Distinct patterns of gene expression during regeneration and asexual reproduction in the annelid Pristina leidyi

Abstract

Regeneration, the ability to replace lost body parts, is a widespread phenomenon in the animal kingdom often connected to asexual reproduction or fission, since the only difference between the two appears to be the stimulus that triggers them. Both developmental processes have largely been characterized; however, the molecular toolkit and genetic mechanisms underlying these events remain poorly unexplored.Annelids, in particular the oligochaete Pristina leidyi, provide a good model system to investigate these processes as they show diverse ways to regenerate, and can reproduce asexually through fission under laboratory conditions. Here, we used a comparative transcriptomics approach based on RNA-sequencing and differential gene expression analyses to understand the molecular mechanisms involved in anterior regeneration and asexual reproduction. We found 291 genes upregulated during anterior regeneration, including several regeneration-related genes previously reported in other annelids such as frizzled, paics, and vdra. On the other hand, during asexual reproduction, 130 genes were found upregulated, and unexpectedly, many of them were related to germline development during sexual reproduction. We also found important differences between anterior regeneration and asexual reproduction, with the latter showing a gene expression profile more similar to that of control individuals. Nevertheless, we identified 35 genes that were upregulated in both conditions, many of them related to cell pluripotency, stem cells, and cell proliferation. Overall, our results shed light on the molecular mechanisms that control anterior regeneration and asexual reproduction in annelids and reveal similarities with other animals, suggesting that the genetic machinery controlling these processes is conserved across metazoans.

Recent Light on the Developmental Perspectives of Regeneration in Annelids

“…Important distinctions were also seen between asexual reproduction and anterior regeneration, with the latter exhibiting a gene expression profile more akin to that of control subjects. Nevertheless, we discovered 35 genes, many of which were connected to stem cells, cell proliferation, and pluripotency, that were increased in both circumstances [Olmo et al, 2022].…”

Spatial Colinear but Broken Temporal Expression of Duplicated ParaHox Genes in Asexually Reproducing Annelids, Nais communis and Pristina longiseta

“…For example, in P. longiseta, the Plo-otx and Plo-six3 genes show early expression in the segment in which the fission zone will develop, and thus mark the anterior border of the posterior zooid at early stages [35,41]. Despite the obvious advantages of this model for studying the (re)patterning processes during postembryonic development, our knowledge about the molecular mechanisms of body remodeling in adult bilaterians, in particular annelids, is very limited [35,[41][42][43][44][45].…”

Environmental and molecular regulation of asexual reproduction in the sea anemone Nematostella vectensis

“…Efforts to identify molecular mechanisms that regulate asexual reproduction are limited to the window during which a clone is being generated. Within Bilateria, gene expression has been characterized during asexual fissioning in the annelid Pristina leidyi [16], and functional experiments argue TGFβ, Wnt signalling, and homeobox transcription factors regulate fissioning in Planaria [12,17,18]. Within Cnidaria, FGF signalling has been implicated in extracellular matrix degradation leading to clone detachment during asexual reproduction in the coral Pocillopora acuta [19], and both FGF and Notch regulate bud site position, outgrowth and detachment in Hydra [20][21][22].…”