant mesodermal band cells. At later stages, <it>Ct-eve2 </it>is expressed in the central and peripheral nervous system, and in mesoderm along the dorsal midline. In late stage larvae and adults, <it>Ct-eve1 </it>and <it>Ct-eve2 </it>are expressed in the posterior growth zone.</p> <p>Conclusions</p> <p><it>C. teleta eve, Pax3/7 </it>and <it>runt </it>homologs all have distinct expression patterns and share expression domains with homologs from other bilaterians. None of the pair-rule orthologs examined in <it>C. teleta </it>exhibit segmental or pair-rule stripes of expression in the ectoderm or mesoderm, consistent with an independent origin of segmentation between annelids and arthropods.</p

A comprehensive fate map by intracellular injection of identified blastomeres in the marine polychaete Capitella teleta

<p>Abstract</p> <p>Background</p> <p>The polychaete annelid <it>Capitella teleta </it>(formerly <it>Capitella </it>sp. I) develops by spiral cleavage and has been the focus of several recent developmental studies aided by a fully sequenced genome. Fate mapping in polychaetes has lagged behind other spiralian taxa, because of technical limitations.</p> <p>Results</p> <p>To generate a modern fate map for <it>C. teleta</it>, we injected 1,1'-dioctadecyl-3,3,3'3'-tetramethylindocarbocyanine perchlorate (DiI) into individual identified blastomeres through fourth-quartet micromere formation. Confocal laser scanning microscopy at single-cell resolution was used to characterize blastomere fates during larval stages. Our results corroborate previous observations from classic studies, and show a number of similarities with other spiralian fate maps, including unique and stereotypic fates for individual blastomeres, presence of four discrete body domains arising from the A, B, C and D cell quadrants, generation of anterior ectoderm from first quartet micromeres, and contributions to trunk ectoderm and ventral nerve cord by the 2d somatoblast. Of particular interest are several instances in which the <it>C. teleta </it>fate map deviates from other spiralian fate maps. For example, we identified four to seven distinct origins of mesoderm, all ectomesodermal. In addition, the left and right mesodermal bands arise from 3d and 3c, respectively, whereas 4d generates a small number of trunk muscle cells, the primordial germ cells and the anus. We identified a complex set of blastomere contributions to the posterior gut in <it>C. teleta</it>, which establishes the most complete map of posterior gut territories to date.</p> <p>Conclusions</p> <p>Our detailed cellular descriptions reveal previously underappreciated complexity in the ontogenetic contributions to several spiralian larval tissues, including the mesoderm, nervous system and gut. The formation of the mesodermal bands by 3c and 3d is in stark contrast to other spiralians, in which 4d generates the mesodermal bands. The results of this study provide a framework for future phylogenetic comparisons and functional analyses of cell-fate specification.</p

Expression and phylogenetic analysis of the zic gene family in the evolution and development of metazoans

<p>Abstract</p> <p>Background</p> <p><it>zic </it>genes are members of the <it>gli/glis/nkl/zic </it>super-family of C2H2 zinc finger (ZF) transcription factors. Homologs of the <it>zic </it>family have been implicated in patterning neural and mesodermal tissues in bilaterians. Prior to this study, the origin of the metazoan <it>zic </it>gene family was unknown and expression of <it>zic </it>gene homologs during the development of early branching metazoans had not been investigated.</p> <p>Results</p> <p>Phylogenetic analyses of novel <it>zic </it>candidate genes identified a definitive <it>zic </it>homolog in the placozoan <it>Trichoplax adhaerens</it>, two <it>gli/glis/nkl-</it>like genes in the ctenophore <it>Mnemiopsis leidyi</it>, confirmed the presence of three <it>gli/glis/nkl</it>-like genes in Porifera, and confirmed the five previously identified <it>zic </it>genes in the cnidarian <it>Nematostella vectensis</it>. In the cnidarian <it>N. vectensis</it>, <it>zic </it>homologs are expressed in ectoderm and the gastrodermis (a bifunctional endomesoderm), in presumptive and developing tentacles, and in oral and sensory apical tuft ectoderm. The <it>Capitella teleta zic </it>homolog (<it>Ct-zic</it>) is detectable in a subset of the developing nervous system, the foregut, and the mesoderm associated with the segmentally repeated chaetae. Lastly, expression of <it>gli </it>and <it>glis </it>homologs in <it>Mnemiopsis</it>. <it>leidyi </it>is detected exclusively in neural cells in floor of the apical organ.</p> <p>Conclusions</p> <p>Based on our analyses, we propose that the <it>zic </it>gene family arose in the common ancestor of the Placozoa, Cnidaria and Bilateria from a <it>gli/glis/nkl</it>-like gene and that both ZOC and ZF-NC domains evolved prior to cnidarian-bilaterian divergence. We also conclude that <it>zic </it>expression in neural ectoderm and developing neurons is pervasive throughout the Metazoa and likely evolved from neural expression of an ancestral <it>gli/glis/nkl/zic </it>gene. <it>zic </it>expression in bilaterian mesoderm may be related to the expression in the gastrodermis of a cnidarian-bilaterian common ancestor.</p

Threshold-Dependent BMP-Mediated Repression: A Model for a Conserved Mechanism That Patterns the Neuroectoderm

Subdivision of the neuroectoderm into three rows of cells along the dorsal-ventral axis by neural identity genes is a highly conserved developmental process. While neural identity genes are expressed in remarkably similar patterns in vertebrates and invertebrates, previous work suggests that these patterns may be regulated by distinct upstream genetic pathways. Here we ask whether a potential conserved source of positional information provided by the BMP signaling contributes to patterning the neuroectoderm. We have addressed this question in two ways: First, we asked whether BMPs can act as bona fide morphogens to pattern the Drosophila neuroectoderm in a dose-dependent fashion, and second, we examined whether BMPs might act in a similar fashion in patterning the vertebrate neuroectoderm. In this study, we show that graded BMP signaling participates in organizing the neural axis in Drosophila by repressing expression of neural identity genes in a threshold-dependent fashion. We also provide evidence for a similar organizing activity of BMP signaling in chick neural plate explants, which may operate by the same double negative mechanism that acts earlier during neural induction. We propose that BMPs played an ancestral role in patterning the metazoan neuroectoderm by threshold-dependent repression of neural identity genes

Developmental expression of COE across the Metazoa supports a conserved role in neuronal cell-type specification and mesodermal development

The transcription factor COE (collier/olfactory-1/early B cell factor) is an unusual basic helix–loop–helix transcription factor as it lacks a basic domain and is maintained as a single copy gene in the genomes of all currently analysed non-vertebrate Metazoan genomes. Given the unique features of the COE gene, its proposed ancestral role in the specification of chemosensory neurons and the wealth of functional data from vertebrates and Drosophila, the evolutionary history of the COE gene can be readily investigated. We have examined the ways in which COE expression has diversified among the Metazoa by analysing its expression from representatives of four disparate invertebrate phyla: Ctenophora (Mnemiopsis leidyi); Mollusca (Haliotis asinina); Annelida (Capitella teleta and Chaetopterus) and Echinodermata (Strongylocentrotus purpuratus). In addition, we have studied COE function with knockdown experiments in S. purpuratus, which indicate that COE is likely to be involved in repressing serotonergic cell fate in the apical ganglion of dipleurula larvae. These analyses suggest that COE has played an important role in the evolution of ectodermally derived tissues (likely primarily nervous tissues) and mesodermally derived tissues. Our results provide a broad evolutionary foundation from which further studies aimed at the functional characterisation and evolution of COE can be investigated