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Segment number threshold determines juvenile onset of germline cluster expansion in Platynereis dumerilii

Development of sexual characters and generation of gametes are tightly coupled with growth. Platynereis dumerilii is a marine annelid that has been used to study germline development and gametogenesis. P. dumerilii has germ cell clusters found across the body in the juvenile worms, and the clusters...

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Autores principales: Kuehn, Emily, Clausen, David S., Null, Ryan W., Metzger, Bria M., Willis, Amy D., Özpolat, B. Duygu
Formato: Online Artículo Texto
Lenguaje:English
Publicado: John Wiley and Sons Inc. 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9114164/
https://www.ncbi.nlm.nih.gov/pubmed/34793615
http://dx.doi.org/10.1002/jez.b.23100
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author Kuehn, Emily
Clausen, David S.
Null, Ryan W.
Metzger, Bria M.
Willis, Amy D.
Özpolat, B. Duygu
author_facet Kuehn, Emily
Clausen, David S.
Null, Ryan W.
Metzger, Bria M.
Willis, Amy D.
Özpolat, B. Duygu
author_sort Kuehn, Emily
collection PubMed
description Development of sexual characters and generation of gametes are tightly coupled with growth. Platynereis dumerilii is a marine annelid that has been used to study germline development and gametogenesis. P. dumerilii has germ cell clusters found across the body in the juvenile worms, and the clusters eventually form the gametes. Like other segmented worms, P. dumerilii grows by adding new segments at its posterior end. The number of segments reflect the growth state of the worms and therefore is a useful and measurable growth state metric to study the growth‐reproduction crosstalk. To understand how growth correlates with progression of gametogenesis, we investigated germline development across several developmental stages. We discovered a distinct transition period when worms increase the number of germline clusters at a particular segment number threshold. Additionally, we found that keeping worms short in segment number, by manipulating environmental conditions or via amputations, supported a segment number threshold requirement for germline development. Finally, we asked if these clusters in P. dumerilii play a role in regeneration (as similar free‐roaming cells are observed in Hydra and planarian regeneration) and found that the clusters were not required for regeneration in P. dumerilii, suggesting a strictly germline nature. Overall, these molecular analyses suggest a previously unidentified developmental transition dependent on the growth state of juvenile P. dumerilii leading to substantially increased germline expansion.
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spelling pubmed-91141642022-10-14 Segment number threshold determines juvenile onset of germline cluster expansion in Platynereis dumerilii Kuehn, Emily Clausen, David S. Null, Ryan W. Metzger, Bria M. Willis, Amy D. Özpolat, B. Duygu J Exp Zool B Mol Dev Evol Research Articles Development of sexual characters and generation of gametes are tightly coupled with growth. Platynereis dumerilii is a marine annelid that has been used to study germline development and gametogenesis. P. dumerilii has germ cell clusters found across the body in the juvenile worms, and the clusters eventually form the gametes. Like other segmented worms, P. dumerilii grows by adding new segments at its posterior end. The number of segments reflect the growth state of the worms and therefore is a useful and measurable growth state metric to study the growth‐reproduction crosstalk. To understand how growth correlates with progression of gametogenesis, we investigated germline development across several developmental stages. We discovered a distinct transition period when worms increase the number of germline clusters at a particular segment number threshold. Additionally, we found that keeping worms short in segment number, by manipulating environmental conditions or via amputations, supported a segment number threshold requirement for germline development. Finally, we asked if these clusters in P. dumerilii play a role in regeneration (as similar free‐roaming cells are observed in Hydra and planarian regeneration) and found that the clusters were not required for regeneration in P. dumerilii, suggesting a strictly germline nature. Overall, these molecular analyses suggest a previously unidentified developmental transition dependent on the growth state of juvenile P. dumerilii leading to substantially increased germline expansion. John Wiley and Sons Inc. 2021-11-18 2022-06 /pmc/articles/PMC9114164/ /pubmed/34793615 http://dx.doi.org/10.1002/jez.b.23100 Text en © 2021 The Authors. Journal of Experimental Zoology Part B: Molecular and Developmental Evolution published by Wiley Periodicals LLC https://creativecommons.org/licenses/by-nc-nd/4.0/This is an open access article under the terms of the http://creativecommons.org/licenses/by-nc-nd/4.0/ (https://creativecommons.org/licenses/by-nc-nd/4.0/) License, which permits use and distribution in any medium, provided the original work is properly cited, the use is non‐commercial and no modifications or adaptations are made.
spellingShingle Research Articles
Kuehn, Emily
Clausen, David S.
Null, Ryan W.
Metzger, Bria M.
Willis, Amy D.
Özpolat, B. Duygu
Segment number threshold determines juvenile onset of germline cluster expansion in Platynereis dumerilii
title Segment number threshold determines juvenile onset of germline cluster expansion in Platynereis dumerilii
title_full Segment number threshold determines juvenile onset of germline cluster expansion in Platynereis dumerilii
title_fullStr Segment number threshold determines juvenile onset of germline cluster expansion in Platynereis dumerilii
title_full_unstemmed Segment number threshold determines juvenile onset of germline cluster expansion in Platynereis dumerilii
title_short Segment number threshold determines juvenile onset of germline cluster expansion in Platynereis dumerilii
title_sort segment number threshold determines juvenile onset of germline cluster expansion in platynereis dumerilii
topic Research Articles
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9114164/
https://www.ncbi.nlm.nih.gov/pubmed/34793615
http://dx.doi.org/10.1002/jez.b.23100
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