Comparative Analysis of Heat Exposure-Induced Molecular Changes in Two Turtle Species with Contrasting Thermal Adaptations

Jian Hong , Yangchun Gao , Jiaxuan Li , Yan Ge , Yufeng Wei , Youqiang Yin , Qianru Liang , Shiping Gong

Integrative Zoology ›› 2026, Vol. 21 ›› Issue (3) : 609 -623.

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Integrative Zoology ›› 2026, Vol. 21 ›› Issue (3) :609 -623. DOI: 10.1111/1749-4877.13011
ORIGINAL ARTICLE
Comparative Analysis of Heat Exposure-Induced Molecular Changes in Two Turtle Species with Contrasting Thermal Adaptations
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Abstract

Global climate change has heightened heat stress, threatening amphibian and reptile survival, including turtles. Although turtle species vary in heat tolerance, the molecular mechanisms behind these differences are not well understood. This study aimed to identify differentially expressed genes (DEGs) in response to heat stress (32°C) versus normal temperature (25°C) in eight tissues (brain, heart, intestine, liver, lung, muscle, spleen, and stomach) of two turtle species: Platysternon megacephalum (low heat tolerance) and Trachemys scripta elegans (high heat tolerance) using RNA-seq. The results revealed significant down-regulation of genes involved in energy and lipid metabolism in P. megacephalum, suggesting metabolic suppression under heat stress. Furthermore, the jumonji and AT-rich interaction domain containing 2 (JARID2) gene, which regulates cell proliferation and differentiation, was up-regulated in all tissues of P. megacephalum but down-regulated in all tissues of T. scripta elegans under heat stress. Pathway analysis revealed that protein processing in the endoplasmic reticulum was significantly enriched in brain, heart, lung, and muscle tissues of P. megacephalum, with BiP, CHOP, NEF, and HSPs significantly up-regulated in brain tissue, highlighting this pathway's impact on heat stress response. Seven hub genes were identified in the protein processing in the endoplasmic reticulum pathway in P. megacephalum. In contrast, T. scripta elegans showed a moderate response, with up-regulation of ribosomal genes in the brain to enhance protein synthesis and folding, while down-regulation of cell cycle genes in the intestine helped conserve energy for cellular repair. No significant pathways were found in other tissues of T. scripta elegans. These molecular responses in T. scripta elegans likely contribute to its better adaptation to heat stress. This study provides new insights into the molecular mechanisms of heat stress adaptation in turtles, offering valuable knowledge for understanding their ability to cope with future climate change.

Keywords

endoplasmic reticulum / heat stress / Platysternon megacephalum / Trachemys scripta elegans / transcriptomic analysis

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Jian Hong, Yangchun Gao, Jiaxuan Li, Yan Ge, Yufeng Wei, Youqiang Yin, Qianru Liang, Shiping Gong. Comparative Analysis of Heat Exposure-Induced Molecular Changes in Two Turtle Species with Contrasting Thermal Adaptations. Integrative Zoology, 2026, 21 (3) : 609-623 DOI:10.1111/1749-4877.13011

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References

[1]

Akashi, H. D., A. Cádiz Díaz, S. Shigenobu, T. Makino, and M. Kawata. 2016. “Differentially Expressed Genes Associated with Adaptation to Different Thermal Environments in Three Sympatric Cuban Anolis Lizards.” Molecular Ecology 25: 2273–2285.

[2]

Alexa, A., and J. Rahnenführer. 2009. “Gene Set Enrichment Analysis with topGO.” Bioconductor Improv 27: 1–26.

[3]

Bánhegyi, G., P. Baumeister, A. Benedetti, et al. 2007. “Endoplasmic Reticulum Stress.” Annals of the New York Academy of Sciences 1113: 58–71.

[4]

Barbarossa, V., J. Bosmans, N. Wanders, et al. 2021. “Threats of Global Warming to the World's Freshwater Fishes.” Nature Communications 12: 1701.

