|
|
|
| Study on Transcriptional Characteristics in Muscle Tissue of Diploid and Triploid Paralichthys olivaceus in Response to Heat Stress |
| WANG De-Yun1,2, WANG Li-Juan2,3,4, YOU Feng2,3,4, YUE Xin-Lu5, WU Zhi-Hao2,3,4,* |
1 School of Marine Science and Engineering, Qingdao Agricultural University, Qingdao 266109, China;
2 State Key Laboratory of Breeding Biotechnology and Sustainable Aquaculture, Institute of Oceanology, Chinese Academy of Sciences, Qingdao 266000, China;
3 Laboratory for Marine Biology and Biotechnology, Qingdao Marine Science and Technology Center, Qingdao 266000, China;
4 Laboratory of Experimental Marine Biology, Institute of Oceanology, Chinese Academy of Sciences, Qingdao 266000, China;
5 Weihai Shenghang Aquatic Science and Technology Co., Ltd., Weihai 264200, China |
|
|
|
|
Abstract High temperature has been a severe challenge to the aquaculture. In recent years, with the continuous rise of water temperatures and prolonged duration of high-temperature periods in summer, the impact of heat stress on fish has become increasingly apparent. Triploid fishes exhibit advantages in growth performance, stress resistance and quality traits due to low or complete sterility, and have been widely applied in aquaculture. However, research on their heat tolerance and molecular responses to heat stress remains limited. Olive flounder(Paralichthys olivaceus) is a commercially important marine fish species in China. The present study evaluated the heat tolerance of triploid flounder, analyzed its molecular response to heat stress in muscle via transcriptome sequencing, and compared with those of diploids. The results demonstrated that triploid flounder exhibited significantly enhanced heat tolerance compared to diploids, with both the higher high temperature threshold and longer survival time under high temperature than those of diploids(P<0.01). Under heat stress at 31 ℃ for 24 h, diploid fish displayed adaptive changes in gene expression, a total of 847 genes were differentially expressed, including 618 up-regulated and 229 down-regulated genes, among which genes related to apoptosis and metabolic regulation were significantly upregulated. In contrast, high temperature exerted a relatively minor effect on gene expression in triploid fish, with only 19 genes differentially expressed(16 up-regulated and 3 down-regulated). Among these, genes involved in carbohydrate, fatty acid, amino acid metabolism, apoptosis and FoxO signaling pathway were downregulated. These findings enrich the theoretical foundation for research on fish stress resistance, and provide critical insights for the development of heat-tolerant germplasm.
|
|
Received: 31 December 2025
|
|
|
|
Corresponding Authors:
*wuzhihao@qdio.ac.cn
|
|
|
|
[1] 蔡榕硕, 谭红建. 2024. 中国近海变暖和海洋热浪演变特征及气候成因研究进展[J]. 大气科学, 48(1): 121-146.
(Cai R S, Tan H J.2024. Research progress on the evolution characteristics and climatic causes of warming and marine heatwaves in the coastal seas of China[J]. Chinese Journal of Atmospheric Sciences, 48(1): 121-146.)
[2] 程丽娜, 徐冬冬, 李三磊, 等. 2011. 高温胁迫对不同规格褐牙鲆生长性能的影响[J]. 上海海洋大学学报, 20(3): 368-373.
(Cheng L N, Xu D D, Li S L, et al.2011. Effects of high temperature stress on growth performance of Paralichthys olivaceus with different sizes[J]. Journal of Shanghai Ocean University, 20(3): 368-373.)
[3] 何雨, 刘峰, 张天乐, 等. 2024. 高温胁迫对小黄鱼肝脏组织结构和细胞凋亡的影响[J]. 浙江农业学报, 36(1): 58-66.
(He Y, Liu F, Zhang T L, et al.2024. Effects of heat stress on liver tissue structure and cell apoptosis of small yellow croaker[J]. Acta Agriculturae Zhejiangensis, 36(1): 58-66.)
[4] 李荣岭, 张兆远, 王丹晨, 等. 2007. 不同生长速度牙鲆的肌肉组织基因差异表达研究[J]. 山东农业大学学报(自然科学版), 38(1): 7-10.
(Li R L, Zhang Z Y, Wang D C, et al.2007. Differential gene expression in muscle tissue of Paralichthys olivaceus with different growth rates[J]. Journal of Shandong Agricultural University(Natural Science Edition), 38(1): 7-10.)
[5] 柳意樊. 2014. 褐牙鲆(Paralichthys olivaceus)和杂交鲆(P. olivaceus♀×P. dentatus♂)幼鱼高温耐受性研究[D]. 硕士学位论文, 中国科学院研究生院(海洋研究所), 导师: 李军, pp. 24-26.
