Parallel Evolution of Two dmrt1-Derived Genes, dmy and dm-W, for Vertebrate Sex Determination

Ogita, Yusaku; Mawaribuchi, Shuuji; Nakasako, Kei; Tamura, Kei; Matsuda, Masaru; Katsumura, Takafumi; Oota, Hiroki; Watanabe, Go; Yoneda, Shigetaka; Takamatsu, Nobuhiko; Ito, Michihiko

doi:10.1016/j.isci.2019.100757

Cited by 14 publications

(7 citation statements)

References 31 publications

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“…Dmrt1 is essential for normal testis differentiation in mammals and is expressed in both germ cells and Sertoli cells (Raymond et al, 1999, Raymond et al, 2000, Kim et al, 2007, Matson et al, 2010, Herpin et al, 2010, Kopp, 2012). In addition, variants of dmrt1 are major sex determining genes in some amphibia, perhaps some snakes, in birds, and some fish (Nanda et al, 2002, Kobayashi et al, 2004, Smith et al, 2009, Janes et al, 2014, Cui et al, 2017, Mustapha et al, 2018, Ioannidis et al, 2021, Ogita et al, 2020). In NA gonads at 19dpf, dmrt1 was expressed at low levels in both ZW and ZZ germ cells in 1930c16 (Fig.…”

Section: Resultsmentioning

confidence: 99%

Direct Male Development in Chromosomally ZZ Zebrafish

Wilson,

Batzel,

Postlethwait

2023

Preprint

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The genetics of sex determination varies across taxa, sometimes even within a species. Major domesticated strains of zebrafish (Danio rerio), including AB and TU, lack a strong genetic sex determining locus, but strains more recently derived from nature, like Nadia (NA), possess a ZZ male/ZW female chromosomal sex-determination system. AB strain fish pass through a juvenile ovary stage, forming oocytes that survive in fish that become females but die in fish that become males. To understand mechanisms of gonad development in NA zebrafish, we studied histology and single cell transcriptomics in developing ZZ and ZW fish. ZW fish developed oocytes by 22 days post-fertilization (dpf) but ZZ fish directly formed testes, avoiding a juvenile ovary phase. Gonads of some ZW and WW fish, however, developed oocytes that died as the gonad became a testis, mimicking AB fish, suggesting that the gynogenetically derived AB strain is chromosomally WW. Single-cell RNA-seq of 19dpf gonads showed similar cell types in ZZ and ZW fish, including germ cells, precursors of gonadal support cells, steroidogenic cells, interstitial/stromal cells, and immune cells, consistent with a bipotential juvenile gonad. In contrast, scRNA-seq of 30dpf gonads revealed that cells in ZZ gonads had transcriptomes characteristic of testicular Sertoli, Leydig, and germ cells while ZW gonads had granulosa cells, theca cells, and developing oocytes. Hematopoietic and vascular cells were similar in both sex genotypes. These results show that juvenile NA zebrafish initially develop a bipotential gonad; that a factor on the NA W chromosome or fewer than two Z chromosomes is essential to initiate oocyte development; and without the W factor or with two Z doses, NA gonads develop directly into testes without passing through the juvenile ovary stage. Sex determination in AB and TU strains mimics NA ZW and WW zebrafish, suggesting loss of the Z chromosome during domestication. Genetic analysis of the NA strain will facilitate our understanding of the evolution of sex determination mechanisms.

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Section: Resultsmentioning

confidence: 99%

Direct Male Development in Chromosomally ZZ Zebrafish

Wilson,

Batzel,

Postlethwait

2023

Preprint

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“…This might thus appear in populations where two male-specific loci were observed, i.e., the populations POP_BSPGIA and POP_BSPG. Such male sex-determining genes originate either by duplication followed by neo-functionalization or allelic diversification in Nile tilapia, Northern pike ( Esox Lucius Linnaeus, 1758 [ 111 ]), and medaka ( Oryzias latipes ) [ 112 , 113 ]. Likewise, 128 of 1033 (12.391%) male-linked loci were located in other chromosomes, with eight loci determined on BSP18, while BSP18 contained foxL2 , sox3 , sox8a , sox9a , and sox9b .…”

Section: Discussionmentioning

confidence: 99%

Something Fishy about Siamese Fighting Fish (Betta splendens) Sex: Polygenic Sex Determination or a Newly Emerged Sex-Determining Region?

