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Comparative transcriptomic analysis delineates adaptation strategies of Rana kukunoris toward cold stress on the Qinghai-Tibet Plateau
Cold hardiness is fundamental for amphibians to survive during the extremely cold winter on the Qinghai-Tibet plateau. Exploring the gene regulation mechanism of freezing-tolerant Rana kukunoris could help us to understand how the frogs survive in winter. Transcriptome of liver and muscle of R. kuku...
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Published in: | BMC genomics 2024-04, Vol.25 (1), p.363-363, Article 363 |
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description | Cold hardiness is fundamental for amphibians to survive during the extremely cold winter on the Qinghai-Tibet plateau. Exploring the gene regulation mechanism of freezing-tolerant Rana kukunoris could help us to understand how the frogs survive in winter.
Transcriptome of liver and muscle of R. kukunoris collected in hibernation and spring were assisted by single molecule real-time (SMRT) sequencing technology. A total of 10,062 unigenes of R. kukunoris were obtained, and 9,924 coding sequences (CDS) were successfully annotated. Our examination of the mRNA response to whole body freezing and recover in the frogs revealed key genes concerning underlying antifreeze proteins and cryoprotectants (glucose and urea). Functional pathway analyses revealed differential regulated pathways of ribosome, energy supply, and protein metabolism which displayed a freeze-induced response and damage recover. Genes related to energy supply in the muscle of winter frogs were up-regulated compared with the muscle of spring frogs. The liver of hibernating frogs maintained modest levels of protein synthesis in the winter. In contrast, the liver underwent intensive high levels of protein synthesis and lipid catabolism to produce substantial quantity of fresh proteins and energy in spring. Differences between hibernation and spring were smaller than that between tissues, yet the physiological traits of hibernation were nevertheless passed down to active state in spring.
Based on our comparative transcriptomic analyses, we revealed the likely adaptive mechanisms of R. kukunoris. Ultimately, our study expands genetic resources for the freezing-tolerant frogs. |
doi_str_mv | 10.1186/s12864-024-10248-8 |
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Transcriptome of liver and muscle of R. kukunoris collected in hibernation and spring were assisted by single molecule real-time (SMRT) sequencing technology. A total of 10,062 unigenes of R. kukunoris were obtained, and 9,924 coding sequences (CDS) were successfully annotated. Our examination of the mRNA response to whole body freezing and recover in the frogs revealed key genes concerning underlying antifreeze proteins and cryoprotectants (glucose and urea). Functional pathway analyses revealed differential regulated pathways of ribosome, energy supply, and protein metabolism which displayed a freeze-induced response and damage recover. Genes related to energy supply in the muscle of winter frogs were up-regulated compared with the muscle of spring frogs. The liver of hibernating frogs maintained modest levels of protein synthesis in the winter. In contrast, the liver underwent intensive high levels of protein synthesis and lipid catabolism to produce substantial quantity of fresh proteins and energy in spring. Differences between hibernation and spring were smaller than that between tissues, yet the physiological traits of hibernation were nevertheless passed down to active state in spring.