[5]

Bentley, B. P., B. J. Haas, J. N. Tedeschi, and O. Berry. 2017. “Loggerhead Sea Turtle Embryos (Caretta caretta) Regulate Expression of Stress Response and Developmental Genes When Exposed to a Biologically Realistic Heat Stress.” Molecular Ecology 26: 2978–2992.

[6]

Bhagarathi, L. K., P. N. B. Da Silva, F. Pestano, and C. Cossiah. 2024. “Impact of Climate Change on the Reproduction, Distribution and Abundance of Herpetofauna: A Review of Literature.” GSC Advanced Research 18: 266–282.

[7]

Bolger, A. M., M. Lohse, and B. Usadel. 2014. “Trimmomatic: A Flexible Trimmer for Illumina Sequence Data.” Bioinformatics 30: 2114–2120.

[8]

Bowden, T. J., K. D. Thompson, A. L. Morgan, R. M. Gratacap, and S. Nikoskelainen. 2007. “Seasonal Variation and the Immune Response: A Fish Perspective.” Fish Shellfish Immunology 22: 695–706.

[9]

Buckley, B. A., A. Y. Gracey, and G. N. Somero. 2006. “The Cellular Response to Heat Stress in the Goby Gillichthys mirabilis: A cDNA Microarray and Protein-Level Analysis.” Journal of Experimental Biology 209: 2660–2677.

[10]

Burger, J. 2009. Red-Eared Slider Turtles (Trachemys scripta elegans). Freshwater Ecology Conservation Lab, University of Washington.

[11]

Chang, J., Y. Pan, W. Liu, et al. 2022. “Acute Temperature Adaptation Mechanisms in the Native Reptile Species Eremias argus.” Science of the Total Environment 818: 151773.

[12]

Chen, Y., E. Liu, C. Li, et al. 2021. “Effects of Heat Stress on Histopathology, Antioxidant Enzymes, and Transcriptomic Profiles in Gills of Pikeperch Sander lucioperca.” Aquaculture 534: 736277.

[13]

Chen, Y., X. Wu, J. Lai, et al. 2023. “Integrated Biochemical, Transcriptomic and Metabolomic Analyses Provide Insight into Heat Stress Response in Yangtze Sturgeon (Acipenser dabryanus).” Ecotoxicology Environmental Safety 249: 114366.

[14]

Chin, C. H., S. H. Chen, H. H. Wu, C. W. Ho, M. T. Ko, and C. Y. Lin. 2014. “cytoHubba: Identifying Hub Objects and Sub-Networks from Complex Interactome.” BMC Systems Biology 8, no. Suppl 4: S11.

[15]

Choi, H. H., D. M. Shin, G. Kang, et al. 2010. “Endoplasmic Reticulum Stress Response Is Involved in Mycobacterium tuberculosis Protein ESAT-6-Mediated Apoptosis.” FEBS Letters 584: 2445–2454.

[16]

Coenye, T. 2021. “Do Results Obtained with RNA-Sequencing Require Independent Verification?” Biofilm 3: 100043.

[17]

Dang, W., Y. C. Hu, J. Geng, J. Wang, and H. L. Lu. 2019. “Thermal Physiological Performance of Two Freshwater Turtles Acclimated to Different Temperatures.” Journal of Comparative Physiology B 189: 121–130.

[18]

Everaert, C., M. Luypaert, J. L. V. Maag, et al. 2017. “Benchmarking of RNA-Sequencing Analysis Workflows Using Whole-Transcriptome RT-qPCR Expression Data.” Scientific Reports 7, no. 1: 1559.

[19]

Fabri, J., N. P. De Sá, I. Malavazi, and M. Del Poeta. 2020. “The Dynamics and Role of Sphingolipids in Eukaryotic Organisms Upon Thermal Adaptation.” Progress in Lipid Research 80: 101063.

[20]

Fan, Z., J. Mao, Y. Wang, et al. 2024. “Transcriptomic WGCNA Analyses Reveal Endoplasmic Reticulum Response of Patinopecten yessoensis Under Acute Heat Stress.” Aquaculture 589: 740938.

