The Onset of Whole-Body Regeneration in Botryllus schlosseri: Morphological and Molecular Characterization

Abstract

Colonial tunicates are the only chordates that regularly regenerate a fully functional whole body as part of their asexual life cycle, starting from specific epithelia and/or mesenchymal cells. In addition, in some species, whole-body regeneration (WBR) can also be triggered by extensive injuries, which deplete most of their tissues and organs and leave behind only small fragments of their body. In this manuscript, we characterized the onset of WBR in Botryllus schlosseri, one colonial tunicate long used as a laboratory model. We first analyzed the transcriptomic response to a WBR-triggering injury. Then, through morphological characterization, in vivo observations via time-lapse, vital dyes, and cell transplant assays, we started to reconstruct the dynamics of the cells triggering regeneration, highlighting an interplay between mesenchymal and epithelial cells. The dynamics described here suggest that WBR in B. schlosseri is initiated by extravascular tissue fragments derived from the injured individuals rather than particular populations of blood-borne cells, as has been described in closely related species. The morphological and molecular datasets here reported provide the background for future mechanistic studies of the WBR ontogenesis in B. schlosseri and allow to compare it with other regenerative processes occurring in other tunicate species and possibly independently evolved.

Regeneração de corpo inteiro (WBR) e suas potenciais aplicações na saúde humana: uma revisão da literatura

“…Determinadas espécies de tunicados podem sofrer lesões tão avassaladoras ao ponto de esgotar seus tecidos e restar apenas alguns fragmentos e, a partir destes se regenerar inteiramente (RICCI et al, 2022).…”

First chromosome-level genome assembly of the colonial tunicateBotryllus schlosseri

“…(2016) RNAseq (24) and Ricci et al . (2022) RNAseq (7). TransDecoder (95) was run within PASA to identify coding sequences within the assembled transcripts.…”

“…Over the last decades, a scientific community has taken shape and several research groups have made significant efforts to improve breeding conditions (17)(18)(19) and to develop and adapt imaging and molecular biology techniques (7,8,20). Several anatomical descriptions and staging methods have been proposed (4,21) and various stage-specific and tissue-specific transcriptomic databases have been produced (7,(22)(23)(24)(25)(26). In 2013, a draft genome of B. schlosseri become available (27).…”

“…Finally, if all zooids and buds are removed from a colony of B. schlosseri, new buds can develop from the extracorporeal vascular sys-tem through a regenerative process known as vascular budding (5). The regenerating zooids propagate asexually and eventually reform a new colony (6,7). Zooids belonging to the same colony are essentially all clones.…”

“…Botryllus schlosseri was introduced in laboratories more than half a century ago (13), mainly as a model to study asexual development, regeneration (14), allorecognition and chimerism (15,16). Over the last decades, a scientific community has taken shape and several research groups have made significant efforts to improve breeding conditions (17)(18)(19) and to develop and adapt imaging and molecular biology techniques (7,8,20). Several anatomical descriptions and staging methods have been proposed (4,21) and various stage-specific and tissue-specific transcriptomic databases have been produced (7,(22)(23)(24)(25)(26).…”