Based on our comparative transcriptomic analyses, we revealed the likely adaptive mechanisms of R. kukunoris. Ultimately, our study expands genetic resources for the freezing-tolerant frogs.</description><identifier>ISSN: 1471-2164</identifier><identifier>EISSN: 1471-2164</identifier><identifier>DOI: 10.1186/s12864-024-10248-8</identifier><identifier>PMID: 38609871</identifier><language>eng</language><publisher>England: BioMed Central Ltd</publisher><subject>Amino acids ; Amphibians ; Analysis ; Animals ; Antifreeze proteins ; Antifreezes ; Anura ; Aquatic reptiles ; Catabolism ; Cold ; Cold hardiness ; Cold tolerance ; Cold-Shock Response - genetics ; Cryoprotectants ; Cryoprotectors ; Dextrose ; Emergence period ; Energy ; Energy metabolism ; Enzymes ; Freeze exposure ; Freezing ; Frogs ; Gene expression ; Gene Expression Profiling ; Gene regulation ; Genes ; Genetic resources ; Glucose ; Hibernation ; Invertebrates ; Lipid metabolism ; Lipids ; Liver ; Methods ; Muscle ; Muscles ; Pacbio sequel ; Physiology ; Protein biosynthesis ; Protein metabolism ; Protein synthesis ; Protein turnover ; Proteins ; Rana kukunoris ; Ranidae - genetics ; Reptiles & amphibians ; Ribosomes ; RNA ; SMRT protein ; Spring ; Survival ; Temperature ; Tibet ; Transcriptome ; Transcriptomes ; Transcriptomics ; Urea ; Winter ; Yeast</subject><ispartof>BMC genomics, 2024-04, Vol.25 (1), p.363-363, Article 363</ispartof><rights>2024. The Author(s).</rights><rights>COPYRIGHT 2024 BioMed Central Ltd.</rights><rights>2024. This work is licensed under http://creativecommons.org/licenses/by/4.0/ (the “License”). Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><cites>FETCH-LOGICAL-c493t-c255006fe548fe1c33b4540f424a49446bbb4ad6fd9473f45a122863ee168e733</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktohtml>$$Uhttps://www.proquest.com/docview/3037855380?pq-origsite=primo$$EHTML$$P50$$Gproquest$$Hfree_for_read</linktohtml><link.rule.ids>314,780,784,25753,27924,27925,37012,37013,44590</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/38609871$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Zhang, Tao</creatorcontrib><creatorcontrib>Jia, Lun</creatorcontrib><creatorcontrib>Niu, Zhiyi</creatorcontrib><creatorcontrib>Li, Xinying</creatorcontrib><creatorcontrib>Men, Shengkang</creatorcontrib><creatorcontrib>Jiang, Lu</creatorcontrib><creatorcontrib>Ma, Miaojun</creatorcontrib><creatorcontrib>Wang, Huihui</creatorcontrib><creatorcontrib>Tang, Xiaolong</creatorcontrib><creatorcontrib>Chen, Qiang</creatorcontrib><title>Comparative transcriptomic analysis delineates adaptation strategies of Rana kukunoris toward cold stress on the Qinghai-Tibet Plateau</title><title>BMC genomics</title><addtitle>BMC Genomics</addtitle><description>Cold hardiness is fundamental for amphibians to survive during the extremely cold winter on the Qinghai-Tibet plateau. Exploring the gene regulation mechanism of freezing-tolerant Rana kukunoris could help us to understand how the frogs survive in winter.
Transcriptome of liver and muscle of R. kukunoris collected in hibernation and spring were assisted by single molecule real-time (SMRT) sequencing technology. A total of 10,062 unigenes of R. kukunoris were obtained, and 9,924 coding sequences (CDS) were successfully annotated. Our examination of the mRNA response to whole body freezing and recover in the frogs revealed key genes concerning underlying antifreeze proteins and cryoprotectants (glucose and urea). Functional pathway analyses revealed differential regulated pathways of ribosome, energy supply, and protein metabolism which displayed a freeze-induced response and damage recover. Genes related to energy supply in the muscle of winter frogs were up-regulated compared with the muscle of spring frogs. The liver of hibernating frogs maintained modest levels of protein synthesis in the winter. In contrast, the liver underwent intensive high levels of protein synthesis and lipid catabolism to produce substantial quantity of fresh proteins and energy in spring. Differences between hibernation and spring were smaller than that between tissues, yet the physiological traits of hibernation were nevertheless passed down to active state in spring.