[21]

Florea, L., L. Song, and S. L. Salzberg. 2013. “Thousands of Exon Skipping Events Differentiate Among Splicing Patterns in Sixteen Human Tissues.” F1000Research 2: 188.

[22]

Gao, Y., Y. Wei, D. Cao, and S. Gong. 2021. “Transcriptome Analysis Reveals Decreased Immunity Under Heat Stress in Mauremys mutica.” Aquaculture 531: 735894.

[23]

Garcia, R. A., M. Cabeza, C. Rahbek, and M. B. AraÚJo. 2014. “Multiple Dimensions of Climate Change and Their Implications for Biodiversity.” Science 344: 1247579.

[24]

Gilbert, E., A. Žagar, M. López-Darias, et al. 2024. “Environmental Factors Influence Cross-Talk Between a Heat Shock Protein and an Oxidative Stress Protein Modification in the Lizard Gallotia galloti.” PLoS ONE 19, no. 3: e0300111.

[25]

Gong, S., Y. Gao, H. Duan, Y. Ge, and Y. Wei. 2023. “Incorporating Physiological Data into Species Distribution Models to Predict the Potential Distribution Range of the Red-Eared Slider in China.” Ecological Indicators 154: 110749.

[26]

Hanot, M., L. Raby, P. Völkel, X. Le Bourhis, and P. O. Angrand. 2023. “The Contribution of the Zebrafish Model to the Understanding of Polycomb Repression in Vertebrates.” International Journal of Molecular Sciences 24: 2322.

[27]

Hu, J., Y. Zhang, K. Yan, et al. 2023. “Change and Regulation of Nutritional Metabolism in Silver Pomfret During Compensatory Growth.” Marine Biotechnology 25, no. 6: 1085–1098.

[28]

Huey, R. B., M. R. Kearney, A. Krockenberger, J. A. Holtum, M. Jess, and S. E. Williams. 2012. “Predicting Organismal Vulnerability to Climate Warming: Roles of Behaviour, Physiology and Adaptation.” Philosophical Transactions of the Royal Society B: Biological Sciences 367, no. 1596: 1665–1679.

[29]

Jesus, T. F., A. R. Grosso, V. M. F. Almeida-Val, and M. M. Coelho. 2016. “Transcriptome Profiling of Two Iberian Freshwater Fish Exposed to Thermal Stress.” Journal of Thermal Biology 55: 54–61.

[30]

Jeyachandran, S., H. Chellapandian, K. Park, and I. S. Kwak. 2023. “A Review on the Involvement of Heat Shock Proteins (Extrinsic Chaperones) in Response to Stress Conditions in Aquatic Organisms.” Antioxidants 12: 1444.

[31]

Jiang, S., C. Zhang, X. Pan, K. B. Storey, and W. Zhang. 2024. “Distinct Metabolic Responses to Thermal Stress Between Invasive Freshwater Turtle Trachemys scripta elegans and Native Freshwater Turtles in China.” Integrative Zoology 19: 1057–1075.

[32]

Jones, R. L. 1996. “Home Range and Seasonal Movements of the Turtle Graptemys flavimaculata.” Journal of Herpetology 30, no. 3: 376–385.

[33]

Jones, R. L. 2017. “Long-term Trends in Ringed Sawback (Graptemys oculifera) Growth, Survivorship, Sex Ratios, and Population Sizes in the Pearl River, Mississippi.” Chelonian Conservation and Biology 16, no. 2: 215–228.

[34]

Jørgensen, L. B., M. Ørsted, H. Malte, T. Wang, and J. Overgaard. 2022. “Extreme Escalation of Heat Failure Rates in Ectotherms with Global Warming.” Nature 611: 93–98.

[35]

Juan, C. A., J. M. Pérez De La Lastra, F. J. Plou, and E. Pérez-Lebeña. 2021. “The Chemistry of Reactive Oxygen Species (ROS) Revisited: Outlining Their Role in Biological Macromolecules (DNA, Lipids and Proteins) and Induced Pathologies.” International Journal of Molecular Sciences 22: 4642.