(Liu Y F.2014. High temperature tolerance of juvenile olive flounder(Paralichthys olivaceus) and hybrid flounder(P. olivaceus♀×P. dentatus♂)[D]. Thesis for M.S., Graduate School of the Chinese Academy of Sciences(Institute of Oceanology), Supervisor: Li J, pp. 24-26.)
[6] 孟亮, 王新安, 马爱军, 等. 2021. 高温胁迫下牙鲆 qPCR 内参基因的筛选与验证[J]. 水产学报, 45(6): 892-902.
(Meng L, Wang X A, Ma A J, et al.2021. Screening and validation of reference genes for qPCR in Japanese flounder(Paralichthys olivaceus) under heat stress[J]. Journal of Fisheries of China, 45(6): 892-902.)
[7] 徐冬冬, 楼宝, 詹炜, 等. 2010. 高温胁迫对褐牙鲆生长及肝脏抗氧化酶活性的影响[J]. 水产学报, 34(10): 1537-1544.
(Xu D D, Lou B, Zhan W, et al.2010. Effects of high temperature stress on growth and liver antioxidant enzyme activities of olive flounder(Paralichthys olivaceus)[J]. Journal of Fisheries of China, 34(10): 1537-1544.)
[8] 尤锋, 刘静. 1995. 三倍体牙鲆的核型证明[J]. 海洋与湖沼, 26(5): 115-118.
(You F, Liu J.1995. Karyotype verification of triploid Paralichthys olivaceus[J]. Oceanologia et Limnologia Sinica, 26(5): 115-118.)
[9] Barbarossa V, Bosmans J, Wanders N, et al.2021. Threats of global warming to the world's freshwater fishes[J]. Nature Communications, 12: 1701.
[10] Cal R, Terrones J, Vidal S, et al.2010. Differential incidence of gonadal apoptosis in triploid-induced male and female turbot(Scophthalmus maximus)[J]. Aquaculture, 307(3-4): 193-200.
[11] Che D, Wen H, Li J, et al.2019. Comparison studies of antioxidant enzymes between diploid and triploid rainbow trout in acute high temperature stress[J]. Open Journal of Fisheries Research, 6(2): 31-41.
[12] Cleveland B M, Weber G M.2014. Ploidy effects on genes regulating growth mechanisms during fasting and refeeding in juvenile rainbow trout(Oncorhynchus mykiss)[J]. Molecular and Cellular Endocrinology, 382: 139-149.
[13] Ellis K E, Iwama G K, Palmer B M, et al.2013. Secondary stress responses(plasma glucose and ions) during hypoxic critical thermal maxima tests in diploid and triploid brook trout(Salvelinus fontinalis) are consistent with predictions of acute stress and do not differ between ploidy levels[J]. Journal of Fish Biology, 83(4): 1017-1030.
[14] Enomoto A, Fukasawa T.2022. The role of calcium-calpain pathway in hyperthermia[J]. Frontiers in Molecular Medicine, 2: 1005258.
[15] Esam F, Khalafalla M M, Gewaily M S, et al.2022. Acute ammonia exposure combined with heat stress impaired the histological features of gills and liver tissues and the expression responses of immune and antioxidative related genes in Nile tilapia[J]. Ecotoxicology and Environmental Safety, 231: 113187.
[16] Fraser T W K, Fleming M S, Poppe T T, et al.2014. The effect of ploidy and incubation temperature on survival and the prevalence of aplasia of the septum transversum in Atlantic salmon, Salmo salar L.[J]. Journal of Fish Diseases, 37: 189-200.
[17] He J, Qiang J, Yang H, et al.2015. Changes in the fatty acid composition and regulation of antioxidant enzymes and physiology of juvenile genetically improved farmed tilapia Oreochromis niloticus(L.), subjected to short-term low temperature stress[J]. Journal of Thermal Biology, 53: 90-97.
[18] Hibino S, Amiya N, Nakano N, et al.2024. Onset of estivation in western sand lance Ammodytes japonicus is not solely triggered by elevating water temperature[J]. Journal of Ethology, 42: 131-135.
[19] Hu Q, Lu J, Yang Y, et al.2023. Acute thermal stress reduces skeletal muscle growth and quality in gibel carp(Carassius gibelio)[J]. Water, 15(15): 2706.
[20] Hu P, Gao Q, Han Y Z, et al.2015. Comparison of muscle physicochemical properties and texture characteristics of wild, pond-cultured and industrial-cultured olive flounder(Paralichthys olivaceus)[J]. Acta Hydrobiologica Sinica, 39(4): 723-729.
[21] IPCC.2023. Summary for policymakers[R]//Lee H, Romero J, eds. Climate change 2023: synthesis report. Contribution of Working Groups I, II and III to the Sixth Assessment Report of the Intergovernmental Panel on Climate Change. Geneva: IPCC, pp. 1-34.
[22] Keyvanshokooh S.2025.The performance of triploids versus diploids in aquaculture: A review through the omics window[J]. Aquaculture International, 33: 36.
