Epigenetic modification and inheritance in sexual reversal of fish
- Changwei Shao1,8,
- Qiye Li2,3,4,5,8,
- Songlin Chen1,8,9,
- Pei Zhang2,
- Jinmin Lian2,
- Qiaomu Hu1,
- Bing Sun1,
- Lijun Jin2,
- Shanshan Liu1,
- Zongji Wang2,3,
- Hongmei Zhao2,
- Zonghui Jin2,
- Zhuo Liang1,
- Yangzhen Li1,
- Qiumei Zheng2,
- Yong Zhang2,
- Jun Wang2,6,7 and
- Guojie Zhang2,4,9
- 1Yellow Sea Fisheries Research Institute, CAFS, Key Lab for Sustainable Development of Marine Fisheries, Ministry of Agriculture, Qingdao 266071, China;
- 2China National Genebank, BGI-Shenzhen, Shenzhen 518083, China;
- 3School of Bioscience and Bioengineering, South China University of Technology, Guangzhou 510006, China;
- 4Centre for Social Evolution, Department of Biology, University of Copenhagen, DK-2100 Copenhagen, Denmark;
- 5Centre for GeoGenetics, Natural History Museum of Denmark, University of Copenhagen, 1350 Copenhagen K, Denmark;
- 6Department of Biology, University of Copenhagen, DK-2200 Copenhagen, Denmark;
- 7King Abdulaziz University, Jeddah 22254, Saudi Arabia
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↵8 These authors contributed equally to this work.
Abstract
Environmental sex determination (ESD) occurs in divergent, phylogenetically unrelated taxa, and in some species, co-occurs with genetic sex determination (GSD) mechanisms. Although epigenetic regulation in response to environmental effects has long been proposed to be associated with ESD, a systemic analysis on epigenetic regulation of ESD is still lacking. Using half-smooth tongue sole (Cynoglossus semilaevis) as a model—a marine fish that has both ZW chromosomal GSD and temperature-dependent ESD—we investigated the role of DNA methylation in transition from GSD to ESD. Comparative analysis of the gonadal DNA methylomes of pseudomale, female, and normal male fish revealed that genes in the sex determination pathways are the major targets of substantial methylation modification during sexual reversal. Methylation modification in pseudomales is globally inherited in their ZW offspring, which can naturally develop into pseudomales without temperature incubation. Transcriptome analysis revealed that dosage compensation occurs in a restricted, methylated cytosine enriched Z chromosomal region in pseudomale testes, achieving equal expression level in normal male testes. In contrast, female-specific W chromosomal genes are suppressed in pseudomales by methylation regulation. We conclude that epigenetic regulation plays multiple crucial roles in sexual reversal of tongue sole fish. We also offer the first clues on the mechanisms behind gene dosage balancing in an organism that undergoes sexual reversal. Finally, we suggest a causal link between the bias sex chromosome assortment in the offspring of a pseudomale family and the transgenerational epigenetic inheritance of sexual reversal in tongue sole fish.
Footnotes
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↵9 Corresponding authors
E-mail zhanggj{at}genomics.cn
E-mail chensl{at}ysfri.ac.cn
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[Supplemental material is available for this article.]
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Article published online before print. Article, supplemental material, and publication date are at http://www.genome.org/cgi/doi/10.1101/gr.162172.113.
- Received June 17, 2013.
- Accepted January 23, 2014.
This article is distributed exclusively by Cold Spring Harbor Laboratory Press for the first six months after the full-issue publication date (see http://genome.cshlp.org/site/misc/terms.xhtml). After six months, it is available under a Creative Commons License (Attribution-NonCommercial 3.0 Unported), as described at http://creativecommons.org/licenses/by-nc/3.0/.