[36]

Kazmi, S., Y. Y. L. Wang, Y. E. Cai, and Z. Wang. 2022. “Temperature Effects in Single or Combined with Chemicals to the Aquatic Organisms: An Overview of Thermo-Chemical Stress.” Ecological Indicators 143: 109354.

[37]

Kim, D., B. Langmead, and S. L. Salzberg. 2015. “HISAT: A Fast Spliced Aligner with Low Memory Requirements.” Nature Methods 12: 357–360.

[38]

Knapp, B. D., and K. C. Huang. 2022. “The Effects of Temperature on Cellular Physiology.” Annual Review of Biophysics 51: 499–526.

[39]

Koo, J., T. G. Son, S. Y. Kim, and K. Y. Lee. 2015. “Differential Responses of Apis mellifera Heat Shock Protein Genes to Heat Shock, Flower-Thinning Formulations, and Imidacloprid.” Journal of Asia-Pacific Entomology 18: 583–589.

[40]

Kültz, D. 2005. “Molecular and Evolutionary Basis of the Cellular Stress Response.” Annual Review of Physiology 67: 225–257.

[41]

Landeira, D., and A. G. Fisher. 2011. “Inactive yet Indispensable: The Tale of Jarid2.” Trends in Cell Biology 21: 74–80.

[42]

Li, B., S. Sun, J. Zhu, S. Yanli, Z. Wuxiao, and X. Ge. 2019a. “Transcriptome Profiling and Histology Changes in Juvenile Blunt Snout Bream (Megalobrama amblycephala) Liver Tissue in Response to Acute Thermal Stress.” Genomics 111: 242–250.

[43]

Li, C., H. Fang, and D. Xu. 2019b. “Effect of Seasonal High Temperature on the Immune Response in Apostichopus japonicus by Transcriptome Analysis.” Fish & Shellfish Immunology 92: 765–771.

[44]

Li, C., W. Zhao, C. Qin, et al. 2021. “Comparative Transcriptome Analysis Reveals Changes in Gene Expression in Sea Cucumber (Holothuria leucospilota) in Response to Acute Temperature Stress.” Comparative Biochemistry Physiology Part D: Genomics Proteomics 40: 100883.

[45]

Li, G., R. Margueron, M. Ku, P. Chambon, B. E. Bernstein, and D. Reinberg. 2010. “Jarid2 and PRC2, Partners in Regulating Gene Expression.” Genes & Development 24: 368–380.

[46]

Li, X., X. Hu, A. Lv, and Z. Guan. 2022. “Skin Immune Response to Aeromonas hydrophila Infection in Crucian Carp Carassius auratus Revealed by Multi-omics Analysis.” Fish & Shellfish Immunology 127: 866–875.

[47]

Liu, S., F. Tian, D. Qi, et al. 2023. “Physiological, Metabolomic, and Transcriptomic Reveal Metabolic Pathway Alterations in Gymnocypris przewalskii due to Cold Exposure.” BMC Genomics [Electronic Resource] 24, no. 1: 545.

[48]

Long, Y., L. Li, Q. Li, X. He, and Z. Cui. 2012. “Transcriptomic Characterization of Temperature Stress Responses in Larval Zebrafish.” PLoS ONE 7: e37209.

[49]

López-Maury, L., S. Marguerat, and J. Bähler. 2008. “Tuning Gene Expression to Changing Environments: From Rapid Responses to Evolutionary Adaptation.” Nature Reviews Genetics 9: 583–593.

[50]

Love, M. I., W. Huber, and S. Anders. 2014. “Moderated Estimation of Fold Change and Dispersion for RNA-Seq Data with DESeq2.” Genome Biology 15: 1–21.

