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A Krüppel-like factor is required for development and regeneration of germline and yolk cells from somatic stem cells in planarians

Sexually reproducing animals segregate their germline from their soma. In addition to gamete-producing gonads, planarian and parasitic flatworm reproduction relies on yolk cell–generating accessory reproductive organs (vitellaria) supporting development of yolkless oocytes. Despite the importance of...

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Autores principales: Issigonis, Melanie, Redkar, Akshada B., Rozario, Tania, Khan, Umair W., Mejia-Sanchez, Rosa, Lapan, Sylvain W., Reddien, Peter W., Newmark, Phillip A.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9286257/
https://www.ncbi.nlm.nih.gov/pubmed/35839223
http://dx.doi.org/10.1371/journal.pbio.3001472
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author Issigonis, Melanie
Redkar, Akshada B.
Rozario, Tania
Khan, Umair W.
Mejia-Sanchez, Rosa
Lapan, Sylvain W.
Reddien, Peter W.
Newmark, Phillip A.
author_facet Issigonis, Melanie
Redkar, Akshada B.
Rozario, Tania
Khan, Umair W.
Mejia-Sanchez, Rosa
Lapan, Sylvain W.
Reddien, Peter W.
Newmark, Phillip A.
author_sort Issigonis, Melanie
collection PubMed
description Sexually reproducing animals segregate their germline from their soma. In addition to gamete-producing gonads, planarian and parasitic flatworm reproduction relies on yolk cell–generating accessory reproductive organs (vitellaria) supporting development of yolkless oocytes. Despite the importance of vitellaria for flatworm reproduction (and parasite transmission), little is known about this unique evolutionary innovation. Here, we examine reproductive system development in the planarian Schmidtea mediterranea, in which pluripotent stem cells generate both somatic and germ cell lineages. We show that a homolog of the pluripotency factor Klf4 is expressed in primordial germ cells (PGCs), presumptive germline stem cells (GSCs), and yolk cell progenitors. Knockdown of this klf4-like (klf4l) gene results in animals that fail to specify or maintain germ cells; surprisingly, they also fail to maintain yolk cells. We find that yolk cells display germ cell–like attributes and that vitellaria are structurally analogous to gonads. In addition to identifying a new proliferative cell population in planarians (yolk cell progenitors) and defining its niche, our work provides evidence supporting the hypothesis that flatworm germ cells and yolk cells share a common evolutionary origin.
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spelling pubmed-92862572022-07-16 A Krüppel-like factor is required for development and regeneration of germline and yolk cells from somatic stem cells in planarians Issigonis, Melanie Redkar, Akshada B. Rozario, Tania Khan, Umair W. Mejia-Sanchez, Rosa Lapan, Sylvain W. Reddien, Peter W. Newmark, Phillip A. PLoS Biol Research Article Sexually reproducing animals segregate their germline from their soma. In addition to gamete-producing gonads, planarian and parasitic flatworm reproduction relies on yolk cell–generating accessory reproductive organs (vitellaria) supporting development of yolkless oocytes. Despite the importance of vitellaria for flatworm reproduction (and parasite transmission), little is known about this unique evolutionary innovation. Here, we examine reproductive system development in the planarian Schmidtea mediterranea, in which pluripotent stem cells generate both somatic and germ cell lineages. We show that a homolog of the pluripotency factor Klf4 is expressed in primordial germ cells (PGCs), presumptive germline stem cells (GSCs), and yolk cell progenitors. Knockdown of this klf4-like (klf4l) gene results in animals that fail to specify or maintain germ cells; surprisingly, they also fail to maintain yolk cells. We find that yolk cells display germ cell–like attributes and that vitellaria are structurally analogous to gonads. In addition to identifying a new proliferative cell population in planarians (yolk cell progenitors) and defining its niche, our work provides evidence supporting the hypothesis that flatworm germ cells and yolk cells share a common evolutionary origin. Public Library of Science 2022-07-15 /pmc/articles/PMC9286257/ /pubmed/35839223 http://dx.doi.org/10.1371/journal.pbio.3001472 Text en © 2022 Issigonis et al https://creativecommons.org/licenses/by/4.0/This is an open access article distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
spellingShingle Research Article
Issigonis, Melanie
Redkar, Akshada B.
Rozario, Tania
Khan, Umair W.
Mejia-Sanchez, Rosa
Lapan, Sylvain W.
Reddien, Peter W.
Newmark, Phillip A.
A Krüppel-like factor is required for development and regeneration of germline and yolk cells from somatic stem cells in planarians
title A Krüppel-like factor is required for development and regeneration of germline and yolk cells from somatic stem cells in planarians
title_full A Krüppel-like factor is required for development and regeneration of germline and yolk cells from somatic stem cells in planarians
title_fullStr A Krüppel-like factor is required for development and regeneration of germline and yolk cells from somatic stem cells in planarians
title_full_unstemmed A Krüppel-like factor is required for development and regeneration of germline and yolk cells from somatic stem cells in planarians
title_short A Krüppel-like factor is required for development and regeneration of germline and yolk cells from somatic stem cells in planarians
title_sort krüppel-like factor is required for development and regeneration of germline and yolk cells from somatic stem cells in planarians
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9286257/
https://www.ncbi.nlm.nih.gov/pubmed/35839223
http://dx.doi.org/10.1371/journal.pbio.3001472
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