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Novel budding mode in Polyandrocarpa zorritensis: a model for comparative studies on asexual development and whole body regeneration

BACKGROUND: In tunicates, the capacity to build an adult body via non-embryonic development (NED), i.e., asexual budding and whole body regeneration, has been gained or lost several times across the whole subphylum. A recent phylogeny of the family Styelidae revealed an independent acquisition of NE...

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Autores principales: Scelzo, Marta, Alié, Alexandre, Pagnotta, Sophie, Lejeune, Camille, Henry, Pauline, Gilletta, Laurent, Hiebert, Laurel S., Mastrototaro, Francesco, Tiozzo, Stefano
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6446293/
https://www.ncbi.nlm.nih.gov/pubmed/30984365
http://dx.doi.org/10.1186/s13227-019-0121-x
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author Scelzo, Marta
Alié, Alexandre
Pagnotta, Sophie
Lejeune, Camille
Henry, Pauline
Gilletta, Laurent
Hiebert, Laurel S.
Mastrototaro, Francesco
Tiozzo, Stefano
author_facet Scelzo, Marta
Alié, Alexandre
Pagnotta, Sophie
Lejeune, Camille
Henry, Pauline
Gilletta, Laurent
Hiebert, Laurel S.
Mastrototaro, Francesco
Tiozzo, Stefano
author_sort Scelzo, Marta
collection PubMed
description BACKGROUND: In tunicates, the capacity to build an adult body via non-embryonic development (NED), i.e., asexual budding and whole body regeneration, has been gained or lost several times across the whole subphylum. A recent phylogeny of the family Styelidae revealed an independent acquisition of NED in the colonial species Polyandrocarpa zorritensis and highlighted a novel budding mode. In this paper, we provide the first detailed characterization of the asexual life cycle of P. zorritensis. RESULTS: Bud formation occurs along a tubular protrusion of the adult epidermis, the stolon, in a vascularized area defined as budding nest. The bud arises through a folding of the epithelia of the stolon with the contribution of undifferentiated mesenchymal cells. This previously unreported mode of bud onset leads to the formation of a double vesicle, which starts to develop into a zooid through morphogenetic mechanisms common to other Styelidae. The budding nest can also continue to accumulate nutrients and develop into a round-shaped structure, designated as spherule, which represents a dormant form able to survive low temperatures. CONCLUSIONS: To understand the mechanisms of NED and their evolution, it is fundamental to start from a robust phylogenetic framework in order to select relevant species to compare. The anatomical description of P. zorritensis NED provides the foundation for future comparative studies on plasticity of budding and regeneration in tunicates. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (10.1186/s13227-019-0121-x) contains supplementary material, which is available to authorized users.
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spelling pubmed-64462932019-04-12 Novel budding mode in Polyandrocarpa zorritensis: a model for comparative studies on asexual development and whole body regeneration Scelzo, Marta Alié, Alexandre Pagnotta, Sophie Lejeune, Camille Henry, Pauline Gilletta, Laurent Hiebert, Laurel S. Mastrototaro, Francesco Tiozzo, Stefano EvoDevo Research BACKGROUND: In tunicates, the capacity to build an adult body via non-embryonic development (NED), i.e., asexual budding and whole body regeneration, has been gained or lost several times across the whole subphylum. A recent phylogeny of the family Styelidae revealed an independent acquisition of NED in the colonial species Polyandrocarpa zorritensis and highlighted a novel budding mode. In this paper, we provide the first detailed characterization of the asexual life cycle of P. zorritensis. RESULTS: Bud formation occurs along a tubular protrusion of the adult epidermis, the stolon, in a vascularized area defined as budding nest. The bud arises through a folding of the epithelia of the stolon with the contribution of undifferentiated mesenchymal cells. This previously unreported mode of bud onset leads to the formation of a double vesicle, which starts to develop into a zooid through morphogenetic mechanisms common to other Styelidae. The budding nest can also continue to accumulate nutrients and develop into a round-shaped structure, designated as spherule, which represents a dormant form able to survive low temperatures. CONCLUSIONS: To understand the mechanisms of NED and their evolution, it is fundamental to start from a robust phylogenetic framework in order to select relevant species to compare. The anatomical description of P. zorritensis NED provides the foundation for future comparative studies on plasticity of budding and regeneration in tunicates. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (10.1186/s13227-019-0121-x) contains supplementary material, which is available to authorized users. BioMed Central 2019-04-03 /pmc/articles/PMC6446293/ /pubmed/30984365 http://dx.doi.org/10.1186/s13227-019-0121-x Text en © The Author(s) 2019 Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.
spellingShingle Research
Scelzo, Marta
Alié, Alexandre
Pagnotta, Sophie
Lejeune, Camille
Henry, Pauline
Gilletta, Laurent
Hiebert, Laurel S.
Mastrototaro, Francesco
Tiozzo, Stefano
Novel budding mode in Polyandrocarpa zorritensis: a model for comparative studies on asexual development and whole body regeneration
title Novel budding mode in Polyandrocarpa zorritensis: a model for comparative studies on asexual development and whole body regeneration
title_full Novel budding mode in Polyandrocarpa zorritensis: a model for comparative studies on asexual development and whole body regeneration
title_fullStr Novel budding mode in Polyandrocarpa zorritensis: a model for comparative studies on asexual development and whole body regeneration
title_full_unstemmed Novel budding mode in Polyandrocarpa zorritensis: a model for comparative studies on asexual development and whole body regeneration
title_short Novel budding mode in Polyandrocarpa zorritensis: a model for comparative studies on asexual development and whole body regeneration
title_sort novel budding mode in polyandrocarpa zorritensis: a model for comparative studies on asexual development and whole body regeneration
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6446293/
https://www.ncbi.nlm.nih.gov/pubmed/30984365
http://dx.doi.org/10.1186/s13227-019-0121-x
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