ABSTRACT
The capacity to regenerate lost tissues varies significantly among animals. Some phyla, such as the annelids, display substantial regenerating abilities, although little is known about the cellular mechanisms underlying the process. To precisely determine the origin, plasticity and fate of the cells participating in blastema formation and posterior end regeneration after amputation in the annelid Platynereis dumerilii, we developed specific tools to track different cell populations. Using these tools, we find that regeneration is partly promoted by a population of proliferative gut cells whose regenerative potential varies as a function of their position along the antero-posterior axis of the worm. Gut progenitors from anterior differentiated tissues are lineage restricted, whereas gut progenitors from the less differentiated and more proliferative posterior tissues are much more plastic. However, they are unable to regenerate the stem cells responsible for the growth of the worms. Those stem cells are of local origin, deriving from the cells present in the segment abutting the amputation plane, as are most of the blastema cells. Our results favour a hybrid and flexible cellular model for posterior regeneration in Platynereis relying on different degrees of cell plasticity.
Footnotes
Author contributions
Conceptualization: L. Bideau, P.G.-H., V.R., M.V., E.G.; Methodology: L. Bideau, V.R., M.V., E.G.; Validation: L. Bideau, E.G.; Formal analysis: L. Bideau, E.G.; Investigation: L. Bideau, Z.V.-R., L. Baduel, M.B., E.G.; Resources: M.V., E.G.; Writing - original draft: L. Bideau, E.G.; Writing - review & editing: L. Bideau, P.G.-H., V.R., E.G.; Visualization: L. Bideau, E.G.; Supervision: P.G.-H., V.R., M.V., E.G.; Project administration: M.V., E.G.; Funding acquisition: M.V., E.G.
Funding
Work in our team is supported by funding from Labex ‘Who Am I’ laboratory of excellence (ANR-11-LABX-0071) funded by the French Government through its ‘Investments for the Future’ program operated by the Agence Nationale de la Recherche (ANR-11-IDEX-0005-01 and ANR-19-CE27-0027-01), by the Institut des Sciences Biologiques (INSB) of the Centre National de la Recherche Scientifique (CNRS) (Diversity of Biological Mechanisms), by the Université Paris Cité, by the Association pour la Recherche sur le Cancer (PJA 20191209482) and by the comité départemental de Paris de la Ligue Contre le Cancer (RS20/75-20). L. Bideau has been awarded a CDSN PhD fellowship from the École normale supérieure de Lyon and the fourth year of his PhD is supported by Labex ‘Who am I’.
Data availability
All relevant data can be found within the article and its supplementary information.
Special Issue
This article is part of the Special Issue ‘Uncovering developmental diversity’, edited by Cassandra Extavour, Liam Dolan and Karen Sears. See related articles at https://journals.biologists.com/dev/issue/151/20.