[51]

Lu, H., Y. Hu, S. Li, W. Dang, and Y. Zhang. 2020. “Acclimatory Responses of Thermal Physiological Performances in Hatchling Yellow Pond Turtles (Mauremys mutica).” Animal Biology 70: 55–65.

[52]

Luo, M., W. Zhu, Z. Liang, et al. 2024. “High-Temperature Stress Response: Insights into the Molecular Regulation of American Shad (Alosa sapidissima) Using a Multi-Omics Approach.” Science of the Total Environment 916: 170329.

[53]

Ma, C. S., G. Ma, and S. Pincebourde. 2021. “Survive a Warming Climate: Insect Responses to Extreme High Temperatures.” Annual Review of Entomology 66: 163–184.

[54]

Mayer, M. P., and B. Bukau. 2005. “Hsp70 Chaperones: Cellular Functions and Molecular Mechanism.” Cellular Molecular Life Sciences 62: 670–684.

[55]

Maytin, E. V., M. Ubeda, J. C. Lin, and J. F. Habener. 2001. “Stress-Inducible Transcription Factor CHOP/gadd153 Induces Apoptosis in Mammalian Cells via p38 Kinase-Dependent and -Independent Mechanisms.” Experimental Cell Research 267: 193–204.

[56]

Moore, B., J. Jolly, M. Izumiyama, E. Kawai, T. Ravasi, and T. Ryu. 2024. “Tissue-Specific Transcriptional Response of Post-Larval Clownfish to Ocean Warming.” Science of The Total Environment 908: 168221.

[57]

Morrison, S. F., and K. Nakamura. 2019. “Central Mechanisms for Thermoregulation.” Annual Review of Physiology 81, no. 1: 285–308.

[58]

Oyadomari, S., and M. Mori. 2004. “Roles of CHOP/GADD153 in Endoplasmic Reticulum Stress.” Cell Death Differentiation 11: 381–389.

[59]

Parkhomchuk, D., T. Borodina, V. Amstislavskiy, et al. 2009. “Transcriptome Analysis by Strand-Specific Sequencing of Complementary DNA.” Nucleic Acids Research 37: e123–e123.

[60]

Patrício, A. R., L. A. Hawkes, J. R. Monsinjon, B. J. Godley, and M. M Fuentes. 2021. “Climate Change and Marine Turtles: Recent Advances and Future Directions.” Endangered Species Research 44: 363–395.

[61]

Perkins-Kirkpatrick, S. E., and S. C. Lewis. 2020. “Increasing Trends in Regional Heatwaves.” Nature Communications 11: 3357.

[62]

Pertea, M., G. M. Pertea, C. M. Antonescu, T. C. Chang, J. T. Mendell, and S. L. Salzberg. 2015. “StringTie Enables Improved Reconstruction of a Transcriptome from RNA-Seq Reads.” Nature Biotechnology 33: 290–295.

[63]

Rahman, M. S., and M. S. Rahman. 2021. “Effects of Elevated Temperature on Prooxidant-Antioxidant Homeostasis and Redox Status in the American Oyster: Signaling Pathways of Cellular Apoptosis During Heat Stress.” Environmental Research 196: 110428.

[64]

Rangan, K. J., and S. L. Reck-Peterson. 2023. “RNA Recoding in Cephalopods Tailors Microtubule Motor Protein Function.” Cell 186, no. 12: 2531–2543.

[65]

Richter-Boix, A., M. Katzenberger, H. Duarte, M. Quintela, M. Tejedo, and A. Laurila. 2015. “Local Divergence of Thermal Reaction Norms Among Amphibian Populations Is Affected by Pond Temperature Variation.” Evolution; International Journal of Organic Evolution 69, no. 8: 2210–2226.

[66]

Rossi, A., C. Bacchetta, and J. Cazenave. 2017. “Effect of Thermal Stress on Metabolic and Oxidative Stress Biomarkers of Hoplosternum littorale (Teleostei, Callichthyidae).” Ecological Indicators 79: 361–370.

