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DNA Methylation Profiling of Ovarian Tissue of Climbing Perch (Anabas testudienus) in Response to Monocrotophos Exposure

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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.

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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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Authors and Affiliations

  1. ICAR-Central Institute of Freshwater Aquaculture, Bhubaneswar, 751 002, Odisha, India

    Kiran D. Rasal, Sujata Mohapatra, Manohar Vasam, Rajesh Kumar & Jitendra Kumar Sundaray

  2. ICAR-Central Institute of Fisheries Education, Mumbai, 400 061, Maharashtra, India

    Kiran D. Rasal, Pokanti Vinay Kumar, Shasti Risha K, Prachi Asgolkar, Arpit Acharya, Diganta Dey & Siba Shinde

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  1. Kiran D. Rasal
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  11. Jitendra Kumar Sundaray
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Contributions

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.

Corresponding author

Correspondence to Jitendra Kumar Sundaray.

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The authors declare no competing interests.

Ethics Approval and Consent to Participate

All the animals used for this study approved and signed an informed consent agreement form by the Institute Animal Ethics Committee of ICAR-CIFA, Bhubaneswar, Odisha, India.

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The authors declare no competing interests.

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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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