Abstract
Epigenetic modifications like DNA methylation can alter an organism’s phenotype without changing its DNA sequence. Exposure to environmental toxicants has the potential to change the resilience of aquatic species. However, little information is available on the dynamics of DNA methylation in fish gonadal tissues in response to organophosphates. In the present work, reduced-representation bisulfite sequencing was performed to identify DNA methylation patterns in the ovarian tissues of Anabas testudienus exposed to organophosphates, specifically monocrotophos (MCP). Through sequencing, an average of 41,087 methylated cytosine sites were identified and distributed in different parts of genes, i.e., in transcription start sites (TSS), promoters, exons, etc. A total of 1058 and 1329 differentially methylated regions (DMRs) were detected as hyper-methylated and hypo-methylated in ovarian tissues, respectively. Utilizing whole-genome data of the climbing perch, the DMRs, and their associated overlapping genes revealed a total of 22 genes within exons, 45 genes at transcription start sites (TSS), and 218 genes in intergenic regions. Through gene ontology analysis, a total of 16 GO terms particularly involved in ovarian follicular development, response to oxidative stress, oocyte maturation, and multicellular organismal response to stress associated with reproductive biology were identified. After functional enrichment analysis, relevant DMGs such as steroid hormone biosynthesis (Cyp19a, 11-beta-HSD, 17-beta-HSD), hormone receptors (ar, esrrga), steroid metabolism (StAR), progesterone-mediated oocyte maturation (igf1ar, pgr), associated with ovarian development in climbing perch showed significant differential methylation patterns. The differentially methylated genes (DMGs) were subjected to analysis using real-time PCR, which demonstrated altered gene expression levels. This study revealed a molecular-level alteration in genes associated with ovarian development in response to chemical exposure. This work provides evidence for understanding the relationship between DNA methylation and gene regulation in response to chemicals that affect the reproductive fitness of aquatic animals.
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Data Availability
The generated data are available in the NCBI database. The accession numbers for our submissions are SRR22905449 and SRR22904546.
References
Akalin A, Kormaksson M, Li S, Garrett-Bakelman FE, Figueroa ME, Melnick A, Mason CE (2012) methylKit: a comprehensive R package for the analysis of genome-wide DNA methylation profiles. Genome Biol 13:R87. https://doi.org/10.1186/gb-2012-13-10-r87
Alavian-Ghavanini A, Rüegg J (2018) Understanding epigenetic effects of endocrine disrupting chemicals: from mechanisms to novel test methods. Basic Clin Pharmacol Toxicol 122:38–45
Aluru N, Kuo E, Helfrich LW, Karchner SI, Linney EA, Pais JE, Franks DG (2015) Developmental exposure to 2,3,7,8-tetrachlorodibenzo-p-dioxin alters DNA methyltransferase (dnmt) expression in zebrafish (Danio rerio). Toxicol Appl Pharmacol 284:142–151
Aluru N, Karchner SI, Krick KS, Zhu W, Liu J (2018) Role of DNA methylation in altered gene expression patterns in adult zebrafish (Danio rerio) exposed to 3, 3′, 4, 4′, 5-pentachlorobiphenyl (PCB 126). Environ Epigen 4. https://doi.org/10.1093/eep/dvy005
