Evolution of Allorecognition in the Tunicata

Nydam, Marie L.

doi:10.3390/biology9060129

“…In addition to this role during regeneration [12], hemocytes are involved in numerous biological processes in colonial tunicates, including immune response [13][14][15], allorecognition [16][17][18], and asexual reproduction [19][20][21]. Colonial tunicates' hemolymph is typically composed of less than a dozen 4-to 25-μm-wide cell types classified into four functional classes: undifferentiated, phagocytic, cytotoxic, and storage cells [22][23][24][25].…”

Section: Introductionmentioning

confidence: 99%

Noninvasive Intravascular Microtransfusion in Colonial Tunicates

Serrato

¹

,

Bilella

²

,

Blanchoud

³

2022

Methods in Molecular Biology

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Tunicates are a diverse group of worldwide marine filter-feeders that are vertebrates’ closest invertebrate relatives. Colonial tunicates are the only know chordates that have been shown to undergo whole-body regeneration (WBR). Botrylloides in particular can regenerate one fully functional adult from a minute fragment of their vascular system in as little as 10 days. This regenerative process relies on the proliferation of circulating stem cells, likely supported by the activity of some of the 11 identified types of hemocytes. To study and challenge WBR, it is thus important to have the capacity to isolate, analyze, and manipulate hemolymph in regenerating colonies. Here we present a microtransfusion technique that permits the collection of pure hemocytes, the quantification of their purity, their labeling, and reinjection into colonial tunicates. To exemplify our approach, we present in addition a protocol to analyze the isolated hemocytes using flow cytometry. Our approach is minimally invasive, does not induce lethality, and therefore allows repeated transfusion into exactly the same colony with minimal disruption to the process being studied.

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“…Among tunicates, both the diversity of the cellular onsets and the phylogenetic distribution suggests that the WBR capacity via propagative and survival budding is a plastic trait that evolved multiple times ( Alié et al, 2018 ; Nydam, 2020 ). Mesenchymal stem cell-driven budding like vascular budding, has been suggested as a propagative and/or survival mode of WBR in several species of tunicates and it has been documented in Botryllus schlosseri’ s closest related species such as Botrylloides diegensis ( Supplementary Figure S1 ).…”

Section: Discussionmentioning

confidence: 99%

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

Ricci

¹

,

Salmon

²

,

Olivier

³

et al. 2022

Front. Cell Dev. Biol.

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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.

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“…Among tunicates, both the diversity of the cellular onsets and the phylogenetic distribution suggests that the WBR capacity via propagative and survival budding is a plastic trait that evolved multiple times (Alié et al, 2018;Nydam, 2020). Mesenchymal stem cell-driven budding like vascular budding, 21 has been suggested as a propagative and/or survival mode of WBR in several species of tunicates and it has been documented in Botryllus schlosseri's closest related species such as Botrylloides diegensis (Supplementary Figure 1).…”

Section: Variation Of Injury-induced Wbr Capacities Across Botryllinaementioning

confidence: 99%

The onset of whole-body regeneration inBotryllus schlosseri: morphological and molecular characterization

Ricci

¹

,

Salmon

²

,

Olivier

³

et al. 2022

Preprint

0

View full text Add to dashboard Cite

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.

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Evolution of Allorecognition in the Tunicata

Cited by 8 publications

References 84 publications

Noninvasive Intravascular Microtransfusion in Colonial Tunicates

Noninvasive Intravascular Microtransfusion in Colonial Tunicates

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

The onset of whole-body regeneration inBotryllus schlosseri: morphological and molecular characterization

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