Ruta, C. | Search bioRxiv

bioRxiv2024

Molecular profile, source and lineage restriction of stem cells in an annelid regeneration model

Regeneration of missing body parts can be observed in diverse animal phyla, but it remains unclear to which extent these capacities rely on shared or divergent principles. Research into this question requires detailed knowledge about the involved molecular and cellular principles in suitable reference models. By combining single-cell RNA sequencing and mosaic transgenesis in the marine annelid Platynereis dumerilii, we map cellular profiles and lineage restrictions during posterior regeneration. Our data reveal cell-type specific injury responses, re-expression of positional identity factors, and the re-emergence of stem cell signatures in multiple cell populations. Epidermis and mesodermal coelomic tissue produce distinct putative posterior stem cells (PSCs) in the emerging blastema. A novel mosaic transgenesis strategy reveals both developmental compartments and lineage restrictions during regenerative growth. Our work supports the notion that posterior regeneration involves dedifferentiation, and reveals molecular and mechanistic parallels between annelid and vertebrate regeneration.

developmental biology↗

bioRxiv2019

Globins and hemogenic cells in the marine Annelid Platynereis dumerilii shed new light on blood evolution in Bilaterians

BackgroundHow vascular systems and their respiratory pigments evolved is still debated. While many animals present a vascular system, hemoglobin exists as a blood pigment only in a few groups (Vertebrates, Annelids, a few Arthropod and Mollusk species). Hemoglobins are formed of globin sub-units, belonging to multigene families, in various multimeric assemblages. It was so far unclear whether hemoglobin families from different Bilaterian groups had a common origin. ResultsTo unravel globin evolution in Bilaterians, we studied the marine Annelid Platynereis dumerilii, a species with a slow evolving genome. Platynereis exhibits a closed vascular system filled with extracellular hemoglobin. Platynereis genome and transcriptomes reveal a family of 19 globins, nine of which are predicted to be extracellular. Extracellular globins are produced by specialized cells lining the vessels of the segmental appendages of the worm, serving as gills, and thus likely participate in the assembly of the giant hexagonal bilayer hemoglobin of the worm. Extracellular globin mRNAs are absent in smaller juvenile, accumulate considerably in growing and more active worms and peak in swarming adults, as the need for O2 culminates. Next, we conducted a Metazoan-wide phylogenetic analysis of globins using data from complete genomes. We establish that five globin genes (stem globins) were present in the last common ancestor of Bilaterians. Based on these results, we propose a new nomenclature of globins, with five clades. All five ancestral stem-globin clades are retained in some Spiralians, while some clades disappeared early in Deuterostome and Ecdysozoan evolution. All known Bilaterian blood globin families are grouped in a single clade (clade I) together with intracellular globins of Bilaterians devoid of red blood. ConclusionsWe uncover a complex "pre-blood" evolution of globins, with an early gene radiation in ancestral Bilaterians. Circulating hemoglobins in various bilaterian groups evolved convergently, presumably in correlation with animal size and activity. However, all hemoglobins derive from a clade I globin, or cytoglobin, probably involved in intracellular O2 transit and regulation (clade I). The Annelid Platynereis is remarkable in having a large family of extracellular blood globins, while retaining all clades of ancestral Bilaterian globins.

evolutionary biology↗