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microRNA profiling in the Weddell seal suggests novel regulatory mechanisms contributing to diving adaptation

BACKGROUND: The Weddell Seal (Leptonychotes weddelli) represents a remarkable example of adaptation to diving among marine mammals. This species is capable of diving > 900 m deep and remaining underwater for more than 60 min. A number of key physiological specializations have been identified, inc...

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Autores principales: Penso-Dolfin, Luca, Haerty, Wilfried, Hindle, Allyson, Di Palma, Federica
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7158035/
https://www.ncbi.nlm.nih.gov/pubmed/32293246
http://dx.doi.org/10.1186/s12864-020-6675-0
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author Penso-Dolfin, Luca
Haerty, Wilfried
Hindle, Allyson
Di Palma, Federica
author_facet Penso-Dolfin, Luca
Haerty, Wilfried
Hindle, Allyson
Di Palma, Federica
author_sort Penso-Dolfin, Luca
collection PubMed
description BACKGROUND: The Weddell Seal (Leptonychotes weddelli) represents a remarkable example of adaptation to diving among marine mammals. This species is capable of diving > 900 m deep and remaining underwater for more than 60 min. A number of key physiological specializations have been identified, including the low levels of aerobic, lipid-based metabolism under hypoxia, significant increase in oxygen storage in blood and muscle; high blood volume and extreme cardiovascular control. These adaptations have been linked to increased abundance of key proteins, suggesting an important, yet still understudied role for gene reprogramming. In this study, we investigate the possibility that post-transcriptional gene regulation by microRNAs (miRNAs) has contributed to the adaptive evolution of diving capacities in the Weddell Seal. RESULTS: Using small RNA data across 4 tissues (brain, heart, muscle and plasma), in 3 biological replicates, we generate the first miRNA annotation in this species, consisting of 559 high confidence, manually curated miRNA loci. Evolutionary analyses of miRNA gain and loss highlight a high number of Weddell seal specific miRNAs. Four hundred sixteen miRNAs were differentially expressed (DE) among tissues, whereas 80 miRNAs were differentially expressed (DE) across all tissues between pups and adults and age differences for specific tissues were detected in 188 miRNAs. mRNA targets of these altered miRNAs identify possible protective mechanisms in individual tissues, particularly relevant to hypoxia tolerance, anti-apoptotic pathways, and nitric oxide signal transduction. Novel, lineage-specific miRNAs associated with developmental changes target genes with roles in angiogenesis and vasoregulatory signaling. CONCLUSIONS: Altogether, we provide an overview of miRNA composition and evolution in the Weddell seal, and the first insights into their possible role in the specialization to diving.
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spelling pubmed-71580352020-04-20 microRNA profiling in the Weddell seal suggests novel regulatory mechanisms contributing to diving adaptation Penso-Dolfin, Luca Haerty, Wilfried Hindle, Allyson Di Palma, Federica BMC Genomics Research Article BACKGROUND: The Weddell Seal (Leptonychotes weddelli) represents a remarkable example of adaptation to diving among marine mammals. This species is capable of diving > 900 m deep and remaining underwater for more than 60 min. A number of key physiological specializations have been identified, including the low levels of aerobic, lipid-based metabolism under hypoxia, significant increase in oxygen storage in blood and muscle; high blood volume and extreme cardiovascular control. These adaptations have been linked to increased abundance of key proteins, suggesting an important, yet still understudied role for gene reprogramming. In this study, we investigate the possibility that post-transcriptional gene regulation by microRNAs (miRNAs) has contributed to the adaptive evolution of diving capacities in the Weddell Seal. RESULTS: Using small RNA data across 4 tissues (brain, heart, muscle and plasma), in 3 biological replicates, we generate the first miRNA annotation in this species, consisting of 559 high confidence, manually curated miRNA loci. Evolutionary analyses of miRNA gain and loss highlight a high number of Weddell seal specific miRNAs. Four hundred sixteen miRNAs were differentially expressed (DE) among tissues, whereas 80 miRNAs were differentially expressed (DE) across all tissues between pups and adults and age differences for specific tissues were detected in 188 miRNAs. mRNA targets of these altered miRNAs identify possible protective mechanisms in individual tissues, particularly relevant to hypoxia tolerance, anti-apoptotic pathways, and nitric oxide signal transduction. Novel, lineage-specific miRNAs associated with developmental changes target genes with roles in angiogenesis and vasoregulatory signaling. CONCLUSIONS: Altogether, we provide an overview of miRNA composition and evolution in the Weddell seal, and the first insights into their possible role in the specialization to diving. BioMed Central 2020-04-15 /pmc/articles/PMC7158035/ /pubmed/32293246 http://dx.doi.org/10.1186/s12864-020-6675-0 Text en © The Author(s). 2020 Open AccessThis 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/. 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 in a credit line to the data.
spellingShingle Research Article
Penso-Dolfin, Luca
Haerty, Wilfried
Hindle, Allyson
Di Palma, Federica
microRNA profiling in the Weddell seal suggests novel regulatory mechanisms contributing to diving adaptation
title microRNA profiling in the Weddell seal suggests novel regulatory mechanisms contributing to diving adaptation
title_full microRNA profiling in the Weddell seal suggests novel regulatory mechanisms contributing to diving adaptation
title_fullStr microRNA profiling in the Weddell seal suggests novel regulatory mechanisms contributing to diving adaptation
title_full_unstemmed microRNA profiling in the Weddell seal suggests novel regulatory mechanisms contributing to diving adaptation
title_short microRNA profiling in the Weddell seal suggests novel regulatory mechanisms contributing to diving adaptation
title_sort microrna profiling in the weddell seal suggests novel regulatory mechanisms contributing to diving adaptation
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7158035/
https://www.ncbi.nlm.nih.gov/pubmed/32293246
http://dx.doi.org/10.1186/s12864-020-6675-0
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