Panthum

Jaisamut

Singchat

et al. 2022

Cells

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Fishes provide a unique and intriguing model system for studying the genomic origin and evolutionary mechanisms underlying sex determination and high sex-chromosome turnover. In this study, the mode of sex determination was investigated in Siamese fighting fish, a species of commercial importance. Genome-wide SNP analyses were performed on 75 individuals (40 males and 35 females) across commercial populations to determine candidate sex-specific/sex-linked loci. In total, 73 male-specific loci were identified and mapped to a 5.6 kb region on chromosome 9, suggesting a putative male-determining region (pMDR) containing localized dmrt1 and znrf3 functional sex developmental genes. Repeat annotations of the pMDR revealed an abundance of transposable elements, particularly Ty3/Gypsy and novel repeats. Remarkably, two out of the 73 male-specific loci were located on chromosomes 7 and 19, implying the existence of polygenic sex determination. Besides male-specific loci, five female-specific loci on chromosome 9 were also observed in certain populations, indicating the possibility of a female-determining region and the polygenic nature of sex determination. An alternative explanation is that male-specific loci derived from other chromosomes or female-specific loci in Siamese fighting fish recently emerged as new sex-determining loci during domestication and repeated hybridization.

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“…We hypothesize that the duplication of dsx would promote the evolution of not only tissue-specific, but also sex-specific regulatory modules. Duplications of Dmrt genes have been reported in diverse organisms ranging from vertebrates ( Ogita et al 2020 ) to hexapods ( Price et al 2015 ; Panara et al 2019 ; Gruzin et al 2020 ) and may be a key step in the evolution of complex sexually dimorphic traits. In this regard, our findings of the dsx paralogs highlight Z. cesonia as a potentially powerful system to study the evolution of molecular mechanisms that regulate sexually dimorphic development.…”

Section: Discussionmentioning

confidence: 99%

Novel Doublesex Duplication Associated with Sexually Dimorphic Development of Dogface Butterfly Wings

Rodriguez-Caro

Fenner

Bhardwaj

et al. 2021

Molecular Biology and Evolution

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Sexually dimorphic development is responsible for some of the most remarkable phenotypic variation found in nature. Alternative splicing of the transcription factor gene doublesex is a highly conserved developmental switch controlling the expression of sex specific pathways. Here, we leverage sex-specific differences in butterfly wing color pattern to characterize the genetic basis of sexually dimorphic development. We use RNA-seq, immunolocalization, and motif binding site analysis to test specific predictions about the role of Doublesex in the development of structurally-based ultraviolet (UV) wing patterns in Zerene cesonia (Southern Dogface). Unexpectedly, we discover a novel duplication of Doublesex that shows a sex-specific burst of expression associated with the sexually dimorphic UV coloration. The derived copy consists of a single exon that encodes a DNA binding but no protein binding domain, and has experienced rapid amino-acid divergence. We propose the novel dsx paralog may suppress UV scale differentiation in females, which is supported by an excess of Dsx binding sites at cytoskeletal and chitin-related genes with sex-biased expression. These findings illustrate the molecular flexibility of the dsx gene in mediating the differentiation of secondary sexual characteristics.

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Parallel Evolution of Two dmrt1-Derived Genes, dmy and dm-W, for Vertebrate Sex Determination

Cited by 14 publications

References 31 publications

Direct Male Development in Chromosomally ZZ Zebrafish

Direct Male Development in Chromosomally ZZ Zebrafish

Something Fishy about Siamese Fighting Fish (Betta splendens) Sex: Polygenic Sex Determination or a Newly Emerged Sex-Determining Region?

Novel Doublesex Duplication Associated with Sexually Dimorphic Development of Dogface Butterfly Wings

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