Transposon-induced epigenetic silencing in the X chromosome as a novel form of dmrt1 expression regulation during sex determination in the fighting fish

Background: Fishes are the one of the most diverse groups of animals with respect to their modes of sex determination, providing unique models for uncovering the evolutionary and molecular mechanisms underlying sex determination and reversal. Here, we have investigated how sex is determined in a spe...

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Main Authors: Wang, Le, Sun, Fei, Wan, Zi Yi, Yang, Zituo, Tay, Yi Xuan, Lee, May, Ye, Baoqing, Wen, Yanfei, Meng, Zining, Fan, Bin, Alfiko, Yuzer, Shen, Yubang, Piferrer, Francesc, Meyer, Axel, Schartl, Manfred, Yue, Gen Hua
Other Authors: School of Biological Sciences
Format: Article
Language:English
Published: 2022
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Online Access:https://hdl.handle.net/10356/161494
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Institution: Nanyang Technological University
Language: English
id sg-ntu-dr.10356-161494
record_format dspace
institution Nanyang Technological University
building NTU Library
continent Asia
country Singapore
Singapore
content_provider NTU Library
collection DR-NTU
language English
topic Science::Biological sciences
Teleost
Sex Determination
spellingShingle Science::Biological sciences
Teleost
Sex Determination
Wang, Le
Sun, Fei
Wan, Zi Yi
Yang, Zituo
Tay, Yi Xuan
Lee, May
Ye, Baoqing
Wen, Yanfei
Meng, Zining
Fan, Bin
Alfiko, Yuzer
Shen, Yubang
Piferrer, Francesc
Meyer, Axel
Schartl, Manfred
Yue, Gen Hua
Transposon-induced epigenetic silencing in the X chromosome as a novel form of dmrt1 expression regulation during sex determination in the fighting fish
description Background: Fishes are the one of the most diverse groups of animals with respect to their modes of sex determination, providing unique models for uncovering the evolutionary and molecular mechanisms underlying sex determination and reversal. Here, we have investigated how sex is determined in a species of both commercial and ecological importance, the Siamese fighting fish Betta splendens. Results: We conducted association mapping on four commercial and two wild populations of B. splendens. In three of the four commercial populations, the master sex determining (MSD) locus was found to be located in a region of ~ 80 kb on LG2 which harbours five protein coding genes, including dmrt1, a gene involved in male sex determination in different animal taxa. In these fish, dmrt1 shows a male-biased gonadal expression from undifferentiated stages to adult organs and the knockout of this gene resulted in ovarian development in XY genotypes. Genome sequencing of XX and YY genotypes identified a transposon, drbx1, inserted into the fourth intron of the X-linked dmrt1 allele. Methylation assays revealed that epigenetic changes induced by drbx1 spread out to the promoter region of dmrt1. In addition, drbx1 being inserted between two closely linked cis-regulatory elements reduced their enhancer activities. Thus, epigenetic changes, induced by drbx1, contribute to the reduced expression of the X-linked dmrt1 allele, leading to female development. This represents a previously undescribed solution in animals relying on dmrt1 function for sex determination. Differentiation between the X and Y chromosomes is limited to a small region of ~ 200 kb surrounding the MSD gene. Recombination suppression spread slightly out of the SD locus. However, this mechanism was not found in the fourth commercial stock we studied, or in the two wild populations analysed, suggesting that it originated recently during domestication. Conclusions: Taken together, our data provide novel insights into the role of epigenetic regulation of dmrt1 in sex determination and turnover of SD systems and suggest that fighting fish are a suitable model to study the initial stages of sex chromosome evolution.