Aniagu SO, Williams TD, Allen Y, Katsiadaki I, Chipman JK (2008) Global genomic methylation levels in the liver and gonads of the three-spine stickleback (Gasterosteus aculeatus) after exposure to hexabromocyclododecane and 17-beta oestradiol. Environ Int 34:310–317
Anqi Y, Saina Y, Chujie C, Yanfei Y, Xiangwei T, Jiajia M, Jiaojiao X, Maoliang R, Bin C (2022) Regulation of DNA methylation during the testicular development of Shaziling pigs. Genomics 114:110450. https://doi.org/10.1016/j.ygeno.2022.110450
Apha, (2005) Standard Methods for Examinations of Water and Wastewater, 21st edn. APHA, AWWA and WEF DC, Washington
Astm (1990) American Society for Testing of Materials method 729–90: 1990 Guide for conducting acute toxicity test with fishes, macroinvertebrates and pesticide on growth and survival of African catfish, amphibians
Beemelmanns A, Ribas L, Anastasiadi D, Moraleda-Prados J, Zanuzzo FS, Rise ML, Gamperl AK (2021) DNA methylation dynamics in Atlantic salmon (Salmo salar) challenged with high temperature and moderate hypoxia. 7. https://doi.org/10.3389/fmars.2020.604878
Beketov MA, Kefford BJ, Schäfer RB, Liess M (2013) Pesticides Reduce Regional Biodiversity of Stream Invertebrates 110:11039–11043. https://doi.org/10.1073/pnas.1305618110
Best C, Ikert H, Kostyniuk DJ, Craig PM, Navarro-Martin L, Marandel L, Mennigen JA (2018) Epigenetics in teleost fish: from molecular mechanisms to physiological phenotypes. Comp Biochem Physiol B Biochem Mol Biol 224:210–244
Bharti S, Rasool F (2021) Analysis of the biochemical and histopathological impact of a mild dose of commercial malathion on Channa punctatus (Bloch) fish. Toxicol Rep 8:443–455
Brander SM, Biales AD, Connon RE (2017) The role of epigenomics in aquatic toxicology. Environ Toxicol Chem 36:2565–2573
Chandhini S, Rejish Kumar VJ (2019) Transcriptomics in aquaculture: current status and applications. Rev Aquac 11:1379–1397
Corrales J, Fang X, Thornton C, Mei W, Barbazuk WB, Duke M, Scheffler BE, Willett KL (2014) Effects on specific promoter DNA methylation in zebrafish embryos and larvae following benzo[a]pyrene exposure. Comp Biochem Physiol C Toxicol Pharmacol 163:37–46
Edwards JR, Yarychkivska O, Boulard M, Bestor TH (2017) DNA methylation and DNA methyltransferases. Epigenetics Chromatin 10:23. https://doi.org/10.1186/s13072-017-0130-8
Falconer L, Hjøllo SS, Telfer TC, Mcadam BJ, Hermansen Ø, Ytteborg E (2020) The importance of calibrating climate change projections to local conditions at aquaculture sites. Aquaculture 514:734487. https://doi.org/10.1016/j.aquaculture.2019.734487
Fao (2019) Food and Agricultural Organization. Yearbook of Fishery and Aquaculture Statistics 2019
Feng K, Cui X, Song Y, Tao B, Chen J, Wang J, Liu S, Sun Y, Zhu Z, Trudeau VL, Hu W (2019) Gnrh3 regulates PGC proliferation and sex differentiation in developing zebrafish. Endocrinology 161. https://doi.org/10.1210/endocr/bqz024
Fetke JK, Martinson JW, Flick RW, Huang W, Bencic DC, See MJ, Pilgrim EM, Debry RW, Biales AD (2021) DNA methylation and expression of estrogen receptor alpha in fathead minnows exposed to 17α-ethynylestradiol. Aquat Toxicol 233:105788. https://doi.org/10.1016/j.aquatox.2021.105788
Finney DJ (1971) Probit analysis. Cambridge University Press, London. J Pharma Sci 68–72. https://doi.org/10.1002/jps.2600600940
Fürbass, R., Selimyan, R. & Vanselow, J. (2008). DNA methylation and chromatin accessibility of the proximal Cyp19 promoter region 1.5/2 correlate with expression levels in sheep placentomes. 75:1–7.https://doi.org/10.1002/mrd.20756
