DNA Methylation of pacap Gene Is Involved in Growth Superiority of Female Half Smooth Tongue Sole (Cynoglossus semilaevis) in Different Salinities

Alliot, E., Pastoureaud, A., and Thebault, H., 1983. Influence of temperature and salinity on growth and body composition of sea bass fingerlings, Dicentrarchus labrax. Aquaculture, 31(2): 181–194. Angers, B., Castonguay, E., and Massicotte, R., 2010. Environmentally induced phenotypes and DNA methylation: How to deal with unpredictable conditions until the next generation and after. Molecular Ecology, 19(7): 1283–1295. Aniagu, S. O., Williams, T. D., Allen, Y., Katsiadaki, I., and Chipman, J. K., 2008. Global genomic methylation levels in the liver and gonads of the three-spine stickleback (Gasterosteus aculeatus) after exposure to hexabromocyclododecane and 17-β oestradiol. Environment International, 34(3): 310–317. Aubert, N., Falluel-Morel, A., Vaudry, D., Xifro, X., Rodriguez-Alvarez, J., Fisch, C., De Jouffrey, S., Lebigot, J. F., Fournier, A., Vaudry, H., and Gonzalez, B. J., 2006. PACAP and C2-ceramide generate different AP-1 complexes through a MAP-kinase-dependent pathway: Involvement of c-Fos in PACAP-induced Bcl-2 expression. Journal of Neurochemistry, 99(4): 1237–1250. Boeuf, G., and Payan, P., 2001. How should salinity influence fish growth? Comparative Biochemistry and Physiology Part C: Toxicology & Pharmacology, 130(4): 411–423. Callaway, R., Shinn, A. P., Grenfell, S. E., Bron, J. E., Burnell, G., Cook, E. J., Crumlish, M., Culloty, S., Davidson, K., and Ellis, R. P., 2012. Review of climate change impacts on marine aquaculture in the UK and Ireland. Aquatic Conservation: Marine and Freshwater Ecosystems, 22(3): 389–421. Chen, C. F., Wen, H. S., Wang, Z. P., He, F., Zhang, J. R., Chen, X. Y., Jin, G. X., Shi, B., Shi, D., and Yang, Y. P., 2010. Cloning and expression of P450c17-I (17α-hydroxylase/17,20-lyase) in brain and ovary during gonad development in Cynoglossus semilaevis. Fish Physiology and Biochemistry, 36(4): 1001–1012. Chen, S., Li, J., Deng, S., Tian, Y., Wang, Q., Zhuang, Z., Sha, Z., and Xu, J., 2007. Isolation of female-specific AFLP markers and molecular identification of genetic sex in half-smooth tongue sole (Cynoglossus semilaevis). Marine Biotechnology, 9(2): 273–280. Contractor, R. G., Foran, C. M., Li, S., and Willett, K. L., 2004. Evidence of gender-and tissue-specific promoter methylation and the potential for ethinylestradiol-induced changes in Japanese medaka (Oryzias latipes) estrogen receptor and aromatase genes. Journal of Toxicology and Environmental Health, Part A, 67(1): 1–22. Ding, Y., He, F., Wen, H., Li, J., Qian, K., Chi, M., Ni, M., Yin, X., Bu, Y., and Zhao, Y., 2012. Polymorphism in exons CpG rich regions of the cyp17-II gene affecting its mRNA expression and reproductive endocrine levels in female Japanese flounder (Paralichthys olivaceus). General and Comparative Endocrinology, 179(1): 107–114. Fang, Z., Tian, X., and Dong, S., 2016. The growth performance, osmotic physiology and carbohydrate metabolism activity of juvenile Cynoglossus semilaevis acclimated to low salinity water. Periodical of Ocean University of China, 46(8): 19–27. Fox, B. K., Breves, J. P., Davis, L. K., Pierce, A. L., Hirano, T., and Grau, E. G., 2009. Tissue-specific regulation of the growth hormone/insulin-like growth factor axis during fasting and refeeding: Importance of muscle expression of IGF-I and IGF-II mRNA in the tilapia. General and Comparative Endocrinology, 166(3): 573–580. Fu, B., Yu, X., Tong, J., Pang, M., Zhou, Y., Liu, Q., and Tao, W., 2019. Comparative transcriptomic analysis of hypothalamus-pituitary-liver axis in bighead carp (Hypophthalmichthys nobilis) with differential growth rate. BMC Genomics, 20(1): 328. Huang, C., Chao, P., and Lin, H., 2010. Na+/K+-ATPase and vacuolar-type H+-ATPase in the gills of the aquatic air-breathing fish Trichogaster microlepis in response to salinity variation. Comparative Biochemistry and Physiology Part A: Molecular & Integrative Physiology, 155(3): 