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Genome-Wide DNA Methylation and RNA Analysis Reveal Potential Mechanism of Resistance to Streptococcus agalactiae in GIFT Strain of Nile Tilapia (Oreochromis niloticus)

Qiaomu Hu, Qiuwei Ao, Yun Tan, Xi Gan, Yongju Luo and Jiajie Zhu
J Immunol April 24, 2020, ji1901496; DOI: https://doi.org/10.4049/jimmunol.1901496
Qiaomu Hu
*Yangtze River Fisheries Research Institute, Chinese Academy of Fishery Sciences, Wuhan, Hubei 430223, China; and
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Qiuwei Ao
†Guangxi Academy of Fishery Sciences, Guangxi Key Laboratory of Aquatic Genetic Breeding and Healthy Aquaculture, Nanning, Guangxi 530021, China
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Yun Tan
†Guangxi Academy of Fishery Sciences, Guangxi Key Laboratory of Aquatic Genetic Breeding and Healthy Aquaculture, Nanning, Guangxi 530021, China
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Xi Gan
†Guangxi Academy of Fishery Sciences, Guangxi Key Laboratory of Aquatic Genetic Breeding and Healthy Aquaculture, Nanning, Guangxi 530021, China
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Yongju Luo
†Guangxi Academy of Fishery Sciences, Guangxi Key Laboratory of Aquatic Genetic Breeding and Healthy Aquaculture, Nanning, Guangxi 530021, China
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Jiajie Zhu
†Guangxi Academy of Fishery Sciences, Guangxi Key Laboratory of Aquatic Genetic Breeding and Healthy Aquaculture, Nanning, Guangxi 530021, China
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Key Points

  • Whole-genome bisulfite sequencing distinguishes between resistant and susceptible O. niloticus.

  • Promoter methylation regulates gene expression in immune-related genes.

Abstract

Streptococcus agalactiae is an important pathogenic bacterium causing great economic loss in Nile tilapia (Oreochromis niloticus) culture. Resistant and susceptible groups sharing the same genome showed significantly different resistance to S. agalactiae in the genetically improved farmed tilapia strain of Nile tilapia. The resistance mechanism is unclear. We determined genome-wide DNA methylation profiles in spleen of resistant and susceptible O. niloticus at 5 h postinfection with S. agalactiae using whole-genome bisulfite sequencing. The methylation status was higher in the spleen samples from resistant fish than in the susceptible group. A total of 10,177 differentially methylated regions were identified in the two groups, including 3725 differentially methylated genes (DMGs) (3129 hyper-DMGs and 596 hypo-DMGs). The RNA sequencing showed 2374 differentially expressed genes (DEGs), including 1483 upregulated and 891 downregulated. Integrated analysis showed 337 overlapping DEGs and DMGs and 82 overlapping DEGs and differentially methylated region promoters. By integrating promoter DNA methylation with gene expression, we revealed four immune-related genes (Arnt2, Nhr38, Pcdh10, and Ccdc158) as key factors in epigenetic mechanisms contributing to pathogen resistance. Our study provided systematic methylome maps to explore the epigenetic mechanism and reveal the methylation loci of pathogen resistance and identified methylation-regulated genes that are potentially involved in defense against pathogens.

Footnotes

  • This work was supported by the National Key Research and Development Program of China (2018YFD0900302-5), the Major Science and Technology Projects of Guangxi (AA17204080-2), the Guangxi Nature Fund Program (2018JJA130220), the Guangxi Key Laboratory of Aquatic Genetic Breeding and Healthy Aquaculture Program (GXIF2019A03-01), and the Major Science and Technology Projects of Nanning (20192242).

  • The sequence data presented in this article have been submitted to the GenBank under accession numbers SRP220470 and SRP220463.

  • The online version of this article contains supplemental material.

  • Received December 19, 2019.
  • Accepted April 7, 2020.
  • Copyright © 2020 by The American Association of Immunologists, Inc.

This article is distributed under The American Association of Immunologists, Inc., Reuse Terms and Conditions for Author Choice articles.

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The Journal of Immunology: 206 (3)
The Journal of Immunology
Vol. 206, Issue 3
1 Feb 2021
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Genome-Wide DNA Methylation and RNA Analysis Reveal Potential Mechanism of Resistance to Streptococcus agalactiae in GIFT Strain of Nile Tilapia (Oreochromis niloticus)
Qiaomu Hu, Qiuwei Ao, Yun Tan, Xi Gan, Yongju Luo, Jiajie Zhu
The Journal of Immunology April 24, 2020, ji1901496; DOI: 10.4049/jimmunol.1901496

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Genome-Wide DNA Methylation and RNA Analysis Reveal Potential Mechanism of Resistance to Streptococcus agalactiae in GIFT Strain of Nile Tilapia (Oreochromis niloticus)
Qiaomu Hu, Qiuwei Ao, Yun Tan, Xi Gan, Yongju Luo, Jiajie Zhu
The Journal of Immunology April 24, 2020, ji1901496; DOI: 10.4049/jimmunol.1901496
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