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Transcriptome analysis of pika heart tissue reveals mechanisms underlying the adaptation of a keystone species on the roof of the world

High-altitude environments impose intense stresses on living organisms and drive striking phenotypic and genetic adaptations, such as hypoxia resistance, cold tolerance, and increases in metabolic capacity and body mass. As one of the most successful and dominant mammals on the Qinghai-Tibetan Plate...

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Autores principales: Mu, Danping, Wu, Xinlai, Feijó, Anderson, Wu, Wei, Wen, Zhixin, Cheng, Jilong, Xia, Lin, Yang, Qisen, Shan, Wenjuan, Ge, Deyan
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9728954/
https://www.ncbi.nlm.nih.gov/pubmed/36506315
http://dx.doi.org/10.3389/fgene.2022.1020789
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author Mu, Danping
Wu, Xinlai
Feijó, Anderson
Wu, Wei
Wen, Zhixin
Cheng, Jilong
Xia, Lin
Yang, Qisen
Shan, Wenjuan
Ge, Deyan
author_facet Mu, Danping
Wu, Xinlai
Feijó, Anderson
Wu, Wei
Wen, Zhixin
Cheng, Jilong
Xia, Lin
Yang, Qisen
Shan, Wenjuan
Ge, Deyan
author_sort Mu, Danping
collection PubMed
description High-altitude environments impose intense stresses on living organisms and drive striking phenotypic and genetic adaptations, such as hypoxia resistance, cold tolerance, and increases in metabolic capacity and body mass. As one of the most successful and dominant mammals on the Qinghai-Tibetan Plateau (QHTP), the plateau pika (Ochotona curzoniae) has adapted to the extreme environments of the highest altitudes of this region and exhibits tolerance to cold and hypoxia, in contrast to closely related species that inhabit the peripheral alpine bush or forests. To explore the potential genetic mechanisms underlying the adaptation of O. curzoniae to a high-altitude environment, we sequenced the heart tissue transcriptomes of adult plateau pikas (comparing specimens from sites at two different altitudes) and Gansu pikas (O. cansus). Differential expression analysis and weighted gene co-expression network analysis (WGCNA) were used to identify differentially expressed genes (DEGs) and their primary functions. Key genes and pathways related to high-altitude adaptation were identified. In addition to the biological processes of signal transduction, energy metabolism and material transport, the identified plateau pika genes were mainly enriched in biological pathways such as the negative regulation of smooth muscle cell proliferation, the apoptosis signalling pathway, the cellular response to DNA damage stimulus, and ossification involved in bone maturation and heart development. Our results showed that the plateau pika has adapted to the extreme environments of the QHTP via protection against cardiomyopathy, tissue structure alterations and improvements in the blood circulation system and energy metabolism. These adaptations shed light on how pikas thrive on the roof of the world.
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spelling pubmed-97289542022-12-08 Transcriptome analysis of pika heart tissue reveals mechanisms underlying the adaptation of a keystone species on the roof of the world Mu, Danping Wu, Xinlai Feijó, Anderson Wu, Wei Wen, Zhixin Cheng, Jilong Xia, Lin Yang, Qisen Shan, Wenjuan Ge, Deyan Front Genet Genetics High-altitude environments impose intense stresses on living organisms and drive striking phenotypic and genetic adaptations, such as hypoxia resistance, cold tolerance, and increases in metabolic capacity and body mass. As one of the most successful and dominant mammals on the Qinghai-Tibetan Plateau (QHTP), the plateau pika (Ochotona curzoniae) has adapted to the extreme environments of the highest altitudes of this region and exhibits tolerance to cold and hypoxia, in contrast to closely related species that inhabit the peripheral alpine bush or forests. To explore the potential genetic mechanisms underlying the adaptation of O. curzoniae to a high-altitude environment, we sequenced the heart tissue transcriptomes of adult plateau pikas (comparing specimens from sites at two different altitudes) and Gansu pikas (O. cansus). Differential expression analysis and weighted gene co-expression network analysis (WGCNA) were used to identify differentially expressed genes (DEGs) and their primary functions. Key genes and pathways related to high-altitude adaptation were identified. In addition to the biological processes of signal transduction, energy metabolism and material transport, the identified plateau pika genes were mainly enriched in biological pathways such as the negative regulation of smooth muscle cell proliferation, the apoptosis signalling pathway, the cellular response to DNA damage stimulus, and ossification involved in bone maturation and heart development. Our results showed that the plateau pika has adapted to the extreme environments of the QHTP via protection against cardiomyopathy, tissue structure alterations and improvements in the blood circulation system and energy metabolism. These adaptations shed light on how pikas thrive on the roof of the world. Frontiers Media S.A. 2022-11-23 /pmc/articles/PMC9728954/ /pubmed/36506315 http://dx.doi.org/10.3389/fgene.2022.1020789 Text en Copyright © 2022 Mu, Wu, Feijó, Wu, Wen, Cheng, Xia, Yang, Shan and Ge. 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 Genetics
Mu, Danping
Wu, Xinlai
Feijó, Anderson
Wu, Wei
Wen, Zhixin
Cheng, Jilong
Xia, Lin
Yang, Qisen
Shan, Wenjuan
Ge, Deyan
Transcriptome analysis of pika heart tissue reveals mechanisms underlying the adaptation of a keystone species on the roof of the world
title Transcriptome analysis of pika heart tissue reveals mechanisms underlying the adaptation of a keystone species on the roof of the world
title_full Transcriptome analysis of pika heart tissue reveals mechanisms underlying the adaptation of a keystone species on the roof of the world
title_fullStr Transcriptome analysis of pika heart tissue reveals mechanisms underlying the adaptation of a keystone species on the roof of the world
title_full_unstemmed Transcriptome analysis of pika heart tissue reveals mechanisms underlying the adaptation of a keystone species on the roof of the world
title_short Transcriptome analysis of pika heart tissue reveals mechanisms underlying the adaptation of a keystone species on the roof of the world
title_sort transcriptome analysis of pika heart tissue reveals mechanisms underlying the adaptation of a keystone species on the roof of the world
topic Genetics
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9728954/
https://www.ncbi.nlm.nih.gov/pubmed/36506315
http://dx.doi.org/10.3389/fgene.2022.1020789
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