Morphological, cellular and molecular characterization of posterior regeneration in the marine annelid Platynereis dumerilii

Abstract

Regeneration, the ability to restore body parts after an injury or an amputation, is a widespread but highly variable and complex phenomenon in animals. While having fascinating scientists for centuries, fundamental questions about the cellular basis of animal regeneration as well as its evolutionary history remain largely unanswered. We study regeneration of the marine annelid Platynereis dumerilii, an emerging comparative developmental biology model, which, like many other annelids, displays important regenerative abilities. If the posterior part of the body is amputated, P. dumerilii worms are able to regenerate the posteriormost differentiated part of the body and stem cell-rich growth zone that allows to make new segments which replace the amputated ones. We show that posterior regeneration is a rapid process that follows a well reproducible paths and timeline, going through specific stages that we thoroughly defined. Wound healing is achieved by one day post-amputation and a regeneration blastema forms one day later. At this time point, some tissue specification already occurs, and a functional posterior growth zone is re-established as early as three days after amputation. Regeneration is only influenced in a minor manner by worm size and position of the amputation site along the antero-posterior axis of the worm and regenerative abilities persist upon repeated amputations without important alterations of the process. We also show that intense cell proliferation occurs during regeneration and that cell divisions are strictly required for regeneration to normally proceed. Finally, through several 5-ethynyl-2-deoxyuridine (EdU) pulse and chase experiments, we provide evidence in favor of a local origin of the blastema, whose constituting cells mostly derive from the segment immediately abutting the amputation plane. The detailed characterization of P. dumerilii posterior body regeneration presented in this article provides the foundation for future mechanistic and comparative studies of regeneration in this species.