Gao D, Lin J, Ou K, Chen Y, Li H, Dai Q, Yu Z, Zuo Z, Wang C (2018) Embryonic exposure to benzo(a)pyrene inhibits reproductive capability in adult female zebrafish and correlation with DNA methylation. Environ Pollut 240:403–411
Gavery MR, Nichols KM, Berejikian BA, Tatara CP, Goetz GW, Dickey JT, Van Doornik DM, Swanson P (2019) Temporal dynamics of DNA methylation patterns in response to rearing juvenile steelhead (Oncorhynchus mykiss) in a hatchery versus simulated stream environment. 10:356
Gavery MR, Roberts SB (2017) Epigenetic Considerations in Aquaculture Peerj 5:e4147. https://doi.org/10.7717/peerj.4147
Goll MG, Halpern ME (2011) DNA methylation in zebrafish. Prog Mol Biol Transl Sci 101:193–218
Guiguen Y, Fostier A, Piferrer F, Chang CF (2010) Ovarian aromatase and estrogens: a pivotal role for gonadal sex differentiation and sex change in fish. Gen Comp Endocrinol 165:352–366
Hanna RN, Daly SC, Pang Y, Anglade I, Kah O, Thomas P, Zhu Y (2010) Characterization and expression of the nuclear progestin receptor in zebrafish gonads and brain. Biol Reprod 82:112–122
Heras J (2020) Fish transcriptomics: applied to our understanding of aquaculture. Preprints 2020010332 https://doi.org/10.20944/preprints202001.0332.v1
Hu Q, Ao Q, Tan Y, Gan X, Luo Y, Zhu J (2020) Genome-wide DNA methylation and RNA analysis reveal potential mechanism of resistance to Streptococcus agalactiae in GIFT strain of Nile tilapia (Oreochromis niloticus). J Immunol 204:3182–3190
Huang S, Wu Y, Chen K, Zhang X, Zhao J, Luo Q, Liu H, Wang F, Li K, Fei S, Zhang X, Ou M (2023) Gene Expression and Epigenetic Modification of Aromatase during Sex Reversal and Gonadal Development in Blotched Snakehead (channa Maculata) 8:129
Jones PA (2012) Functions of DNA methylation: islands, start sites, gene bodies and beyond. Nat Rev Genet 13:484–492
Karunarathne A, Bhalla A, Sethi A, Perera U, Eddleston M (2021) Importance of pesticides for lethal poisoning in India during 1999 to 2018: a systematic review. BMC Public Health 21:1441. https://doi.org/10.1186/s12889-021-11156-2
Kelley JL, Tobler M, Beck D, Sadler-Riggleman I, Quackenbush CR, Arias Rodriguez L, Skinner MK (2021) Epigenetic inheritance of DNA methylation changes in fish living in hydrogen sulfide-rich springs. Proc Natl Acad Sci USA 118. https://doi.org/10.1073/pnas.2014929118
Khatib I, Rychter P, Falfushynska H (2022) Pesticide pollution: detrimental outcomes and possible mechanisms of fish exposure to common organophosphates and triazines. Journal of Xenobiotics 12:236–265
Knower KC, To SQ, Simpson ER, Clyne CDJM, Endocrinology C (2010) Epigenetic mechanisms regulating CYP19 transcription in human breast adipose fibroblasts. 321:123–130
Korkmaz C, Donmez AE (2017) Effects of diazinon on 17 beta-estradiol, plasma vitellogenin and liver and gonad tissues of common carp (Cyprinus carpio, L., 1758). Turk J Fish Aquat Sci 17:629–640
Kossack ME, High SK, Hopton RE, Yan Y-L, Postlethwait JH, Draper BW (2018) Female sex development and reproductive duct formation depend on Wnt4a in zebrafish. Genetics 211:219–233
Kumar K, L.P.L., Sahoo M, Mohanty U L, Kumar R, Sahu a K, (2013) Length-weight relationship and condition factor of Anabas testudineus and Channa species under different culture systems. World J Fish Mar Sci 5:74–78