Based on our comparative transcriptomic analyses, we revealed the likely adaptive mechanisms of R. kukunoris. Ultimately, our study expands genetic resources for the freezing-tolerant frogs.</description><subject>Amino acids</subject><subject>Amphibians</subject><subject>Analysis</subject><subject>Animals</subject><subject>Antifreeze proteins</subject><subject>Antifreezes</subject><subject>Anura</subject><subject>Aquatic reptiles</subject><subject>Catabolism</subject><subject>Cold</subject><subject>Cold hardiness</subject><subject>Cold tolerance</subject><subject>Cold-Shock Response - genetics</subject><subject>Cryoprotectants</subject><subject>Cryoprotectors</subject><subject>Dextrose</subject><subject>Emergence period</subject><subject>Energy</subject><subject>Energy metabolism</subject><subject>Enzymes</subject><subject>Freeze exposure</subject><subject>Freezing</subject><subject>Frogs</subject><subject>Gene expression</subject><subject>Gene Expression Profiling</subject><subject>Gene regulation</subject><subject>Genes</subject><subject>Genetic resources</subject><subject>Glucose</subject><subject>Hibernation</subject><subject>Invertebrates</subject><subject>Lipid metabolism</subject><subject>Lipids</subject><subject>Liver</subject><subject>Methods</subject><subject>Muscle</subject><subject>Muscles</subject><subject>Pacbio sequel</subject><subject>Physiology</subject><subject>Protein biosynthesis</subject><subject>Protein metabolism</subject><subject>Protein synthesis</subject><subject>Protein turnover</subject><subject>Proteins</subject><subject>Rana kukunoris</subject><subject>Ranidae - genetics</subject><subject>Reptiles & amphibians</subject><subject>Ribosomes</subject><subject>RNA</subject><subject>SMRT protein</subject><subject>Spring</subject><subject>Survival</subject><subject>Temperature</subject><subject>Tibet</subject><subject>Transcriptome</subject><subject>Transcriptomes</subject><subject>Transcriptomics</subject><subject>Urea</subject><subject>Winter</subject><subject>Yeast</subject><issn>1471-2164</issn><issn>1471-2164</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2024</creationdate><recordtype>article</recordtype><sourceid>PIMPY</sourceid><sourceid>DOA</sourceid><recordid>eNptkt1u1DAQhSMEoqXwAlygSNzARYr_EjuX1arASpWAUq6tiTPeepuNF9sB-gI8N85uKSxClmxr9J0z8vgUxXNKTilVzZtImWpERZioaN5UpR4Ux1RIWjHaiId_3Y-KJzGuCaFSsfpxccRVQ1ol6XHxc-E3WwiQ3DcsU4AxmuC2yW-cKWGE4Ta6WPY4uBEhYSyhh23KtB_LmPGEK5er3paXmS5vpptp9CFLkv8OoS-NH_oZxJihsUzXWH5y4-oaXHXlOkzlxyF7wPS0eGRhiPjs7jwpvrw9v1q8ry4-vFsuzi4qI1qeKsPqmpDGYi2URWo470QtiBVMgGiFaLquE9A3tm-F5FbUQFmeEUekjULJ-Umx3Pv2HtZ6G9wGwq324PSu4MNKQ0jODKiBd7RlING2VPQCgUsmJbStIgyEsdnr1d5rG_zXCWPSGxcNDgOM6KeoOeFK8JY0c9uX_6BrP4U83h0lVV1zRf5QK8j93Wh9nrCZTfWZVO28Wpmp0_9QefWYP82PaF2uHwheHwgyk_BHWsEUo15-vjxk2Z41wccY0N7PiBI9h07vQ6dz3vQudFpl0Yu7103dBvt7ye-U8V-iKdFO</recordid><startdate>20240412</startdate><enddate>20240412</enddate><creator>Zhang, Tao</creator><creator>Jia, Lun</creator><creator>Niu, Zhiyi</creator><creator>Li, Xinying</creator><creator>Men, Shengkang</creator><creator>Jiang, Lu</creator><creator>Ma, Miaojun</creator><creator>Wang, Huihui</creator><creator>Tang, Xiaolong</creator><creator>Chen, Qiang</creator><general>BioMed Central Ltd</general><general>BioMed Central</general><general>BMC</general><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>ISR</scope><scope>3V.</scope><scope>7QP</scope><scope>7QR</scope><scope>7SS</scope><scope>7TK</scope><scope>7U7</scope><scope>7X7</scope><scope>7XB</scope><scope>88E</scope><scope>8AO</scope><scope>8FD</scope><scope>8FE</scope><scope>8FH</scope><scope>8FI</scope><scope>8FJ</scope><scope>8FK</scope><scope>ABUWG</scope><scope>AFKRA</scope><scope>AZQEC</scope><scope>BBNVY</scope><scope>BENPR</scope><scope>BHPHI</scope><scope>C1K</scope><scope>CCPQU</scope><scope>DWQXO</scope><scope>FR3</scope><scope>FYUFA</scope><scope>GHDGH</scope><scope>GNUQQ</scope><scope>HCIFZ</scope><scope>K9.