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

ABSTRACT: BACKGROUND:Annelids 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. RESULTS:We 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, ?-catenin and PL10 (in S. gracilis). CONCLUSIONS:Posterior 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.

SUBMITTER: Ribeiro RP

PROVIDER: S-EPMC6854643 | biostudies-literature | 2019 Nov

REPOSITORIES: biostudies-literature

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

Ribeiro Rannyele Passos RP Ponz-Segrelles Guillermo G Bleidorn Christoph C Aguado Maria Teresa MT

BMC genomics 20191114 1

<h4>Background</h4>Annelids 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 instan ...[more]

PMID: 31726983

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Project description:BackgroundIn syllids (Annelida, Syllidae), the regenerative blastema was subject of many studies in the mid and late XXth century. This work on syllid regeneration showed that the blastema is developed by a process of dedifferentiation of cells near the wound, followed by their proliferation and redifferentiation (cells differentiate to the original cell type) or, in some specific cases, transdifferentiation (cells differentiate to a cell type different from the original). Up to date, participation of stem cells or pre-existing proliferative cells in the blastema development has never been observed in syllids. This study provides the first comprehensive description of Syllis malaquini's regenerative capacity, including data on the cellular proliferation dynamics by using an EdU/BrdU labelling approach, in order to trace proliferative cells (S-phase cells) present before and after operation.ResultsSyllis malaquini can restore the anterior and posterior body from different cutting levels under experimental conditions, even from midbody fragments. Our results on cellular proliferation showed that S-phase cells present in the body before bisection do not significantly contribute to blastema development. However, in some specimens cut at the level of the proventricle, cells in S-phase located in the digestive tube before bisection participated in regeneration. Also, our results showed that nucleus shape allows to distinguish different types of blastemal cells as forming specific tissues. Additionally, simultaneous and sequential addition of segments seem to occur in anterior regeneration, while only sequential addition was observed in posterior regeneration. Remarkably, in contrast with previous studies in syllids, sexual reproduction was not induced during anterior regeneration of amputees lacking the proventricle, a foregut organ widely known to be involved in the stolonization control.ConclusionsOur findings led us to consider that although dedifferentiation and redifferentiation might be more common, proliferative cells present before injury can be involved in regenerative processes in syllids, at least in some cases. Also, we provide data for comparative studies on resegmentation as a process that differs between anterior and posterior regeneration; and on the controversial role of the proventricle in the reproduction of different syllid lineages.

Project description:Amblyosyllis is a worldwide distributed group of annelids mainly found in coastal environments. It is well known among the polychaete specialists mostly because of its notable beauty, showing bright colourful patterns and outstanding long and coiled appendices. Amblyosyllis is a monophyletic genus easy to identify due to its distinct diagnostic features; however, the species and their boundaries are, in most cases, not well defined. Herein, we provide an extensive sample of Amblyosyllis material (115 specimens) from several world geographic areas. We have studied the morphological features of each specimen and photographed them alive. Two mitochondrial DNA markers (COI and 16S) and one nuclear gene fragment (28S, D1 region) were sequenced. We performed phylogenetic analyses based on each DNA partition, as well as the combined data sets, obtaining congruent results. Species delimitation methods such as distance analyses, statistical parsimony networks and multi-rate Poisson tree processes were also applied. The combined results obtained from different methodologies and data sets are used to differentiate between, at least, 19 lineages compatible with the separately evolving meta-populations species concept. Four of these lineages are identified as nominal species, including the type species of Amblyosyllis, A. rhombeata. For three other lineages previously synonymized names are recovered, and seven lineages are described as new species. All of these species are described and supported by appropriate iconography. We recognize several morphological characters useful to identify species of Amblyosyllis, which in some cases should also be combined with molecular methods for species delineation. The genetic divergence in the genus is high, contrary to the morphological homogeneity observed. Two species show a wide geographical distribution, while the rest have a more restricted distribution. There are several examples of species with overlapping distribution patterns.

Project description:BackgroundThe ground pattern underlying the nervous system of the last common ancestor in annelids was long thought to be settled, consisting of a dorsal brain, circumoesophageal connectives and a subepithelial, ladder-like ventral nerve cord with segmental ganglia connected by paired connectives. With the advent of immunocytochemical stainings and confocal laser scanning microscopy, it becomes evident that its architecture is extremely diverse, which makes the reconstruction of a ground pattern in annelida challenging. Whereas the nervous systems of many different families has already been described, only very few studies looked at the diversity of nervous systems within such clades to give a closer estimate on how plastic the annelid nervous system really is. So far, little is known on syllid nervous system architecture, one of the largest and most diverse groups of marine annelids.ResultsThe position of the brain, the circumoesophageal connectives, the stomatogastric nervous system, the longitudinal nerves that traverse each segment and the innervation of appendages are relatively uniform within the clade. Both the number of connectives within the ventral nerve cord and the number of segmental nerves, which in earlier studies were used to infer phylogenetic relationships and to reconstruct an annelid ground pattern, are highly diverse and differ between genera or even within a given genus. Differences in the distribution of somata of the brain, the nuchal innervation and its associated cell bodies were found between Syllinae and Exogoninae and may be subfamily-specific.ConclusionsThe nervous system morphology of syllids very likely depends on the taxon-specific ecological requirements. Thus, it is not surprising that in a clade, which occupies such diverse niches as the Annelida, we find similar patterns in phylogenetically widely separated species in similar niches and a high degree of modularity within a family. Only standardized protocols and staining methods can lead to comparable results, but so far different approaches have been taken to describe annelid nervous systems, making homologization of certain structures difficult. This study provides the first thorough description of the nervous system in the family Syllidae, allowing more detailed comparisons between annelid families in the future.

Dataset Information

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

Publications

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

Similar Datasets

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