Kumar K, M.U.L., Kumar R, Damle D, Noor Jahan, Jena J K, Eknath a E, (2012) Culture of freshwater climbing perch, Anabas testudineus. Aquac Asia 17:27–28
Kuo M-W, Lou S-W, Postlethwait J, Chung B-C (2005) Chromosomal organization, evolutionary relationship, and expression of zebrafish GnRH family members. J Biomed Sci 12:629–639
Kurdyukov S, Bullock M (2016) DNA Methylation Analysis: Choosing the Right Method 5:3
Law JA, Jacobsen SE (2010) Establishing, maintaining and modifying DNA methylation patterns in plants and animals. Nat Rev Genet 11:204–220
Leerberg DM, Sano K, Draper BW (2017) Fibroblast growth factor signaling is required for early somatic gonad development in zebrafish. PLoS Genet 13:e1006993. https://doi.org/10.1371/journal.pgen.1006993
Lethimonier C, Madigou T, Muñoz-Cueto J-A, Lareyre J-J, Kah O (2004) Evolutionary aspects of GnRHs, GnRH neuronal systems and GnRH receptors in teleost fish. Gen Comp Endocrinol 135:1–16
Li L, Dong J, Yan L, Yong J, Liu X, Hu Y, Fan X, Wu X, Guo H, Wang X, Zhu X, Li R, Yan J, Wei Y, Zhao Y, Wang W, Ren Y, Yuan P, Yan Z, Hu B, Guo F, Wen L, Tang F, Qiao J (2017) Single-cell RNA-Seq analysis maps development of human germline cells and gonadal niche interactions. Cell Stem Cell 20:858-873.e4
Li P, Chen J, Zhu C, Pan Z, Li Q, Wei H, Wang G, Cheng W, Fu B, Sun Y (2022) DNA methylation difference between female and male ussuri catfish (Pseudobagrus ussuriensis) in Brain and Gonad Tissues. 12:874
Liu, Z., Zhou, T. & Gao, D. (2022). Genetic and epigenetic regulation of growth, reproduction, disease resistance and stress responses in aquaculture. 13. https://doi.org/10.3389/fgene.2022.994471
Livak KJ, Schmittgen TDJM (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCT method. Methods 25:402–408
Lou S, Lee H-M, Qin H, Li J-W, Gao Z, Liu X, Chan LL, Kl Lam V, So W-Y, Wang Y, Lok S, Wang J, Ma RCW, Tsui SK-W, Chan JCN, Chan T-F, Yip KY (2014) Whole-genome bisulfite sequencing of multiple individuals reveals complementary roles of promoter and gene body methylation in transcriptional regulation. Genome Biol 15:408. https://doi.org/10.1186/s13059-014-0408-0
Lubzens E, Young G, Bobe J, Cerdà J (2010) Oogenesis in teleosts: how fish eggs are formed. Gen Comp Endocrinol 165:367–389
Lushchak VI, Matviishyn TM, Husak VV, Storey JM, Storey KB (2018) Pesticide toxicity: a mechanistic approach. EXCLI J 17:1101–1136
Mirbahai L, Yin G, Bignell JP, Li N, Williams TD, Chipman JK (2011) DNA methylation in liver tumorigenesis in fish from the environment. Epigenetics 6:1319–1333
Mohapatra S, Kumar R, Patnaik ST, Mishra CS, Sahoo L, Sundaray JK (2020) Changes in ovary and testis and breeding fitness of the climbing perch, Anabas testudineus (Bloch, 1792), exposed to sub-lethal concentrations of monocrotophos. Aquac Res 51:3230–3236
Mohapatra S, Kumar R, Sundaray JK, Patnaik ST, Mishra CSK, Rather MA (2021) Structural damage in liver, gonads, and reduction in spawning performance and alteration in the haematological parameter of Anabas testudineus by glyphosate- a herbicide. 52:1150–1159.https://doi.org/10.1111/are.14973
Monga R, Ghai S, Datta TK, Singh D (2011) Tissue-specific promoter methylation and histone modification regulate CYP19 gene expression during folliculogenesis and luteinization in buffalo ovary. Gen Comp Endocrinol 173:205–215
Moore LD, Le T, Fan G (2013) DNA methylation and its basic function. Neuropsychopharmacol: offic public Am College Neuropsychopharmacol 38:23–38.