author2 School of Biological Sciences
author_facet School of Biological Sciences
Wang, Le
Sun, Fei
Wan, Zi Yi
Yang, Zituo
Tay, Yi Xuan
Lee, May
Ye, Baoqing
Wen, Yanfei
Meng, Zining
Fan, Bin
Alfiko, Yuzer
Shen, Yubang
Piferrer, Francesc
Meyer, Axel
Schartl, Manfred
Yue, Gen Hua
format Article
author Wang, Le
Sun, Fei
Wan, Zi Yi
Yang, Zituo
Tay, Yi Xuan
Lee, May
Ye, Baoqing
Wen, Yanfei
Meng, Zining
Fan, Bin
Alfiko, Yuzer
Shen, Yubang
Piferrer, Francesc
Meyer, Axel
Schartl, Manfred
Yue, Gen Hua
author_sort Wang, Le
title Transposon-induced epigenetic silencing in the X chromosome as a novel form of dmrt1 expression regulation during sex determination in the fighting fish
title_short Transposon-induced epigenetic silencing in the X chromosome as a novel form of dmrt1 expression regulation during sex determination in the fighting fish
title_full Transposon-induced epigenetic silencing in the X chromosome as a novel form of dmrt1 expression regulation during sex determination in the fighting fish
title_fullStr Transposon-induced epigenetic silencing in the X chromosome as a novel form of dmrt1 expression regulation during sex determination in the fighting fish
title_full_unstemmed Transposon-induced epigenetic silencing in the X chromosome as a novel form of dmrt1 expression regulation during sex determination in the fighting fish
title_sort transposon-induced epigenetic silencing in the x chromosome as a novel form of dmrt1 expression regulation during sex determination in the fighting fish
publishDate 2022
url https://hdl.handle.net/10356/161494
_version_ 1759857556121976832
spelling sg-ntu-dr.10356-1614942023-02-28T17:11:34Z Transposon-induced epigenetic silencing in the X chromosome as a novel form of dmrt1 expression regulation during sex determination in the fighting fish Wang, Le Sun, Fei Wan, Zi Yi Yang, Zituo Tay, Yi Xuan Lee, May Ye, Baoqing Wen, Yanfei Meng, Zining Fan, Bin Alfiko, Yuzer Shen, Yubang Piferrer, Francesc Meyer, Axel Schartl, Manfred Yue, Gen Hua School of Biological Sciences Temasek Life Sciences Laboratory Department of Biological Sciences, National University of Singapore Science::Biological sciences Teleost Sex Determination Background: Fishes are the one of the most diverse groups of animals with respect to their modes of sex determination, providing unique models for uncovering the evolutionary and molecular mechanisms underlying sex determination and reversal. Here, we have investigated how sex is determined in a species of both commercial and ecological importance, the Siamese fighting fish Betta splendens. Results: We conducted association mapping on four commercial and two wild populations of B. splendens. In three of the four commercial populations, the master sex determining (MSD) locus was found to be located in a region of ~ 80 kb on LG2 which harbours five protein coding genes, including dmrt1, a gene involved in male sex determination in different animal taxa. In these fish, dmrt1 shows a male-biased gonadal expression from undifferentiated stages to adult organs and the knockout of this gene resulted in ovarian development in XY genotypes. Genome sequencing of XX and YY genotypes identified a transposon, drbx1, inserted into the fourth intron of the X-linked dmrt1 allele. Methylation assays revealed that epigenetic changes induced by drbx1 spread out to the promoter region of dmrt1. In addition, drbx1 being inserted between two closely linked cis-regulatory elements reduced their enhancer activities. Thus, epigenetic changes, induced by drbx1, contribute to the reduced expression of the X-linked dmrt1 allele, leading to female development. This represents a previously undescribed solution in animals relying on dmrt1 function for sex determination. Differentiation between the X and Y chromosomes is limited to a small region of ~ 200 kb surrounding the MSD gene. Recombination suppression spread slightly out of the SD locus. However, this mechanism was not found in the fourth commercial stock we studied, or in the two wild populations analysed, suggesting that it originated recently during domestication. Conclusions: Taken together, our data provide novel insights into the role of epigenetic regulation of dmrt1 in sex determination and turnover of SD systems and suggest that fighting fish are a suitable model to study the initial stages of sex chromosome evolution. Published version This study was supported by the internal funding of the Temasek Life Sciences Laboratory, Singapore. 2022-09-06T02:02:58Z 2022-09-06T02:02:58Z 2022 Journal Article Wang, L., Sun, F., Wan, Z. Y., Yang, Z., Tay, Y. X., Lee, M., Ye, B., Wen, Y., Meng, Z., Fan, B., Alfiko, Y., Shen, Y., Piferrer, F., Meyer, A., Schartl, M. & Yue, G. H. (2022). Transposon-induced epigenetic silencing in the X chromosome as a novel form of dmrt1 expression regulation during sex determination in the fighting fish. BMC Biology, 20(1), 5-. https://dx.doi.org/10.1186/s12915-021-01205-y 1741-7007 https://hdl.handle.net/10356/161494 10.1186/s12915-021-01205-y 34996452 2-s2.0-85122668529 1 20 5 en BMC Biology © The Author(s). 2021 Open Access. This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data. application/pdf