[23] Khan J R, Iftikar F I, Herbert N A, et al.2014. Thermal plasticity of skeletal muscle mitochondrial activity and whole animal respiration in a common intertidal triplefin fish, Forsterygion lapillum(Family: Tripterygiidae)[J]. Journal of Comparative Physiology B, 184(8): 991-1001.
[24] Kikuchi K, Takeda S.2001. Present status of research and production of Japanese flounder, Paralichthys olivaceus, in Japan[J]. Journal of Applied Aquaculture, 11(1/2): 165-175.
[25] Leal M J, Van Eenennaam J P, Schreier A D, et al.2019. Triploidy in white sturgeon(Acipenser transmontanus): Effects of acute stress and warm acclimation on physiological performance[J]. Comparative Biochemistry and Physiology Part A: Molecular & Integrative Physiology, 229: 10-17.
[26] Li X, Liu Y, Duan C, et al.2025. Effects of chronic high-temperature stress on muscle tissue integrity and metabolism-related genes in Clarias fuscus[J]. Comparative Biochemistry and Physiology Part D: Genomics Proteomics, 55: 101497.
[27] Liang Y, Zhang Y, Sun B, et al.2017. Heat stress induces metabolic rearrangement in the muscle of olive flounder(Paralichthys olivaceus)[J]. Fish & Shellfish Immunology, 68: 435-442.
[28] Liu H, Wu Z H, Zhu X P, et al.2018. Comparative performance of growth, vertebral structure and muscle composition in diploid and triploid Paralichthys olivaceus[J]. Journal of Fish Diseases, 41: 1495-1504.
[29] Liu H, Yang R, Fu Z, et al.2023. Acute thermal stress increased enzyme activity and muscle energy distribution of yellowfin tuna[J]. PLOS ONE, 18(10): e0289606.
[30] Ma F, Zhao L, Ma R L, et al.2023. FoxO signaling and mitochondria-related apoptosis pathways mediate tsinling lenok trout(Brachymystax lenok Tsinlingensis) liver injury under high temperature stress[J]. International Journal of Biological Macromolecules, 251: 126404.
[31] Ma X H, Sun G L, Meng Y Q, et al.2024. Stress response and adaptation mechanism of triploid rainbow trout(Oncorhynchus mykiss) treated with chronic heat challenge[J]. Aquaculture, 593: 741282.
[32] Molina A, Dettleff P, Valenzuela-Muñoz Vet al.2023. High-temperature stress induces autophagy in rainbow trout skeletal muscle[J]. Fishes, 8(6): 303.
[33] Niu Y, Guan L, Wang C, et al.2023. Aestivation induces widespread transcriptional changes in the African lungfish[J]. Frontiers in Genetics, 14: 1096929.
[34] Sakamoto K, Nakajima M, Taniguchi N.2005. Thermal tolerance traits of juveniles of the ayu Plecoglossus altivelis and Japanese flounder Paralichthys olivaceus evaluated by their caudal fin cells[J]. Aquaculture, 246(1-4): 93-99.
[35] San L Z, Wang G X, He Z W, et al.2024. Genome-wide association study for high-temperature tolerance in the Japanese flounder[J]. Animal, 18(9): 101273.
[36] Shrimpton J, Heath J, Devlin R, et al.2012. Effect of triploidy on growth and ionoregulatory performance in ocean-type Chinook salmon: A quantitative genetics approach[J]. Aquaculture, 362: 248-254.
[37] Sun J L, Zhao L L, Wu H, et al.2020. Acute hypoxia changes the mode of glucose and lipid utilization in the liver of the largemouth bass(Micropterus salmoides)[J]. The Science of the Total Environment, 713: 1135157.
[38] Verhille C, Anttila K, Farrell A P.2013. A heart to heart on temperature: Impaired temperature tolerance of triploid rainbow trout(Oncorhynchus mykiss) due to early onset of cardiac arrhythmia[J]. Comparative Biochemistry and Physiology Part A, 164(4): 653-657.
[39] Wang R, Han P, Liu X, et al.2023. Genome-wide identification of TNF receptor-associated factors in Japanese flounder(Paralichthys olivaceus) and functional analysis of resistance to temperature and Edwardsiella tarda stress[J]. Fish & Shellfish Immunology, 138: 108862.
[40] Wu Q, Song Z, Wang L, et al.2023. Comparative study on the gonadal development in the diploid and artificially induced triploid olive flounder Paralichthys olivaceus[J]. Aquaculture, 565: 739106.
[41] Zhang C, Ding W, Cao Z, et al.2021. Effects of acute high temperature stress on antioxidant enzymes activity, digestive enzymes activity and gene expression of heat shock proteins in mandarin fish(Siniperca chuatsi)[J]. Journal of Southern Agriculture, 52(3): 815-826. |
|
|
|