Navarro-Martín L, Viñas J, Ribas L, Díaz N, Gutiérrez A, Di Croce L, 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 Genet 7:e1002447. https://doi.org/10.1371/journal.pgen.1002447
Oecd (1992) Organization for Economic Co-operation and Development (OECD). Guideline 203. OECD Guideline for Testing of Chemicals: Fish, Acute Toxicity Test
Ogino Y, Ansai S, Watanabe E, Yasugi M, Katayama Y, Sakamoto H, Okamoto K, Okubo K, Yamamoto Y, Hara I, Yamazaki T, Kato A, Kamei Y, Naruse K, Ohta K, Ogino H, Sakamoto T, Miyagawa S, Sato T, Yamada G, Baker ME, Iguchi T (2023) Evolutionary differentiation of androgen receptor is responsible for sexual characteristic development in a teleost fish. Nat Commun 14:1428. https://doi.org/10.1038/s41467-023-37026-6
Olsvik PA, Williams TD, Tung HS, Mirbahai L, Sanden M, Skjaerven KH, Ellingsen S (2014) Impacts of TCDD and MeHg on DNA methylation in zebrafish (Danio rerio) across two generations. Comp Biochem Physiol C Toxicol Pharmacol 165:17–27
Olsvik PA, Whatmore P, Penglase SJ, Skjærven KH, Anglès D’auriac M, Ellingsen S (2019) Associations between behavioral effects of bisphenol A and DNA methylation in zebrafish embryos. Front Genet 10:184. https://doi.org/10.3389/fgene.2019.00184
Ortiz-Delgado JB, Funes V, Albendín G, Scala E, Sarasquete C (2021) Toxicity of malathion during Senegalese sole, Solea senegalensis larval development and metamorphosis: histopathological disorders and effects on type B esterases and CYP1A enzymatic systems. 36:1894–1910.https://doi.org/10.1002/tox.23310
Paksa A, Raz E (2015) Zebrafish germ cells: motility and guided migration. Curr Opin Cell Biol 36:80–85
Pamanji R, Bethu MS, Yashwanth B, Leelavathi S, Venkateswara Rao J (2015) Developmental toxic effects of monocrotophos, an organophosphorous pesticide, on zebrafish (Danio rerio) embryos. Environ Sci Pollut Res 22:7744–7753
Pan Y, Chen L, Cheng J, Zhu X, Wu P, Bao L, Chu W, He S, Liang X, Zhang J (2021) Genome-wide DNA methylation profiles provide insight into epigenetic regulation of red and white muscle development in Chinese perch Siniperca chuatsi. Comp Biochem Physiol B: Biochem Mol Biol 256:110647. https://doi.org/10.1016/j.cbpb.2021.110647
Pan Z, Wang X, Di R, Liu Q, Hu W, Cao X, Guo X, He X, Lv S, Li F, Wang H, Chu M (2018) A 5-methylcytosine site of growth differentiation factor 9 (GDF9) gene affects its tissue-specific expression in sheep. 8:200
Paul BN, Chanda S, Bhowmick S, Sridhar N, Saha GS, Gir SS (2017) Nutrient profile of indian climbing perch, Anabas testudineus
Rani G, Kumaraguru AK (2014) Behavioural responses and acute toxicity of Clarias batrachus to synthetic pyrethroid insecticide, λ-cyhalothrin. SAARC J Agri 15:99–109
Shi R, Li X, Cheng P, Yang Q, Chen Z, Chen S, Wang N (2022) Characterization of growth differentiation factor 9 and bone morphogenetic factor 15 in Chinese tongue sole (Cynoglossus semilaevis): sex-biased expression pattern and promoter regulation. Theriogenology 182:119–128
Smith J, Sen S, Weeks RJ, Eccles MR, Chatterjee A (2020) Promoter DNA hypermethylation and paradoxical gene activation. Trends in Cancer 6:392–406
Stadlinger N, Berg H, Van Den Brink PJ, Tam NT, Gunnarsson JS (2018) Comparison of predicted aquatic risks of pesticides used under different rice-farming strategies in the Mekong Delta. Vietnam Environ Sci Pollut Res 25:13322–13334
Stopa N, Krebs JE, Shechter D (2015) The PRMT5 arginine methyltransferase: many roles in development, cancer and beyond. Cell Mol Life Sci 72:2041–2059
