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Integrated analysis of transcriptome and metabolome data reveals insights for molecular mechanisms in overwintering Tibetan frogs, Nanorana parkeri

Nanorana parkeri (Anura, Dicroglossidae) is a unique frog living at high altitude on the Tibetan plateau where they must endure a long winter dormancy at low temperatures without feeding. Here, we presented a comprehensive transcriptomic and metabolomic analysis of liver tissue from summer-active ve...

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Autores principales: Niu, Yonggang, Zhang, Xuejing, Men, Shengkang, Storey, Kenneth B., Chen, Qiang
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9868574/
https://www.ncbi.nlm.nih.gov/pubmed/36699683
http://dx.doi.org/10.3389/fphys.2022.1104476
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author Niu, Yonggang
Zhang, Xuejing
Men, Shengkang
Storey, Kenneth B.
Chen, Qiang
author_facet Niu, Yonggang
Zhang, Xuejing
Men, Shengkang
Storey, Kenneth B.
Chen, Qiang
author_sort Niu, Yonggang
collection PubMed
description Nanorana parkeri (Anura, Dicroglossidae) is a unique frog living at high altitude on the Tibetan plateau where they must endure a long winter dormancy at low temperatures without feeding. Here, we presented a comprehensive transcriptomic and metabolomic analysis of liver tissue from summer-active versus overwintering N. parkeri, providing the first broad analysis of altered energy metabolism and gene expression in this frog species. We discovered that significantly up-regulated genes (2,397) in overwintering frogs mainly participated in signal transduction and immune responses, phagosome, endocytosis, lysosome, and autophagy, whereas 2,169 down-regulated genes were mainly involved in metabolic processes, such as oxidation-reduction process, amino acid metabolic process, fatty acid metabolic process, and TCA cycle. Moreover, 35 metabolites were shown to be differentially expressed, including 22 down-regulated and 13 up-regulated in winter. These included particularly notable reductions in the concentrations of most amino acids. These differentially expressed metabolites were mainly involved in amino acid biosynthesis and metabolism. To sum up, these findings suggest that gene expression and metabolic processes show adaptive regulation in overwintering N. parkeri, that contributes to maintaining homeostasis and enhancing protection in the hypometabolic state. This study has greatly expanded our understanding of the winter survival mechanisms in amphibians.
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spelling pubmed-98685742023-01-24 Integrated analysis of transcriptome and metabolome data reveals insights for molecular mechanisms in overwintering Tibetan frogs, Nanorana parkeri Niu, Yonggang Zhang, Xuejing Men, Shengkang Storey, Kenneth B. Chen, Qiang Front Physiol Physiology Nanorana parkeri (Anura, Dicroglossidae) is a unique frog living at high altitude on the Tibetan plateau where they must endure a long winter dormancy at low temperatures without feeding. Here, we presented a comprehensive transcriptomic and metabolomic analysis of liver tissue from summer-active versus overwintering N. parkeri, providing the first broad analysis of altered energy metabolism and gene expression in this frog species. We discovered that significantly up-regulated genes (2,397) in overwintering frogs mainly participated in signal transduction and immune responses, phagosome, endocytosis, lysosome, and autophagy, whereas 2,169 down-regulated genes were mainly involved in metabolic processes, such as oxidation-reduction process, amino acid metabolic process, fatty acid metabolic process, and TCA cycle. Moreover, 35 metabolites were shown to be differentially expressed, including 22 down-regulated and 13 up-regulated in winter. These included particularly notable reductions in the concentrations of most amino acids. These differentially expressed metabolites were mainly involved in amino acid biosynthesis and metabolism. To sum up, these findings suggest that gene expression and metabolic processes show adaptive regulation in overwintering N. parkeri, that contributes to maintaining homeostasis and enhancing protection in the hypometabolic state. This study has greatly expanded our understanding of the winter survival mechanisms in amphibians. Frontiers Media S.A. 2023-01-09 /pmc/articles/PMC9868574/ /pubmed/36699683 http://dx.doi.org/10.3389/fphys.2022.1104476 Text en Copyright © 2023 Niu, Zhang, Men, Storey and Chen. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Physiology
Niu, Yonggang
Zhang, Xuejing
Men, Shengkang
Storey, Kenneth B.
Chen, Qiang
Integrated analysis of transcriptome and metabolome data reveals insights for molecular mechanisms in overwintering Tibetan frogs, Nanorana parkeri
title Integrated analysis of transcriptome and metabolome data reveals insights for molecular mechanisms in overwintering Tibetan frogs, Nanorana parkeri
title_full Integrated analysis of transcriptome and metabolome data reveals insights for molecular mechanisms in overwintering Tibetan frogs, Nanorana parkeri
title_fullStr Integrated analysis of transcriptome and metabolome data reveals insights for molecular mechanisms in overwintering Tibetan frogs, Nanorana parkeri
title_full_unstemmed Integrated analysis of transcriptome and metabolome data reveals insights for molecular mechanisms in overwintering Tibetan frogs, Nanorana parkeri
title_short Integrated analysis of transcriptome and metabolome data reveals insights for molecular mechanisms in overwintering Tibetan frogs, Nanorana parkeri
title_sort integrated analysis of transcriptome and metabolome data reveals insights for molecular mechanisms in overwintering tibetan frogs, nanorana parkeri
topic Physiology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9868574/
https://www.ncbi.nlm.nih.gov/pubmed/36699683
http://dx.doi.org/10.3389/fphys.2022.1104476
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