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.

Highlights

  • IntroductionStudies including molecular data during regeneration in annelids have been published for the clitellates Enchytraeus japonensis Nakamura, 1993 [11,12,13,14,15] and Pristina leidyi Smith, 1896 [1, 16,17,18,19,20]; and the non-clitellates Alitta virens Sars, 1835 [21,22,23,24], Capitella teleta Blake, Grassle and Eckelbarger, 2009 [25,26,27,28,29], and Platynereis dumerilli (Audouin and Milne Edwards, 1833) [3, 30,31,32,33,34,35]

  • Some genes that are expressed in the segment addition zone (SAZ) during regular growth/development have been detected in different stages of posterior regeneration in annelids, for example, Hox genes [21,22,23, 27, 45], β-catenin [17], and genes of the germline multipotency program such as piwi, vasa, nanos, and PL10 [27, 46,47,48]

  • Illumina NGS and assembly We used a comparative transcriptomic approach in order to compare gene expression in three conditions: anterior regeneration (AR), posterior regeneration (PR), and non-regenerating (NR), i.e. intact individuals in regular posterior growth. mRNA samples of S. hystrix and S. gracilis were sequenced for each condition using an Illumina sequencing platform

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Summary

Introduction

Studies including molecular data during regeneration in annelids have been published for the clitellates Enchytraeus japonensis Nakamura, 1993 [11,12,13,14,15] and Pristina leidyi Smith, 1896 [1, 16,17,18,19,20]; and the non-clitellates Alitta virens Sars, 1835 [21,22,23,24], Capitella teleta Blake, Grassle and Eckelbarger, 2009 [25,26,27,28,29], and Platynereis dumerilli (Audouin and Milne Edwards, 1833) [3, 30,31,32,33,34,35] All those species regenerate the posterior body, but only E. japonensis and P. leidyi exhibit anterior regeneration [1, 11,12,13,14,15, 17,18,19,20]. Some genes that are expressed in the SAZ during regular growth/development have been detected in different stages of posterior regeneration in annelids, for example, Hox genes [21,22,23, 27, 45], β-catenin [17], and genes of the germline multipotency program such as piwi, vasa, nanos, and PL10 [27, 46,47,48]

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