Comparative transcriptomics in Syllidae (Annelida) indicates that posterior regeneration and regular growth are comparable, while anterior regeneration is a distinct process

Abstract

BackgroundAnnelids exhibit remarkable postembryonic developmental abilities. Most annelids grow during their whole life by adding segments through the action of a segment addition zone (SAZ) located in front of the pygidium. In addition, they show an outstanding ability to regenerate their bodies. Experimental evidence and field observations show that many annelids are able to regenerate their posterior bodies, while anterior regeneration is often limited or absent. Syllidae, for instance, usually show high abilities of posterior regeneration, although anterior regeneration varies across species. Some syllids are able to partially restore the anterior end, while others regenerate all lost anterior body after bisection. Here, we used comparative transcriptomics to detect changes in the gene expression profiles during anterior regeneration, posterior regeneration and regular growth of two syllid species: Sphaerosyllis hystrix and Syllis gracilis; which exhibit limited and complete anterior regeneration, respectively.ResultsWe detected a high number of genes with differential expression: 4771 genes in S. hystrix (limited anterior regeneration) and 1997 genes in S. gracilis (complete anterior regeneration). For both species, the comparative transcriptomic analysis showed that gene expression during posterior regeneration and regular growth was very similar, whereas anterior regeneration was characterized by up-regulation of several genes. Among the up-regulated genes, we identified putative homologs of regeneration-related genes associated to cellular proliferation, nervous system development, establishment of body axis, and stem-cellness; such as rup and JNK (in S. hystrix); and glutamine synthetase, elav, slit, Hox genes, β-catenin and PL10 (in S. gracilis).ConclusionsPosterior regeneration and regular growth show no significant differences in gene expression in the herein investigated syllids. However, anterior regeneration is associated with a clear change in terms of gene expression in both species. Our comparative transcriptomic analysis was able to detect differential expression of some regeneration-related genes, suggesting that syllids share some features of the regenerative mechanisms already known for other annelids and invertebrates.

A Comprehensive Ultrastructure and Transcriptome Analyses of Early Regeneration in Ophryotrocha Xiamen Sp. Nov. (Annelida: Dorvilleidae)

“…The regeneration process was a complex morphological change, while only 243 transcripts with signi cantly differing transcript levels were found in O. xiamen. This could be explained by ndings in other annelid that genes involved in the regeneration and normal growth process were largely overlapping and have been demonstrated to have similar expression patterns [31,33,34]. Among these, genes annotated as neurotrypsin, Nos2, DMBT1, SCO spondin, endotubin, 18S rRNA, and 28S rRNA were signi cantly up-regulated.…”

“…By using BLAST searches, we found regeneration-related or putative genes that have been implicated in regeneration in other regeneration models [43]. All these genes have been reported involving in regenerative processes, including wound healing, blastema formation, controlling cell proliferation and morphogenesis [31,33,44]. Among these potential candidate genes, only cyclin B was signi cantly differentially expressed.…”

“…Thus, the cyclin B in O. xiamen was suggested to have same functions in regulating the cell cycle during early regeneration. Meanwhile, other regeneration-related DEGs (fold change >2) including glutamine synthetase, brachyury, Hox A2, indian hedgehog, matrix metalloproteinase, myc, neurogenin, notch 1/2/4, and PRDM8/9, were already shown to be expressed during early regeneration stages in other annelids [31,33,48,49]. Genes, such as frizzled, notch, PRDM, and wnt, were represented by multiple isogroups, likely indicating multiple unique homologs in O. xiamen, which is consistent with what is known about these gene families in other annelids [11,44,50].…”

Atypical reproduction in a syllid worm: the stolon ofSyllis rosea(Annelida, Syllidae) takes care of its offspring

“…Although Syllidae are considered a rather promising group for developmental studies (Aguado et al ., 2015 b ), the majority of studies concentrated on molecular and physiological mechanisms underlying regeneration and asexual reproduction by fission (Weidhase et al ., 2016, 2017; Ribeiro et al ., 2018, 2019), stolonization (Weidhase et al ., 2016; Ponz-Segrelles et al ., 2018) and gemmiparity (Aguado et al ., 2015 a ; Álvarez-Campos et al ., 2018). Further phases of the sexual reproduction, and in particular larval development and dispersal, have been investigated only in a few species (see Table 1), despite the important contribution that this kind of data might give to the understanding of the evolutionary radiation of Syllidae (Aguado et al ., 2012).…”

On the Diversity of Phyllodocida (Annelida: Errantia), with a Focus on Glyceridae, Goniadidae, Nephtyidae, Polynoidae, Sphaerodoridae, Syllidae, and the Holoplanktonic Families

“…Accordingly, all hypotheses on the monophyly of the main groups within Syllidae (i.e., the five subfamilies and the main lineages within them) are highly congruent. This stable phylogenetic scenario allowed to trace the evolution of biological processes such as the reproductive modes and a large variety of regenerative abilities [500,[503][504][505].…”