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Single-nucleus transcriptome inventory of giant panda reveals cellular basis for fitness optimization under low metabolism

BACKGROUND: Energy homeostasis is essential for the adaptation of animals to their environment and some wild animals keep low metabolism adaptive to their low-nutrient dietary supply. Giant panda is such a typical low-metabolic mammal exhibiting species specialization of extremely low daily energy e...

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Autores principales: Yang, Shangchen, Lan, Tianming, Wei, Rongping, Zhang, Ling, Lin, Lin, Du, Hanyu, Huang, Yunting, Zhang, Guiquan, Huang, Shan, Shi, Minhui, Wang, Chengdong, Wang, Qing, Li, Rengui, Han, Lei, Tang, Dan, Li, Haimeng, Zhang, Hemin, Cui, Jie, Lu, Haorong, Huang, Jinrong, Luo, Yonglun, Li, Desheng, Wan, Qiu-Hong, Liu, Huan, Fang, Sheng-Guo
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10588165/
https://www.ncbi.nlm.nih.gov/pubmed/37858133
http://dx.doi.org/10.1186/s12915-023-01691-2
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author Yang, Shangchen
Lan, Tianming
Wei, Rongping
Zhang, Ling
Lin, Lin
Du, Hanyu
Huang, Yunting
Zhang, Guiquan
Huang, Shan
Shi, Minhui
Wang, Chengdong
Wang, Qing
Li, Rengui
Han, Lei
Tang, Dan
Li, Haimeng
Zhang, Hemin
Cui, Jie
Lu, Haorong
Huang, Jinrong
Luo, Yonglun
Li, Desheng
Wan, Qiu-Hong
Liu, Huan
Fang, Sheng-Guo
author_facet Yang, Shangchen
Lan, Tianming
Wei, Rongping
Zhang, Ling
Lin, Lin
Du, Hanyu
Huang, Yunting
Zhang, Guiquan
Huang, Shan
Shi, Minhui
Wang, Chengdong
Wang, Qing
Li, Rengui
Han, Lei
Tang, Dan
Li, Haimeng
Zhang, Hemin
Cui, Jie
Lu, Haorong
Huang, Jinrong
Luo, Yonglun
Li, Desheng
Wan, Qiu-Hong
Liu, Huan
Fang, Sheng-Guo
author_sort Yang, Shangchen
collection PubMed
description BACKGROUND: Energy homeostasis is essential for the adaptation of animals to their environment and some wild animals keep low metabolism adaptive to their low-nutrient dietary supply. Giant panda is such a typical low-metabolic mammal exhibiting species specialization of extremely low daily energy expenditure. It has low levels of basal metabolic rate, thyroid hormone, and physical activities, whereas the cellular bases of its low metabolic adaptation remain rarely explored. RESULTS: In this study, we generate a single-nucleus transcriptome atlas of 21 organs/tissues from a female giant panda. We focused on the central metabolic organ (liver) and dissected cellular metabolic status by cross-species comparison. Adaptive expression mode (i.e., AMPK related) was prominently displayed in the hepatocyte of giant panda. In the highest energy-consuming organ, the heart, we found a possibly optimized utilization of fatty acid. Detailed cell subtype annotation of endothelial cells showed the uterine-specific deficiency of blood vascular subclasses, indicating a potential adaptation for a low reproductive energy expenditure. CONCLUSIONS: Our findings shed light on the possible cellular basis and transcriptomic regulatory clues for the low metabolism in giant pandas and helped to understand physiological adaptation response to nutrient stress. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12915-023-01691-2.
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spelling pubmed-105881652023-10-21 Single-nucleus transcriptome inventory of giant panda reveals cellular basis for fitness optimization under low metabolism Yang, Shangchen Lan, Tianming Wei, Rongping Zhang, Ling Lin, Lin Du, Hanyu Huang, Yunting Zhang, Guiquan Huang, Shan Shi, Minhui Wang, Chengdong Wang, Qing Li, Rengui Han, Lei Tang, Dan Li, Haimeng Zhang, Hemin Cui, Jie Lu, Haorong Huang, Jinrong Luo, Yonglun Li, Desheng Wan, Qiu-Hong Liu, Huan Fang, Sheng-Guo BMC Biol Research Article BACKGROUND: Energy homeostasis is essential for the adaptation of animals to their environment and some wild animals keep low metabolism adaptive to their low-nutrient dietary supply. Giant panda is such a typical low-metabolic mammal exhibiting species specialization of extremely low daily energy expenditure. It has low levels of basal metabolic rate, thyroid hormone, and physical activities, whereas the cellular bases of its low metabolic adaptation remain rarely explored. RESULTS: In this study, we generate a single-nucleus transcriptome atlas of 21 organs/tissues from a female giant panda. We focused on the central metabolic organ (liver) and dissected cellular metabolic status by cross-species comparison. Adaptive expression mode (i.e., AMPK related) was prominently displayed in the hepatocyte of giant panda. In the highest energy-consuming organ, the heart, we found a possibly optimized utilization of fatty acid. Detailed cell subtype annotation of endothelial cells showed the uterine-specific deficiency of blood vascular subclasses, indicating a potential adaptation for a low reproductive energy expenditure. CONCLUSIONS: Our findings shed light on the possible cellular basis and transcriptomic regulatory clues for the low metabolism in giant pandas and helped to understand physiological adaptation response to nutrient stress. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12915-023-01691-2. BioMed Central 2023-10-20 /pmc/articles/PMC10588165/ /pubmed/37858133 http://dx.doi.org/10.1186/s12915-023-01691-2 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/) . The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/ (https://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
Yang, Shangchen
Lan, Tianming
Wei, Rongping
Zhang, Ling
Lin, Lin
Du, Hanyu
Huang, Yunting
Zhang, Guiquan
Huang, Shan
Shi, Minhui
Wang, Chengdong
Wang, Qing
Li, Rengui
Han, Lei
Tang, Dan
Li, Haimeng
Zhang, Hemin
Cui, Jie
Lu, Haorong
Huang, Jinrong
Luo, Yonglun
Li, Desheng
Wan, Qiu-Hong
Liu, Huan
Fang, Sheng-Guo
Single-nucleus transcriptome inventory of giant panda reveals cellular basis for fitness optimization under low metabolism
title Single-nucleus transcriptome inventory of giant panda reveals cellular basis for fitness optimization under low metabolism
title_full Single-nucleus transcriptome inventory of giant panda reveals cellular basis for fitness optimization under low metabolism
title_fullStr Single-nucleus transcriptome inventory of giant panda reveals cellular basis for fitness optimization under low metabolism
title_full_unstemmed Single-nucleus transcriptome inventory of giant panda reveals cellular basis for fitness optimization under low metabolism
title_short Single-nucleus transcriptome inventory of giant panda reveals cellular basis for fitness optimization under low metabolism
title_sort single-nucleus transcriptome inventory of giant panda reveals cellular basis for fitness optimization under low metabolism
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10588165/
https://www.ncbi.nlm.nih.gov/pubmed/37858133
http://dx.doi.org/10.1186/s12915-023-01691-2
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