Antero-posterior gradients of cell plasticity and proliferation modulate posterior regeneration in the annelid Platynereis

Abstract

Regenerative abilities are extremely variable among animals and may be substantial in some phyla, such as the annelids. So far, the cellular mechanisms underlying regeneration in annelids remain elusive. To precisely determine the origin(s), plasticity and fate of the cells participating in the blastema formation during posterior regeneration in the annelid Platynereis dumerilii, we developed specific tools to track proliferative cells as well as gut epithelial cells. We showed that two populations of progenitors are at play during regeneration and that, among them, gut progenitors from differentiated tissues are lineage-restricted. Strikingly, gut progenitors from less differentiated and more proliferative tissues are much more plastic and can produce ectodermal and mesodermal derivatives, in addition to gut cells. However, their plasticity is de facto limited as exemplified by their inability to regenerate populations of stem cells responsible for the constant growth of the worms. We evidenced that those stem cells are from local origin (i.e. from the segment abutting the amputation plan) as most of the blastema cells. Our results are in favour of a hybrid and flexible cellular model for posterior regeneration in Platynereis relying on a gradient of cell plasticity along the antero-posterior axis of the animal.