</scope><scope>LK8</scope><scope>M0S</scope><scope>M1P</scope><scope>M7P</scope><scope>P64</scope><scope>PIMPY</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>PRINS</scope><scope>RC3</scope><scope>7X8</scope><scope>DOA</scope></search><sort><creationdate>20240412</creationdate><title>Comparative transcriptomic analysis delineates adaptation strategies of Rana kukunoris toward cold stress on the Qinghai-Tibet Plateau</title><author>Zhang, Tao ; Jia, Lun ; Niu, Zhiyi ; Li, Xinying ; Men, Shengkang ; Jiang, Lu ; Ma, Miaojun ; Wang, Huihui ; Tang, Xiaolong ; Chen, Qiang</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c493t-c255006fe548fe1c33b4540f424a49446bbb4ad6fd9473f45a122863ee168e733</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2024</creationdate><topic>Amino acids</topic><topic>Amphibians</topic><topic>Analysis</topic><topic>Animals</topic><topic>Antifreeze proteins</topic><topic>Antifreezes</topic><topic>Anura</topic><topic>Aquatic reptiles</topic><topic>Catabolism</topic><topic>Cold</topic><topic>Cold hardiness</topic><topic>Cold tolerance</topic><topic>Cold-Shock Response - genetics</topic><topic>Cryoprotectants</topic><topic>Cryoprotectors</topic><topic>Dextrose</topic><topic>Emergence period</topic><topic>Energy</topic><topic>Energy metabolism</topic><topic>Enzymes</topic><topic>Freeze exposure</topic><topic>Freezing</topic><topic>Frogs</topic><topic>Gene expression</topic><topic>Gene Expression Profiling</topic><topic>Gene regulation</topic><topic>Genes</topic><topic>Genetic resources</topic><topic>Glucose</topic><topic>Hibernation</topic><topic>Invertebrates</topic><topic>Lipid metabolism</topic><topic>Lipids</topic><topic>Liver</topic><topic>Methods</topic><topic>Muscle</topic><topic>Muscles</topic><topic>Pacbio sequel</topic><topic>Physiology</topic><topic>Protein biosynthesis</topic><topic>Protein metabolism</topic><topic>Protein synthesis</topic><topic>Protein turnover</topic><topic>Proteins</topic><topic>Rana kukunoris</topic><topic>Ranidae - genetics</topic><topic>Reptiles & amphibians</topic><topic>Ribosomes</topic><topic>RNA</topic><topic>SMRT protein</topic><topic>Spring</topic><topic>Survival</topic><topic>Temperature</topic><topic>Tibet</topic><topic>Transcriptome</topic><topic>Transcriptomes</topic><topic>Transcriptomics</topic><topic>Urea</topic><topic>Winter</topic><topic>Yeast</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Zhang, Tao</creatorcontrib><creatorcontrib>Jia, Lun</creatorcontrib><creatorcontrib>Niu, Zhiyi</creatorcontrib><creatorcontrib>Li, Xinying</creatorcontrib><creatorcontrib>Men, Shengkang</creatorcontrib><creatorcontrib>Jiang, Lu</creatorcontrib><creatorcontrib>Ma, Miaojun</creatorcontrib><creatorcontrib>Wang, Huihui</creatorcontrib><creatorcontrib>Tang, Xiaolong</creatorcontrib><creatorcontrib>Chen, Qiang</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Gale In Context: Science</collection><collection>ProQuest Central (Corporate)</collection><collection>Calcium & Calcified Tissue Abstracts</collection><collection>Chemoreception Abstracts</collection><collection>Entomology Abstracts (Full archive)</collection><collection>Neurosciences Abstracts</collection><collection>Toxicology Abstracts</collection><collection>Health & Medical Collection</collection><collection>ProQuest Central (purchase pre-March 2016)</collection><collection>Medical Database (Alumni Edition)</collection><collection>ProQuest Pharma Collection</collection><collection>Technology Research Database</collection><collection>ProQuest SciTech Collection</collection><collection>ProQuest Natural Science Collection</collection><collection>Hospital Premium Collection</collection><collection>Hospital Premium Collection (Alumni Edition)</collection><collection>ProQuest Central (Alumni) (purchase pre-March 2016)</collection><collection>ProQuest Central (Alumni)</collection><collection>ProQuest Central UK/Ireland</collection><collection>ProQuest Central Essentials</collection><collection>Biological Science Collection</collection><collection>ProQuest Central</collection><collection>ProQuest Natural Science Collection</collection><collection>Environmental Sciences and Pollution Management</collection><collection>ProQuest One Community College</collection><collection>ProQuest Central</collection><collection>Engineering Research Database</collection><collection>Health Research Premium Collection</collection><collection>Health Research Premium Collection (Alumni)</collection><collection>ProQuest Central Student</collection><collection>SciTech Premium Collection</collection><collection>ProQuest Health & Medical Complete (Alumni)</collection><collection>ProQuest Biological Science Collection</collection><collection>Health & Medical Collection (Alumni Edition)</collection><collection>Medical Database</collection><collection>ProQuest Biological Science Journals</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Publicly Available Content Database</collection><collection>ProQuest One Academic Eastern Edition (DO NOT USE)</collection><collection>ProQuest One Academic</collection><collection>ProQuest One Academic UKI Edition</collection><collection>ProQuest Central China</collection><collection>Genetics Abstracts</collection><collection>MEDLINE - Academic</collection><collection>DOAJ Directory of Open Access Journals</collection><jtitle>BMC genomics</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Zhang, Tao</au><au>Jia, Lun</au><au>Niu, Zhiyi</au><au>Li, Xinying</au><au>Men, Shengkang</au><au>Jiang, Lu</au><au>Ma, Miaojun</au><au>Wang, Huihui</au><au>Tang, Xiaolong</au><au>Chen, Qiang</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Comparative transcriptomic analysis delineates adaptation strategies of Rana kukunoris toward cold stress on the Qinghai-Tibet Plateau</atitle><jtitle>BMC genomics</jtitle><addtitle>BMC Genomics</addtitle><date>2024-04-12</date><risdate>2024</risdate><volume>25</volume><issue>1</issue><spage>363</spage><epage>363</epage><pages>363-363</pages><artnum>363</artnum><issn>1471-2164</issn><eissn>1471-2164</eissn><abstract>Cold hardiness is fundamental for amphibians to survive during the extremely cold winter on the Qinghai-Tibet plateau. Exploring the gene regulation mechanism of freezing-tolerant Rana kukunoris could help us to understand how the frogs survive in winter.
Transcriptome of liver and muscle of R. kukunoris collected in hibernation and spring were assisted by single molecule real-time (SMRT) sequencing technology. A total of 10,062 unigenes of R. kukunoris were obtained, and 9,924 coding sequences (CDS) were successfully annotated. Our examination of the mRNA response to whole body freezing and recover in the frogs revealed key genes concerning underlying antifreeze proteins and cryoprotectants (glucose and urea). Functional pathway analyses revealed differential regulated pathways of ribosome, energy supply, and protein metabolism which displayed a freeze-induced response and damage recover. Genes related to energy supply in the muscle of winter frogs were up-regulated compared with the muscle of spring frogs. The liver of hibernating frogs maintained modest levels of protein synthesis in the winter. In contrast, the liver underwent intensive high levels of protein synthesis and lipid catabolism to produce substantial quantity of fresh proteins and energy in spring. Differences between hibernation and spring were smaller than that between tissues, yet the physiological traits of hibernation were nevertheless passed down to active state in spring.
Based on our comparative transcriptomic analyses, we revealed the likely adaptive mechanisms of R. kukunoris. Ultimately, our study expands genetic resources for the freezing-tolerant frogs.</abstract><cop>England</cop><pub>BioMed Central Ltd</pub><pmid>38609871</pmid><doi>10.1186/s12864-024-10248-8</doi><tpages>1</tpages><oa>free_for_read</oa></addata></record> |
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subjects | Amino acids Amphibians Analysis Animals Antifreeze proteins Antifreezes Anura Aquatic reptiles Catabolism Cold Cold hardiness Cold tolerance Cold-Shock Response - genetics Cryoprotectants Cryoprotectors Dextrose Emergence period Energy Energy metabolism Enzymes Freeze exposure Freezing Frogs Gene expression Gene Expression Profiling Gene regulation Genes Genetic resources Glucose Hibernation Invertebrates Lipid metabolism Lipids Liver Methods Muscle Muscles Pacbio sequel Physiology Protein biosynthesis Protein metabolism Protein synthesis Protein turnover Proteins Rana kukunoris Ranidae - genetics Reptiles & amphibians Ribosomes RNA SMRT protein Spring Survival Temperature Tibet Transcriptome Transcriptomes Transcriptomics Urea Winter Yeast |
title | Comparative transcriptomic analysis delineates adaptation strategies of Rana kukunoris toward cold stress on the Qinghai-Tibet Plateau |
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