Sudhagar A, Kumar G, El-Matbouli M (2018a) Transcriptome Analysis Based on RNA-Seq in Understanding Pathogenic Mechanisms of Diseases and the Immune System of Fish: a Comprehensive Review 19:245
Sudhagar A, Kumar G, El-Matbouli M (2018b) Transcriptome analysis based on RNA-Seq in understanding pathogenic mechanisms of diseases and the immune system of fish: a comprehensive review. Int J Mol Sci 19. https://doi.org/10.3390/ijms19010245
Sundaray JK, Dixit S, Rather A, Rasal KD, Sahoo L (2022) Aquaculture omics: an update on the current status of research and data analysis. Mar Genomics 64:100967. https://doi.org/10.1016/j.margen.2022.100967
Terrazas-Salgado L, García-Gasca A, Betancourt-Lozano M, Llera-Herrera R, Alvarado-Cruz I, Yáñez-Rivera B (2022) Epigenetic transgenerational modifications induced by xenobiotic exposure in zebrafish. Frontiers in Cell and Developmental Biology 10:832982. https://doi.org/10.3389/fcell.2022.832982
Tian H, Ru S, Wang Z, Cai W, Wang W (2009) Estrogenic effects of monocrotophos evaluated by vitellogenin mRNA and protein induction in male goldfish (Carassius auratus). Comp Biochem Physiol C Toxicol Pharmacol 150:231–236
Tian H, Sun Y, Wang H, Bing X, Wang W, Ru S (2017) Monocrotophos pesticide affects synthesis and conversion of sex steroids through multiple targets in male goldfish (Carassius auratus). Sci Rep 7:2306. https://doi.org/10.1038/s41598-017-01935-6
Tripurani SK, Wee G, Lee K-B, Smith GW, Wang L, Jianboyao, (2013) MicroRNA-212 post-transcriptionally regulates oocyte-specific basic-helix-loop-helix transcription factor, factor in the germline alpha (FIGLA), during bovine early embryogenesis. PLoS ONE 8:e76114. https://doi.org/10.1371/journal.pone.0076114
Velmurugan B, Selvanayagam M, Cengiz EI, Unlu E (2007) The effects of monocrotophos to different tissues of freshwater fish Cirrhinus mrigala. Bull Environ Contam Toxicol 78:450–454
Venney CJ, Wellband KW, Heath DD (2021) Rearing environment affects the genetic architecture and plasticity of DNA methylation in Chinook salmon. Heredity (edinb) 126:38–49
Wang S, Bryan C, Xie J, Zhao H, Lin LF, Tai, J.a.C., Horzmann, K.A., Sanchez, O.F., Zhang, M., Freeman, J.L. & Yuan, C. (2022) Atrazine exposure in zebrafish induces aberrant genome-wide methylation. Neurotoxicol Teratol 92:107091. https://doi.org/10.1016/j.ntt.2022.107091
Wang X, Bhandari RK (2020) DNA methylation reprogramming in medaka fish, a promising animal model for environmental epigenetics research. Environ Epigen 6:dvaa008. https://doi.org/10.1093/eep/dvaa008
Xin F, Susiarjo M, Bartolomei MS (2015) Multigenerational and transgenerational effects of endocrine disrupting chemicals: a role for altered epigenetic regulation? Semin Cell Dev Biol 43:66–75
Xiu Y, Shao C, Zhu Y, Li Y, Gan T, Xu W, Piferrer, F, Chen S (2019) Differences in DNA methylation between disease-resistant and disease-susceptible Chinese tongue sole (Cynoglossus semilaevis) families. 10. https://doi.org/10.3389/fgene.2019.00847
Xu Q, Lin H-Y, Yeh S-D, Yu IC, Wang R-S, Chen Y-T, Zhang C, Altuwaijri S, Chen L-M, Chuang K-H, Chiang H-S, Yeh S, Chang C (2007) Infertility with defective spermatogenesis and steroidogenesis in male mice lacking androgen receptor in Leydig cells. Endocrine 32:96–106
Xu N, Chua AK, Jiang H, Liu N-A, Goodarzi MO (2014) Early embryonic androgen exposure induces transgenerational epigenetic and metabolic changes. Mol Endocrinol 28:1329–1336