309–318. Ji, X. S., Chen, S. L., Jiang, Y. L., Xu, T. J., Yang, J. F., and Tian, Y. S., 2011. Growth differences and differential expression analysis of pituitary adenylate cyclase activating polypeptide (PACAP) and growth hormon e-releasing hormone (GHRH) between the sexes in half-smooth tongue sole Cynoglossus semilaevis. General & Comparative Endocrinology, 170(1): 99–109. Karin, M., Liu, Z. G., and Zandi, E., 1997. AP-1 function and regulation. Current Opinion in Cell Biology, 9(2): 240–246. Koshiishi, Y., 1986. Effect of salinity on food intake, growth and feed efficiency of chum salmon, Oncorhynchus keta (Walbaum), and ayu Plecoglossus altivelis Temminck et Schlegel. Bulletin of the Japan Sea National Fisheries Research Institute, 36: 1–14. Li, S., He, F., Wen, H., Li, J., Si, Y., Liu, M., He, H., and Huang, Z., 2017a. Analysis of DNA methylation level by methylation-sensitive amplification polymorphism in half smooth tongue sole (Cynoglossus semilaevis) subjected to salinity stress. Journal of Ocean University of China, 16(2): 269–278. Li, S., He, F., Wen, H., Li, J., Si, Y., Liu, M., Huang, Y., and Meng, L., 2017b. Low salinity affects cellularity, DNA methylation, and mRNA expression of igf1 in the liver of half smooth tongue sole (Cynoglossus semilaevis). Fish Physiology & Biochemistry, 43(6): 1587–1602. Li, S., He, F., Wen, H., Si, Y., Liu, M., Huang, Y., and Wu, S., 2020. Half smooth tongue sole (Cynoglossus semilaevis) under low salinity stress can change hepatic igf2 expression through DNA methylation. Journal of Ocean University of China, 19(1): 171–182. Livak, K. J., and Schmittgen, T. D., 2001. Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCT method. Methods, 25(4): 402–408. Ma, Q., Liu, S., Zhuang, Z., Lin, L., Sun, Z., Liu, C., Su, Y., and Tang, Q., 2011. Genomic structure, polymorphism and expression analysis of growth hormone-releasing hormone and pituitary adenylate cyclase activating polypeptide genes in the half-smooth tongue sole (Cynoglossus semilaevis). Genetics & Molecular Research, 10(4): 3828–3846. Metzger, D. C. H., and Schulte, P. M., 2017. Persistent and plastic effects of temperature on DNA methylation across the genome of threespine stickleback (Gasterosteus aculeatus). Proceedings of the Royal Society B Biological Sciences, 284(1864): 20171667. Metzger, D. C. H., and Schulte, P. M., 2018. The DNA methylation landscape of stickleback reveals patterns of sex chromosome evolution and effects of environmental salinity. Genome Biology and Evolution, 10(3): 775–785. Montero, M., Yon, L., Rousseau, K., Arimura, A., Fournier, A., Dufour, S., and Vaudry, H., 1998. Distribution, characterization, and growth hormone-releasing activity of pituitary adenylate cyclase-activating polypeptide in the European eel, Anguilla anguilla. Endocrinology, 139(10): 4300–4310. Nan, X., Ng, H. H., Johnson, C. A., Laherty, C. D., Turner, B. M., Eisenman, R. N., and Bird, A., 1998. Transcriptional repression by the methyl-CpG-binding protein MeCP2 involves a histone deacetylase complex. Nature, 393(6683): 386–389. Navarro-Martín, L., Viñas, J., Ribas, L., Díaz, N., Gutiérrez, A., Di Croce, L., and Piferrer, F., 2011. DNA methylation of the gonadal aromatase (cyp19a) promoter is involved in temperature-dependent sex ratio shifts in the European sea bass. PLoS Genetics, 7(12): e1002447. Qian, Y., Yan, A., Lin, H., and Li, W., 2012. Molecular characterization of the GHRH/GHRH-R and its effect on GH synthesis and release in orange-spotted grouper (Epinephelus coioides). Comparative Biochemistry and Physiology, Part B, 163(1): 229–237. Schäfer, H., Zheng, J., Gundlach, F., Günther, R., and Schmidt, W. E., 1996. PACAP stimulates transcription of c-Fos and c-Jun and activates the AP-1 transcription factor in rat pancreatic carcinoma cells. Biochemical and Biophysical Research Communications, 221(1): 111–116. Si, Y., Ding, Y., He, F., Wen, H., Li, J., Zhao, J., and Huang, Z., 2016. DNA methylation level of cyp19a1a and Fox12 gene related to their expression patterns and reproduction traits during ovary development stages of Japanese