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Salpa genome and developmental transcriptome analyses reveal molecular flexibility enabling reproductive success in a rapidly changing environment

Ocean warming favors pelagic tunicates, such as salps, that exhibit increasingly frequent and rapid population blooms, impacting trophic dynamics and composition and human marine-dependent activities. Salp blooms are a result of their successful reproductive life history, alternating seasonally betw...

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Autores principales: Castellano, Kate R., Batta-Lona, Paola, Bucklin, Ann, O’Neill, Rachel J.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10686999/
https://www.ncbi.nlm.nih.gov/pubmed/38030690
http://dx.doi.org/10.1038/s41598-023-47429-6
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author Castellano, Kate R.
Batta-Lona, Paola
Bucklin, Ann
O’Neill, Rachel J.
author_facet Castellano, Kate R.
Batta-Lona, Paola
Bucklin, Ann
O’Neill, Rachel J.
author_sort Castellano, Kate R.
collection PubMed
description Ocean warming favors pelagic tunicates, such as salps, that exhibit increasingly frequent and rapid population blooms, impacting trophic dynamics and composition and human marine-dependent activities. Salp blooms are a result of their successful reproductive life history, alternating seasonally between asexual and sexual protogynous (i.e. sequential) hermaphroditic stages. While predicting future salp bloom frequency and intensity relies on an understanding of the transitions during the sexual stage from female through parturition and subsequent sex change to male, these transitions have not been explored at the molecular level. Here we report the development of the first complete genome of S. thompsoni and the North Atlantic sister species S. aspera. Genome and comparative analyses reveal an abundance of repeats and G-quadruplex (G4) motifs, a highly stable secondary structure, distributed throughout both salp genomes, a feature shared with other tunicates that perform alternating sexual-asexual reproductive strategies. Transcriptional analyses across sexual reproductive stages for S. thompsoni revealed genes associated with male sex differentiation and spermatogenesis are expressed as early as birth and before parturition, inconsistent with previous descriptions of sequential sexual differentiation in salps. Our findings suggest salp are poised for reproductive success at birth, increasing the potential for bloom formation as ocean temperatures rise.
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spelling pubmed-106869992023-11-30 Salpa genome and developmental transcriptome analyses reveal molecular flexibility enabling reproductive success in a rapidly changing environment Castellano, Kate R. Batta-Lona, Paola Bucklin, Ann O’Neill, Rachel J. Sci Rep Article Ocean warming favors pelagic tunicates, such as salps, that exhibit increasingly frequent and rapid population blooms, impacting trophic dynamics and composition and human marine-dependent activities. Salp blooms are a result of their successful reproductive life history, alternating seasonally between asexual and sexual protogynous (i.e. sequential) hermaphroditic stages. While predicting future salp bloom frequency and intensity relies on an understanding of the transitions during the sexual stage from female through parturition and subsequent sex change to male, these transitions have not been explored at the molecular level. Here we report the development of the first complete genome of S. thompsoni and the North Atlantic sister species S. aspera. Genome and comparative analyses reveal an abundance of repeats and G-quadruplex (G4) motifs, a highly stable secondary structure, distributed throughout both salp genomes, a feature shared with other tunicates that perform alternating sexual-asexual reproductive strategies. Transcriptional analyses across sexual reproductive stages for S. thompsoni revealed genes associated with male sex differentiation and spermatogenesis are expressed as early as birth and before parturition, inconsistent with previous descriptions of sequential sexual differentiation in salps. Our findings suggest salp are poised for reproductive success at birth, increasing the potential for bloom formation as ocean temperatures rise. Nature Publishing Group UK 2023-11-29 /pmc/articles/PMC10686999/ /pubmed/38030690 http://dx.doi.org/10.1038/s41598-023-47429-6 Text en © The Author(s) 2023 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
Castellano, Kate R.
Batta-Lona, Paola
Bucklin, Ann
O’Neill, Rachel J.
Salpa genome and developmental transcriptome analyses reveal molecular flexibility enabling reproductive success in a rapidly changing environment
title Salpa genome and developmental transcriptome analyses reveal molecular flexibility enabling reproductive success in a rapidly changing environment
title_full Salpa genome and developmental transcriptome analyses reveal molecular flexibility enabling reproductive success in a rapidly changing environment
title_fullStr Salpa genome and developmental transcriptome analyses reveal molecular flexibility enabling reproductive success in a rapidly changing environment
title_full_unstemmed Salpa genome and developmental transcriptome analyses reveal molecular flexibility enabling reproductive success in a rapidly changing environment
title_short Salpa genome and developmental transcriptome analyses reveal molecular flexibility enabling reproductive success in a rapidly changing environment
title_sort salpa genome and developmental transcriptome analyses reveal molecular flexibility enabling reproductive success in a rapidly changing environment
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10686999/
https://www.ncbi.nlm.nih.gov/pubmed/38030690
http://dx.doi.org/10.1038/s41598-023-47429-6
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