[67]

Schröder, M. 2008. “Endoplasmic Reticulum Stress Responses.” Cellular Molecular Life Sciences 65: 862–894.

[68]

Schulze, S. K., R. Kanwar, M. Gölzenleuchter, T. M. Therneau, and A. S. Beutler. 2012. “SERE: Single-parameter Quality Control and Sample Comparison for RNA-Seq.” BMC Genomics [Electronic Resource] 13: 524.

[69]

Scudiero, R., C. M. Motta, and P. Simoniello. 2021. “Impact of Environmental Stressors on Gene Expression in the Embryo of the Italian Wall Lizard.” Applied Sciences 11: 4723.

[70]

Servili, A., A. V. Canario, O. Mouchel, and J. A. Muñoz-Cueto. 2020. “Climate Change Impacts on Fish Reproduction Are Mediated at Multiple Levels of the Brain-Pituitary-Gonad Axis.” General Comparative Endocrinology 291: 113439.

[71]

Shen, J., F. Meng, Y. Zhang, and W. Du. 2013. “Field Body Temperature and Thermal Preference of the Big-Headed Turtle Platysternon megacephalum.” Current Zoology 59: 626–632.

[72]

Shi, K., J. Li, J. Lv, P. Liu, J. Li, and S. Li. 2020. “Full-length Transcriptome Sequences of Ridgetail White Prawn Exopalaemon carinicauda Provide Insight into Gene Expression Dynamics During Thermal Stress.” Science of The Total Environment 747: 141238.

[73]

Shi, K. P., S. L. Dong, Y. G. Zhou, Y. Li, Q. F. Gao, and D. J. Sun. 2019. “RNA-seq Reveals Temporal Differences in the Transcriptome Response to Acute Heat Stress in the Atlantic Salmon (Salmo salar).” Comparative Biochemistry and Physiology Part D: Genomics and Proteomics 30: 169–178.

[74]

Stanford, C. B., J. B. Iverson, A. G. J. Rhodin, et al. 2020. “Turtles and Tortoises Are in Trouble.” Current Biology 30: R721–R735.

[75]

Sun, J., L. Zhao, C. Cui, et al. 2019. “Influence of Long-Term Temperature Stress on Respiration Frequency, Na+/K+-ATPase Activity, and Lipid Metabolism in Common Carp (Cyprinus carpio).” Journal of Thermal Biology 83: 165–171.

[76]

Sung, Y. H., N. E. Karraker, and B. C. Hau. 2013. “Demographic Evidence of Illegal Harvesting of an Endangered Asian Turtle.” Conservation Biology 27: 1421–1428.

[77]

Szklarczyk, D., A. L. Gable, D. Lyon, et al. 2019. “STRING v11: Protein–Protein Association Networks with Increased Coverage, Supporting Functional Discovery in Genome-Wide Experimental Datasets.” Nucleic Acids Research 47: D607–D613.

[78]

Tang, Z., Y. Yang, Z. Wu, and Y. Ji. 2023. “Heat Stress-Induced Intestinal Barrier Impairment: Current Insights into the Aspects of Oxidative Stress and Endoplasmic Reticulum Stress.” Journal of Agricultural Food Chemistry 71: 5438–5449.

[79]

Tepedelen, B. E., and P. B. Kirmizibayrak. 2019. Endoplasmic Reticulum-Associated Degradation (ERAD). IntechOpen Publishers.

[80]

Thuerauf, D. J., M. Marcinko, P. J. Belmont, and C. C. Glembotski. 2007. “Effects of the Isoform-specific Characteristics of ATF6α and ATF6β on Endoplasmic Reticulum Stress Response Gene Expression and Cell Viability.” Journal of Biological Chemistry 282: 22865–22878.

[81]

Wei, Y., Y. Gao, D. Cao, Y. Ge, H. Shi, and S. Gong. 2021. “Effect of Incubation Temperature and Substrate Moisture on Embryonic Development, Hatchling Phenotypes and Post-hatching Growth in the Reeves' Turtle, Mauremys reevesii.” PeerJ 9: e10553.

