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

16 pages, 6 figures, supplementary Information https://doi.org/10.1186/s12915-021-01205-y.-- Availability of data and materials: Sequences used for RAD, RNA, and genome sequencing are achieved in the DDBJ Sequencing Read Archive (SRA) database under BioProject ID: PRJDB7253- PRJDB7255 [23, 88]

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Main Authors: Wang, Le, Su, Fei, Wan, Zi Yi, Yang, Zituo, Tay, Yi Xuan, Lee, May Shu Qing, Ye, Baoqing, Wen, Yanfei, Meng, Zining, Fan, Bin, Alfiko, Yuzer, Shen, Yubang, Piferrer, Francesc, Meyer, Axel, Schartl, Manfred, Yue, Gen Hua
Other Authors: Temasek Life Sciences Laboratory
Format: artículo biblioteca
Language:English
Published: BioMed Central 2022-01
Subjects:Teleost, Sex determination, dmrt1, Transposon, Epigenetic regulation, Sex reversal,
Online Access:http://hdl.handle.net/10261/262575
http://dx.doi.org/10.13039/501100011033
http://dx.doi.org/10.13039/501100010730
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spelling dig-icm-es-10261-2625752022-03-03T03:25:27Z 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 Su, Fei Wan, Zi Yi Yang, Zituo Tay, Yi Xuan Lee, May Shu Qing Ye, Baoqing Wen, Yanfei Meng, Zining Fan, Bin Alfiko, Yuzer Shen, Yubang Piferrer, Francesc Meyer, Axel Schartl, Manfred Yue, Gen Hua Temasek Life Sciences Laboratory Agencia Estatal de Investigación (España) Teleost Sex determination dmrt1 Transposon Epigenetic regulation Sex reversal 16 pages, 6 figures, supplementary Information https://doi.org/10.1186/s12915-021-01205-y.-- Availability of data and materials: Sequences used for RAD, RNA, and genome sequencing are achieved in the DDBJ Sequencing Read Archive (SRA) database under BioProject ID: PRJDB7253- PRJDB7255 [23, 88] 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 This study was supported by the internal funding of the Temasek Life Sciences Laboratory, Singapore With the institutional support of the ‘Severo Ochoa Centre of Excellence’ accreditation (CEX2019-000928-S) Peer reviewed 2022-03-02T12:39:51Z 2022-03-02T12:39:51Z 2022-01 artículo http://purl.org/coar/resource_type/c_6501 BMC Biology 20: 5 (2022) CEX2019-000928-S http://hdl.handle.net/10261/262575 10.1186/s12915-021-01205-y 1741-7007 http://dx.doi.org/10.13039/501100011033 http://dx.doi.org/10.13039/501100010730 en Publisher's version https://doi.org/10.1186/s12915-021-01205-y Sí open BioMed Central
institution ICM ES
collection DSpace
country España
countrycode ES
component Bibliográfico
access En linea
databasecode dig-icm-es
tag biblioteca
region Europa del Sur
libraryname Biblioteca del ICM España
language English
topic Teleost
Sex determination
dmrt1
Transposon
Epigenetic regulation
Sex reversal
Teleost
Sex determination
dmrt1
Transposon
Epigenetic regulation
Sex reversal
spellingShingle Teleost
Sex determination
dmrt1
Transposon
Epigenetic regulation
Sex reversal
Teleost
Sex determination
dmrt1
Transposon
Epigenetic regulation
Sex reversal
Wang, Le
Su, Fei
Wan, Zi Yi
Yang, Zituo
Tay, Yi Xuan
Lee, May Shu Qing
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 16 pages, 6 figures, supplementary Information https://doi.org/10.1186/s12915-021-01205-y.-- Availability of data and materials: Sequences used for RAD, RNA, and genome sequencing are achieved in the DDBJ Sequencing Read Archive (SRA) database under BioProject ID: PRJDB7253- PRJDB7255 [23, 88]
author2 Temasek Life Sciences Laboratory
author_facet Temasek Life Sciences Laboratory
Wang, Le
Su, Fei
Wan, Zi Yi
Yang, Zituo
Tay, Yi Xuan
Lee, May Shu Qing
Ye, Baoqing
Wen, Yanfei
Meng, Zining
Fan, Bin
Alfiko, Yuzer
Shen, Yubang
Piferrer, Francesc
Meyer, Axel
Schartl, Manfred
Yue, Gen Hua
format artículo
topic_facet Teleost
Sex determination
dmrt1
Transposon
Epigenetic regulation
Sex reversal
author Wang, Le
Su, Fei
Wan, Zi Yi
Yang, Zituo
Tay, Yi Xuan
Lee, May Shu Qing
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
publisher BioMed Central
publishDate 2022-01
url http://hdl.handle.net/10261/262575
http://dx.doi.org/10.13039/501100011033
http://dx.doi.org/10.13039/501100010730
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