Yang J, Liu M, Zhou T, Li Q, Lin Z (2023) Transcriptome and methylome dynamics in the gills of large yellow croaker (Larimichthys crocea) during low-salinity adaption. 10. https://doi.org/10.3389/fmars.2023.1082655
Yi SV (2017) Insights into epigenome evolution from animal and plant methylomes. Genome Biol Evol 9:3189–3201
Yilmaz O, Patinote A, Nguyen T, Com E, Pineau C, Bobe J (2019) Genome Editing Reveals Reproductive and Developmental Dependencies on Specific Types of Vitellogenin in Zebrafish (danio Rerio) 86:1168–1188. https://doi.org/10.1002/mrd.23231
Yu Y, Han Y, Niu R, Wang J, Manthari RK, Ommati MM, Sun Z (2018) Ameliorative effect of VE, IGF-I, and hCG on the fluoride-induced testosterone release suppression in mice Leydig cells. Biol Trace Elem Res 181:95–103
Zhang X, Gao L, Yang K, Tian H, Wang W, Ru S (2013) Monocrotophos pesticide modulates the expression of sexual differentiation genes and causes phenotypic feminization in zebrafish (Danio rerio). Comp Biochem Physiol C Toxicol Pharmacol 157:33–40
Zhang T, Guan Y, Wang S, Wang L, Cheng M, Yuan C, Liu Y, Wang Z (2018a) Bisphenol A induced abnormal DNA methylation of ovarian steroidogenic genes in rare minnow Gobiocypris rarus. Gen Comp Endocrinol 269:156–165
Zhang X, Liu W, Wang J, Tian H, Wang W, Ru S (2018b) Quantitative analysis of in-vivo responses of reproductive and thyroid endpoints in male goldfish exposed to monocrotophos pesticide. Comp Biochem Physiol C: Toxicol Pharmacol 211:41–47
Zhao F, Wang B, Zhang X, Tian H, Wang W, Ru S (2015) Induction of DNA base damage and strand breaks in peripheral erythrocytes and the underlying mechanism in goldfish (Carassius auratus) exposed to monocrotophos. Fish Physiol Biochem 41:613–624
Zhao F, Wei P, Wang J, Yu M, Zhang X, Tian H, Wang W, Ru S (2017) Estrogenic effects associated with bisphenol a exposure in male zebrafish (Danio rerio) is associated with changes of endogenous 17β-estradiol and gene specific DNA methylation levels. Gen Comp Endocrinol 252:27–35
Zhou H, Zhuang Z-X, Sun Y-Q, Chen Q, Zheng X-Y, Liang Y-T, Mahboob S, Wang Q, Zhang R, Al-Ghanim KA, Shao C-W, Li Y-J (2019) Changes in DNA methylation during epigenetic-associated sex reversal under low temperature in Takifugu rubripes. PLoS ONE 14:e0221641. https://doi.org/10.1371/journal.pone.0221641
Zhu J, Zhang D, Liu X, Yu G, Cai X, Xu C, Rong F, Ouyang G, Wang J, Xiao W (2019) Zebrafish prmt5 arginine methyltransferase is essential for germ cell development. Development 146. https://doi.org/10.1242/dev.179572
Acknowledgements
The authors are thankful to the Director, Indian Council of Agricultural Research-CIFA, Bhubaneswar, Odisha, India, for providing the research facility and the Director, Indian Council of Agricultural Research-CIFE, Mumbai, for providing the facility for data analysis.
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Conceptualization: J.K.S; Methodology: J.K.S, K.D.R, R.K, S.M, P.V.K, S.S; Investigation: K.D.R, J.K.S; Data processing: K.D.R, M.V; Writing—original draft preparation: K.D.R, S.R, M.V, J.K.S, P.V.K; Writing—review and editing: K.D.R, S.R, J.K.S, M.V; Result validation: K.D.R, A.A, D.D, P.A, S.S; Resources: J.K.S, K.D.R; Supervision: J.K.S.
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Rasal, K.D., Mohapatra, S., Kumar, P.V. et al. DNA Methylation Profiling of Ovarian Tissue of Climbing Perch (Anabas testudienus) in Response to Monocrotophos Exposure. Mar Biotechnol 25, 1123–1135 (2023). https://doi.org/10.1007/s10126-023-10264-x
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DOI: https://doi.org/10.1007/s10126-023-10264-x