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Gene expressions between obligate bamboo-eating pandas and non-herbivorous mammals reveal converged specialized bamboo diet adaptation

BACKGROUND: It is inevitable to change the function or expression of genes during the environmental adaption of species. Both the giant panda (Ailuropoda melanoleuca) and red panda (Ailurus fulgens) belong to Carnivora and have developed similar adaptations to the same dietary switch to bamboos at t...

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Autores principales: Ma, Jinnan, Zhang, Liang, Shen, Fujun, Geng, Yang, Huang, Yan, Wu, Honglin, Fan, Zhenxin, Hou, Rong, Song, Zhaobin, Yue, Bisong, Zhang, Xiuyue
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9843897/
https://www.ncbi.nlm.nih.gov/pubmed/36647013
http://dx.doi.org/10.1186/s12864-023-09111-z
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author Ma, Jinnan
Zhang, Liang
Shen, Fujun
Geng, Yang
Huang, Yan
Wu, Honglin
Fan, Zhenxin
Hou, Rong
Song, Zhaobin
Yue, Bisong
Zhang, Xiuyue
author_facet Ma, Jinnan
Zhang, Liang
Shen, Fujun
Geng, Yang
Huang, Yan
Wu, Honglin
Fan, Zhenxin
Hou, Rong
Song, Zhaobin
Yue, Bisong
Zhang, Xiuyue
author_sort Ma, Jinnan
collection PubMed
description BACKGROUND: It is inevitable to change the function or expression of genes during the environmental adaption of species. Both the giant panda (Ailuropoda melanoleuca) and red panda (Ailurus fulgens) belong to Carnivora and have developed similar adaptations to the same dietary switch to bamboos at the morphological and genomic levels. However, the genetic adaptation at the gene expression level is unclear. Therefore, we aimed to examine the gene expression patterns of giant and red panda convergent specialized bamboo-diets. We examined differences in liver and pancreas transcriptomes between the two panda species and other non-herbivorous species. RESULTS: The clustering and PCA plots suggested that the specialized bamboo diet may drive similar expression shifts in these two species of pandas. Therefore, we focused on shared liver and pancreas DEGs (differentially expressed genes) in the giant and red panda relative to other non-herbivorous species. Genetic convergence occurred at multiple levels spanning carbohydrate metabolism, lipid metabolism, and lysine degradation. The shared adaptive convergence DEGs in both organs probably be an evolutionary response to the high carbohydrate, low lipid and lysine bamboo diet. Convergent expression of those nutrient metabolism-related genes in both pandas was an intricate process and subjected to multi-level regulation, including DNA methylation and transcription factor. A large number of lysine degradation and lipid metabolism related genes were hypermethylated in promoter regions in the red panda. Most genes related to carbohydrate metabolism had reduced DNA methylation with increased mRNA expression in giant pandas. Unlike the red panda, the core gene of the lysine degradation pathway (AASS) doesn’t exhibit hypermethylation modification in the giant panda, and dual-luciferase reporter assay showed that transcription factor, NR3C1, functions as a transcriptional activator in AASS transcription through the binding to AASS promoter region. CONCLUSIONS: Our results revealed the adaptive expressions and regulations of the metabolism-related genes responding to the unique nutrients in bamboo food and provided data accumulation and research hints for the future revelation of complex mechanism of two pandas underlying convergent adaptation to a specialized bamboo diet. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12864-023-09111-z.
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spelling pubmed-98438972023-01-18 Gene expressions between obligate bamboo-eating pandas and non-herbivorous mammals reveal converged specialized bamboo diet adaptation Ma, Jinnan Zhang, Liang Shen, Fujun Geng, Yang Huang, Yan Wu, Honglin Fan, Zhenxin Hou, Rong Song, Zhaobin Yue, Bisong Zhang, Xiuyue BMC Genomics Research BACKGROUND: It is inevitable to change the function or expression of genes during the environmental adaption of species. Both the giant panda (Ailuropoda melanoleuca) and red panda (Ailurus fulgens) belong to Carnivora and have developed similar adaptations to the same dietary switch to bamboos at the morphological and genomic levels. However, the genetic adaptation at the gene expression level is unclear. Therefore, we aimed to examine the gene expression patterns of giant and red panda convergent specialized bamboo-diets. We examined differences in liver and pancreas transcriptomes between the two panda species and other non-herbivorous species. RESULTS: The clustering and PCA plots suggested that the specialized bamboo diet may drive similar expression shifts in these two species of pandas. Therefore, we focused on shared liver and pancreas DEGs (differentially expressed genes) in the giant and red panda relative to other non-herbivorous species. Genetic convergence occurred at multiple levels spanning carbohydrate metabolism, lipid metabolism, and lysine degradation. The shared adaptive convergence DEGs in both organs probably be an evolutionary response to the high carbohydrate, low lipid and lysine bamboo diet. Convergent expression of those nutrient metabolism-related genes in both pandas was an intricate process and subjected to multi-level regulation, including DNA methylation and transcription factor. A large number of lysine degradation and lipid metabolism related genes were hypermethylated in promoter regions in the red panda. Most genes related to carbohydrate metabolism had reduced DNA methylation with increased mRNA expression in giant pandas. Unlike the red panda, the core gene of the lysine degradation pathway (AASS) doesn’t exhibit hypermethylation modification in the giant panda, and dual-luciferase reporter assay showed that transcription factor, NR3C1, functions as a transcriptional activator in AASS transcription through the binding to AASS promoter region. CONCLUSIONS: Our results revealed the adaptive expressions and regulations of the metabolism-related genes responding to the unique nutrients in bamboo food and provided data accumulation and research hints for the future revelation of complex mechanism of two pandas underlying convergent adaptation to a specialized bamboo diet. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12864-023-09111-z. BioMed Central 2023-01-16 /pmc/articles/PMC9843897/ /pubmed/36647013 http://dx.doi.org/10.1186/s12864-023-09111-z Text en © The Author(s) 2023 https://creativecommons.org/licenses/by/4.0/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/ (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
Ma, Jinnan
Zhang, Liang
Shen, Fujun
Geng, Yang
Huang, Yan
Wu, Honglin
Fan, Zhenxin
Hou, Rong
Song, Zhaobin
Yue, Bisong
Zhang, Xiuyue
Gene expressions between obligate bamboo-eating pandas and non-herbivorous mammals reveal converged specialized bamboo diet adaptation
title Gene expressions between obligate bamboo-eating pandas and non-herbivorous mammals reveal converged specialized bamboo diet adaptation
title_full Gene expressions between obligate bamboo-eating pandas and non-herbivorous mammals reveal converged specialized bamboo diet adaptation
title_fullStr Gene expressions between obligate bamboo-eating pandas and non-herbivorous mammals reveal converged specialized bamboo diet adaptation
title_full_unstemmed Gene expressions between obligate bamboo-eating pandas and non-herbivorous mammals reveal converged specialized bamboo diet adaptation
title_short Gene expressions between obligate bamboo-eating pandas and non-herbivorous mammals reveal converged specialized bamboo diet adaptation
title_sort gene expressions between obligate bamboo-eating pandas and non-herbivorous mammals reveal converged specialized bamboo diet adaptation
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9843897/
https://www.ncbi.nlm.nih.gov/pubmed/36647013
http://dx.doi.org/10.1186/s12864-023-09111-z
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