[82]

Wu, Q. 2018. Comparison of Thermal Tolerance, Antioxidant Capacity and HSP70 Expression Between Invasive Trachemys scripta elegans and Native Turtles. Hangzhou Normal University.

[83]

Xie, Y., L. Song, Z. Weng, S. Liu, and Z. Liu. 2015. “Hsp90, Hsp60 and sHsp Families of Heat Shock Protein Genes in Channel Catfish and Their Expression After Bacterial Infections.” Fish Shellfish Immunology 44: 642–651.

[84]

Xu, Y., Z. Wang, Y. Zhang, et al. 2022. “Transcriptome Analysis Reveals Acclimation Responses of Pearl Oysters to Marine Heatwaves.” Science of the Total Environment 810: 151189.

[85]

Yap, K. N., K. Yamada, S. Zikeli, H. Kiaris, and W. R. Hood. 2021. “Evaluating Endoplasmic Reticulum Stress and Unfolded Protein Response Through the Lens of Ecology and Evolution.” Biological Reviews 96, no. 2: 541–556.

[86]

Yu, D., Z. Zhang, Z. Shen, C. Zhang, and H. Liu. 2018. “Regional Differences in Thermal Adaptation of a Cold-Water Fish Rhynchocypris oxycephalus Revealed by Thermal Tolerance and Transcriptomic Responses.” Scientific Reports 8: 11703.

[87]

Yu, G., L. G. Wang, Y. Han, and Q. Y. He. 2012. “ClusterProfiler: An R Package for Comparing Biological Themes Among Gene Clusters.” Omics: A Journal of Integrative Biology 16: 284–287.

[88]

Zhang, C., Y. Xu, Y. Hua, P. Li, K. B. Storey, and W. Zhang. 2023. “Greater Physiological Resistance to Heat May Favour an Invasive Freshwater Turtle, Enabling It to Outcompete Native Species in a Changing Climate.” Freshwater Biology 68: 1588–1601.

[89]

Zhang, X., J. Yuan, X. Zhang, Y. Yu, and F. Li. 2022. “Comparative Transcriptomic Analysis Unveils a Network of Energy Reallocation in Litopenaeus vannamei Responsive to Heat-Stress.” Ecotoxicology and Environmental Safety 238: 113600.

[90]

Zhang, Y. P., W. G. Du, J. W. Shen, and L. Shu. 2009. “Low Optimal Temperatures for Food Conversion and Growth in the Big-Headed Turtle, Platysternon megacephalum.” Aquaculture 295: 106–109.

[91]

Zhao, G., Z. Liu, J. Quan, J. Lu, L. Li, and Y. Pan. 2024. “Ribosome Profiling and RNA Sequencing Reveal Translation and Transcription Regulation Under Acute Heat Stress in Rainbow Trout (Oncorhynchus mykiss, Walbaum, 1792) Liver.” International Journal of Molecular Sciences 25: 8848.

[92]

Zhao, H., H. Ke, L. Zhang, et al. 2022. “Integrated Analysis About the Effects of Heat Stress on Physiological Responses and Energy Metabolism in Gymnocypris chilianensis.” Science of The Total Environment 806: 151252.

[93]

Zheng, J., J. Cao, Y. Mao, Y. Su, and J. Wang. 2019. “Comparative Transcriptome Analysis Provides Comprehensive Insights into the Heat Stress Response of Marsupenaeus japonicus.” Aquaculture 502: 338–346.

[94]

Zhou, C., Y. Duan, J. Li, et al. 2024. “Decoding the Intestinal Response to Heat Stress in Gymnocypris eckloni: Insights from a Thorough Analysis of Microbiome and Transcriptome.” Aquaculture 591: 741112.

[95]

Zinszner, H., M. Kuroda, X. Z. Wang, et al. 1998. “CHOP Is Implicated in Programmed Cell Death in Response to Impaired Function of the Endoplasmic Reticulum.” Genes Development 12: 982–995.

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