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Gene regulation of adult skeletogenesis in starfish and modifications during gene network co-option
The larval skeleton of the echinoderm is believed to have been acquired through co-option of a pre-existing gene regulatory network (GRN); that is, the mechanism for adult skeleton formation in the echinoderm was deployed in early embryogenesis during echinoderm diversification. To explore the evolu...
Autores principales: | , , , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
Nature Publishing Group UK
2021
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Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8505446/ https://www.ncbi.nlm.nih.gov/pubmed/34635691 http://dx.doi.org/10.1038/s41598-021-99521-4 |
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author | Yamazaki, Atsuko Yamakawa, Shumpei Morino, Yoshiaki Sasakura, Yasunori Wada, Hiroshi |
author_facet | Yamazaki, Atsuko Yamakawa, Shumpei Morino, Yoshiaki Sasakura, Yasunori Wada, Hiroshi |
author_sort | Yamazaki, Atsuko |
collection | PubMed |
description | The larval skeleton of the echinoderm is believed to have been acquired through co-option of a pre-existing gene regulatory network (GRN); that is, the mechanism for adult skeleton formation in the echinoderm was deployed in early embryogenesis during echinoderm diversification. To explore the evolutionary changes that occurred during co-option, we examined the mechanism for adult skeletogenesis using the starfish Patiria pectinifera. Expression patterns of skeletogenesis-related genes (vegf, vegfr, ets1/2, erg, alx1, ca1, and clect) suggest that adult skeletogenic cells develop from the posterior coelom after the start of feeding. Treatment with inhibitors and gene knockout using transcription activator-like effector nucleases (TALENs) suggest that the feeding-nutrient sensing pathway activates Vegf signaling via target of rapamycin (TOR) activity, leading to the activation of skeletogenic regulatory genes in starfish. In the larval skeletogenesis of sea urchins, the homeobox gene pmar1 activates skeletogenic regulatory genes, but in starfish, localized expression of the pmar1-related genes phbA and phbB was not detected during the adult skeleton formation stage. Based on these data, we provide a model for the adult skeletogenic GRN in the echinoderm and propose that the upstream regulatory system changed from the feeding-TOR-Vegf pathway to a homeobox gene-system during co-option of the skeletogenic GRN. |
format | Online Article Text |
id | pubmed-8505446 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2021 |
publisher | Nature Publishing Group UK |
record_format | MEDLINE/PubMed |
spelling | pubmed-85054462021-10-13 Gene regulation of adult skeletogenesis in starfish and modifications during gene network co-option Yamazaki, Atsuko Yamakawa, Shumpei Morino, Yoshiaki Sasakura, Yasunori Wada, Hiroshi Sci Rep Article The larval skeleton of the echinoderm is believed to have been acquired through co-option of a pre-existing gene regulatory network (GRN); that is, the mechanism for adult skeleton formation in the echinoderm was deployed in early embryogenesis during echinoderm diversification. To explore the evolutionary changes that occurred during co-option, we examined the mechanism for adult skeletogenesis using the starfish Patiria pectinifera. Expression patterns of skeletogenesis-related genes (vegf, vegfr, ets1/2, erg, alx1, ca1, and clect) suggest that adult skeletogenic cells develop from the posterior coelom after the start of feeding. Treatment with inhibitors and gene knockout using transcription activator-like effector nucleases (TALENs) suggest that the feeding-nutrient sensing pathway activates Vegf signaling via target of rapamycin (TOR) activity, leading to the activation of skeletogenic regulatory genes in starfish. In the larval skeletogenesis of sea urchins, the homeobox gene pmar1 activates skeletogenic regulatory genes, but in starfish, localized expression of the pmar1-related genes phbA and phbB was not detected during the adult skeleton formation stage. Based on these data, we provide a model for the adult skeletogenic GRN in the echinoderm and propose that the upstream regulatory system changed from the feeding-TOR-Vegf pathway to a homeobox gene-system during co-option of the skeletogenic GRN. Nature Publishing Group UK 2021-10-11 /pmc/articles/PMC8505446/ /pubmed/34635691 http://dx.doi.org/10.1038/s41598-021-99521-4 Text en © The Author(s) 2021 https://creativecommons.org/licenses/by/4.0/Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) . |
spellingShingle | Article Yamazaki, Atsuko Yamakawa, Shumpei Morino, Yoshiaki Sasakura, Yasunori Wada, Hiroshi Gene regulation of adult skeletogenesis in starfish and modifications during gene network co-option |
title | Gene regulation of adult skeletogenesis in starfish and modifications during gene network co-option |
title_full | Gene regulation of adult skeletogenesis in starfish and modifications during gene network co-option |
title_fullStr | Gene regulation of adult skeletogenesis in starfish and modifications during gene network co-option |
title_full_unstemmed | Gene regulation of adult skeletogenesis in starfish and modifications during gene network co-option |
title_short | Gene regulation of adult skeletogenesis in starfish and modifications during gene network co-option |
title_sort | gene regulation of adult skeletogenesis in starfish and modifications during gene network co-option |
topic | Article |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8505446/ https://www.ncbi.nlm.nih.gov/pubmed/34635691 http://dx.doi.org/10.1038/s41598-021-99521-4 |
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