flounder (Paralichthys olivaceus). Gene, 575(2): 321–330. Si, Y., He, F., Wen, H., Li, J., Zhao, J., Ren, Y., Zhao, M., Ji, L., Huang, Z., and Zhang, M., 2015. Genetic polymorphisms and DNA methylation in exon 1 CpG-rich regions of PACAP gene and its effect on mRNA expression and growth traits in half smooth tongue sole (Cynoglossus semilaevis). Fish Physiology & Biochemistry, 42(2): 407–421. Si, Y., Wen, H., Li, Y., He, F., Li, J., Li, S., and He, H., 2018. Liver transcriptome analysis reveals extensive transcriptional plasticity during acclimation to low salinity in Cynoglossus semilaevis. BMC Genomics, 19(1): 464. Tao, W., and Boulding, E., 2003. Associations between single nucleotide polymorphisms in candidate genes and growth rate in Arctic charr (Salvelinus alpinus L.). Heredity, 91(1): 60–69. Thanh, N. M., Jung, H., Lyons, R. E., Chand, V., Tuan, N. V., Thu, V. T. M., and Mather, P., 2014. A transcriptomic analysis of striped catfish (Pangasianodon hypophthalmus) in response to salinity adaptation: De novo assembly, gene annotation and marker discovery. Comparative Biochemistry and Physiology Part D: Genomics and Proteomics, 10: 52–63. Tian, X., Wang, G., Dong, S., and Fang, J., 2010. Effects of salinity and temperature on growth, osmophysiology and energy budget of tongue sole (Cynoglossus semilaevis Günther). Journal of Fishery Sciences of China, 17(4): 155–166. Varriale, A., and Bernardi, G., 2006. DNA methylation and body temperature in fishes. Gene, 385: 111–121. Vaudry, D., Falluel-Morel, A., Bourgault, S., Basille, M., Burel, D., Wurtz, O., Fournier, A., Chow, B. K. C., Hashimoto, H., Galas, L., and Vaudry, H., 2009. Pituitary adenylate cyclase-activating polypeptide and its receptors: 20 years after the discovery. Pharmacological Reviews, 61(3): 283–357. Wang, S., Wu, M., Chen, X., Jiang, Y., and Yan, Y., 2012. DsHsp90 is involved in the early response of Dunaliella salina to environmental stress. International Journal of Molecular Sciences, 13(7): 7963–7979. Wang, Y., Sun, L., Zhu, J., Zhao, Y., Wang, H., Liu, H., and Ji, X., 2017. Epigenetic control of cyp19a1a expression is critical for high temperature induced Nile tilapia masculinization. Journal of Thermal Biology, 69: 76–84. Wang, Y., Wang, C., Zhang, J., Chen, Y., and Zuo, Z., 2009. DNA hypomethylation induced by tributyltin, triphenyltin, and a mixture of these in Sebastiscus marmoratus liver. Aquatic Toxicology, 95(2): 93–98. Wang, Z., Huang, J., and Peng, B., 2003. Studies on critical salinity of survival and suitable growth salinity of Cynoglossus semilaevis Günther. Modern Fisheries Information, 18(12): 18–19. Watanabe, W. O., Ernst, D. H., Chasar, M. P., Wicklund, R. I., and Olla, B. L., 1993. The effects of temperature and salinity on growth and feed utilization of juvenile, sex-reversed male Florida red tilapia cultured in a recirculating system. Aquaculture, 112(4): 309–320. Wen, H., Si, Y., Zhang, Y., He, F., and Li, J., 2014. Cloning and expression of follistatin gene in half-smooth tongue sole Cynoglossus semilaevis during the reproduction cycle. Chinese Journal of Oceanology and Limnology, 33(2): 299–308. Xu, H., Cao, L., Zhang, Y., Johnson, R. B., Wei, Y., Zheng, K., and Liang, M., 2017. Dietary arachidonic acid differentially regulates the gonadal steroidogenesis in the marine teleost, tongue sole (Cynoglossus semilaevis), depending on fish gender and maturation stage. Aquaculture, 468: 378–385. Xu, Y., Liu, X., Ma, A., Sun, Z., and Zhuang, Z., 2005. Effects of salinity on embryonic development and growth of early life stages of Cynoglossus semilaevis Günther. Marine Sciences, 29(11): 39–43. Zhang, X., Wen, H., Wang, H., Ren, Y., Zhao, J., and Li, Y., 2017. RNA-Seq analysis of salinity stress-responsive transcriptome in the liver of spotted sea bass (Lateolabrax maculatus). PLoS One, 12(3): e0173238. Zhou, X., Zhu, G., Walilino, J. M., and Sun, J., 2001. Influence of Cu, Zn, Pb, Cd and their heavy metalion mixture on the DNA methylation level of the fish (Carassius auratus). China Environmental Science, 21(6): 549–552.