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.
Highlights
IntroductionWithin the lifespan of a metazoan, sub-lethal damages or loss of body parts can occur frequently as a consequence of predation, competition, pathogens infections, or by accident
The most extreme examples of regeneration occur when the entire functional body is restored from only minute fragments of the original organism, a bona fide ontogenesis generally referred to as whole-body regeneration (WBR)
Among the different taxa that acquired WBR, the interest in tunicates regenerative abilities emerged due to their phylogenetic position as the sister group of vertebrates, and because their regenerative capabilities are plastic within the sub-phylum, FIGURE 7 | Cell proliferation dynamics and Integrin alpha 6 (Ia6) expression in ampullae during the first 3 days after microdissection. (A–B) Confocal z-stack showing the detail of an ampulla: proliferating cells are stained with anti-phospho-HH3, cell nuclei are counter-stained with Hoechst, ampulla shape is outlined with dotted lines. (C) Average number of pHH3+ cells per ampulla for five time-points within the first 3 days after microdissection
Summary
Within the lifespan of a metazoan, sub-lethal damages or loss of body parts can occur frequently as a consequence of predation, competition, pathogens infections, or by accident Animals cope with such traumatic events by developing a wide range of strategies, such as the synthesis of protective structure, scar formation, or various degrees of regeneration (Vorontsova and Liosner, 1961; Sinigaglia et al, 2022). The way the propagative budding processes unfold differs from one species to another, starting from different and often non-homologous cells and tissues, but often converging into a common stage of two concentric hollow vesicles, each of them formed of a monolayer epithelium, reviewed in Alié et al, 2020. The capacity of WBR is a characteristic of their life-cycle, but it can be triggered in response to extensive injury (Tiozzo et al, 2008a), in which case the WBR process is referred to as survival budding (Nakauchi, 1982)
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