Regeneration in the absence of canonical neoblasts in an early branching flatworm

Abstract The remarkable regenerative abilities of flatworms are closely linked to neoblasts – adult pluripotent stem cells that are the only division-competent cell type outside of the reproductive system. Although the presence of neoblast-like cells and whole-body regeneration in other animals has...

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Main Authors: Ludwik Gąsiorowski, Chew Chai, Andrei Rozanski, Gargi Purandare, Fruzsina Ficze, Athanasia Mizi, Bo Wang, Jochen C. Rink
Format: Article
Language:English
Published: Nature Portfolio 2025-01-01
Series:Nature Communications
Online Access:https://doi.org/10.1038/s41467-024-54716-x
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author Ludwik Gąsiorowski
Chew Chai
Andrei Rozanski
Gargi Purandare
Fruzsina Ficze
Athanasia Mizi
Bo Wang
Jochen C. Rink
author_facet Ludwik Gąsiorowski
Chew Chai
Andrei Rozanski
Gargi Purandare
Fruzsina Ficze
Athanasia Mizi
Bo Wang
Jochen C. Rink
author_sort Ludwik Gąsiorowski
collection DOAJ
description Abstract The remarkable regenerative abilities of flatworms are closely linked to neoblasts – adult pluripotent stem cells that are the only division-competent cell type outside of the reproductive system. Although the presence of neoblast-like cells and whole-body regeneration in other animals has led to the idea that these features may represent the ancestral metazoan state, the evolutionary origin of both remains unclear. Here we show that the catenulid Stenostomum brevipharyngium, a member of the earliest-branching flatworm lineage, lacks conventional neoblasts despite being capable of whole-body regeneration and asexual reproduction. Using a combination of single-nuclei transcriptomics, in situ gene expression analysis, and functional experiments, we find that cell divisions are not restricted to a single cell type and are associated with multiple fully differentiated somatic tissues. Furthermore, the cohort of germline multipotency genes, which are considered canonical neoblast markers, are not expressed in dividing cells, but in the germline instead, and we experimentally show that they are neither necessary for proliferation nor regeneration. Overall, our results challenge the notion that canonical neoblasts are necessary for flatworm regeneration and open up the possibility that neoblast-like cells may have evolved convergently in different animals, independent of their regenerative capacity.
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spelling doaj-art-49381b90ca17473b92ceca210e5c5af02025-02-02T12:32:01ZengNature PortfolioNature Communications2041-17232025-01-0116111410.1038/s41467-024-54716-xRegeneration in the absence of canonical neoblasts in an early branching flatwormLudwik Gąsiorowski0Chew Chai1Andrei Rozanski2Gargi Purandare3Fruzsina Ficze4Athanasia Mizi5Bo Wang6Jochen C. Rink7Department of Tissue Dynamics and Regeneration, Max Planck Institute for Multidisciplinary SciencesDepartment of Bioengineering, Stanford UniversityDepartment of Tissue Dynamics and Regeneration, Max Planck Institute for Multidisciplinary SciencesDepartment of Tissue Dynamics and Regeneration, Max Planck Institute for Multidisciplinary SciencesDepartment of Tissue Dynamics and Regeneration, Max Planck Institute for Multidisciplinary SciencesInstitute of Pathology, University Medical Centre GöttingenDepartment of Bioengineering, Stanford UniversityDepartment of Tissue Dynamics and Regeneration, Max Planck Institute for Multidisciplinary SciencesAbstract The remarkable regenerative abilities of flatworms are closely linked to neoblasts – adult pluripotent stem cells that are the only division-competent cell type outside of the reproductive system. Although the presence of neoblast-like cells and whole-body regeneration in other animals has led to the idea that these features may represent the ancestral metazoan state, the evolutionary origin of both remains unclear. Here we show that the catenulid Stenostomum brevipharyngium, a member of the earliest-branching flatworm lineage, lacks conventional neoblasts despite being capable of whole-body regeneration and asexual reproduction. Using a combination of single-nuclei transcriptomics, in situ gene expression analysis, and functional experiments, we find that cell divisions are not restricted to a single cell type and are associated with multiple fully differentiated somatic tissues. Furthermore, the cohort of germline multipotency genes, which are considered canonical neoblast markers, are not expressed in dividing cells, but in the germline instead, and we experimentally show that they are neither necessary for proliferation nor regeneration. Overall, our results challenge the notion that canonical neoblasts are necessary for flatworm regeneration and open up the possibility that neoblast-like cells may have evolved convergently in different animals, independent of their regenerative capacity.https://doi.org/10.1038/s41467-024-54716-x
spellingShingle Ludwik Gąsiorowski
Chew Chai
Andrei Rozanski
Gargi Purandare
Fruzsina Ficze
Athanasia Mizi
Bo Wang
Jochen C. Rink
Regeneration in the absence of canonical neoblasts in an early branching flatworm
Nature Communications
title Regeneration in the absence of canonical neoblasts in an early branching flatworm
title_full Regeneration in the absence of canonical neoblasts in an early branching flatworm
title_fullStr Regeneration in the absence of canonical neoblasts in an early branching flatworm
title_full_unstemmed Regeneration in the absence of canonical neoblasts in an early branching flatworm
title_short Regeneration in the absence of canonical neoblasts in an early branching flatworm
title_sort regeneration in the absence of canonical neoblasts in an early branching flatworm
url https://doi.org/10.1038/s41467-024-54716-x
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