Comparison of Gonadal Transcriptomes Uncovers Reproduction-Related Genes with Sexually Dimorphic Expression Patterns in Diodon hystrix

Chen, Huapu; Li, Zhiyuan; Wang, Yaorong; Huang, Hai; Yang, Xiao; Li, Shuangfei; Yang, Wei; Li, Guangli

doi:10.3390/ani11041042

Cited by 12 publications

(14 citation statements)

References 73 publications

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“…Hsd17b7 could convert estrone to E 2 and played an important role in mouse embryonic development [ 52 ]. The expression levels of cyp11a , hsd3b , and hsd11b2 were observably higher in male P. sinensis than in the female, which was consistent with the results of Oryzias latipes [ 53 ]. However, the expression level of hsd17b7 was inconsistent with that reported in previous studies.…”

Section: Discussionsupporting

confidence: 89%

The Important Role of Sex-Related Sox Family Genes in the Sex Reversal of the Chinese Soft-Shelled Turtle (Pelodiscus sinensis)

Wang

Luo

Qu³

et al. 2022

Biology

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The Chinese soft-shelled turtle Pelodiscus sinensis shows obvious sexual dimorphism. The economic and nutrition value of male individuals are significantly higher than those of female individuals. Pseudo-females which are base to all-male breeding have been obtained by estrogen induction, while the gene function and molecular mechanism of sex reversal remain unclear in P. sinensis. Here, comparative transcriptome analyses of female, male, and pseudo-female gonads were performed, and 14,430 genes differentially expressed were identified in the pairwise comparison of three groups. GO and KEGG analyses were performed on the differentially expressed genes (DEGs), which mainly concentrated on steroid hormone synthesis. Furthermore, the results of gonadal transcriptome analysis revealed that 10 sex-related sox genes were differentially expressed in males vs. female, male vs. pseudo-female, and female vs. pseudo-female. Through the differential expression analysis of these 10 sox genes in mature gonads, six sox genes related to sex reversal were further screened. The molecular mechanism of the six sox genes in the embryo were analyzed during sex reversal after E2 treatment. In mature gonads, some sox family genes, such as sox9sox12, and sox30 were highly expressed in the testis, while sox1, sox3, sox6, sox11, and sox17 were lowly expressed. In the male embryos, exogenous estrogen can activate the expression of sox3 and inhibit the expression of sox8, sox9, and sox11. In summary, sox3 may have a role in the process of sex reversal from male to pseudo-female, when sox8 and sox9 are inhibited. Sox family genes affect both female and male pathways in the process of sex reversal, which provides a new insight for the all-male breeding of the Chinese soft-shelled turtle.

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Section: Discussionsupporting

confidence: 89%

The Important Role of Sex-Related Sox Family Genes in the Sex Reversal of the Chinese Soft-Shelled Turtle (Pelodiscus sinensis)

Wang

Luo

Qu³

et al. 2022

Biology

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“…Numerous studies have capitalized on this powerful tool to analyze the holistic expression patterns in gonads. For instance, the gonad transcriptome of Nile tilapia, Oreochromis niloticus (Tao et al, 2013;Sun et al, 2018;Teng et al, 2020;Lin et al, 2021a), adult spotted scat (He et al, 2019), Chinese tongue sole, Cynoglossus semilaevis (Wang et al, 2019), silver sillago, Sillago sihama (Tian et al, 2019), Hong Kong catfish, Clarias fuscus (Lin et al, 2021b), spot-fin porcupine fish, Diodon hystrix (Chen et al, 2021) and others (Santos et al, 2007;Dıáz et al, 2014;Chen et al, 2021;Kohli et al, 2021;Yao et al, 2021;Zhu et al, 2022), revealed numerous differential and male and female pathway genes. As indicated above, previous studies identified several sex-related genes in adult spotted scat by gonadal transcriptomics (He et al, 2019).…”

Section: Introductionmentioning

confidence: 99%

Comparative transcriptome analysis of the differentiating gonads in Scatophagus argus

et al. 2022

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The reproductive-related studies, including genetic and genomic such as gonadal transcriptome analyses, have previously focused on the adult spotted scat, with little information on juvenile fish. Transcriptomics is a powerful tool that allows for massive parallel analysis to identify differential expression and the patterns of gene expression holistically at a particular stage in a cell or tissue development. This study presents the first report on gonadal transcriptome analysis of the differentiating (juvenile; 4 months after hatch; stage I ovary and testis) spotted scat gonads. The study revealed potential reproduction and gonadal development-related genes. A total of 25936 genes were identified, of which 16248 were co-expressed, 17893 and 17258 expressed in males and females, respectively, from sequence data of testis I (n = 3) and ovary I (n = 2). A total of 6549 differentially expressed genes (DEGs) were identified between males and females. Genes attributable to male gonad development pathway such as dmrt1, gsdf, and amh are significantly expressed in differentiating testes, while female-related genes such as foxl2, cyp19a1a, 42sp50 and sox3 were expressed considerably in differentiating ovaries. In addition, dmrt1/dmrt1y was not expressed in the female (FPKM=0.00), while its paralog dmrt1b was expressed in both males and females. In the male pathway, dmrt1y and gsdf are critical for sex determination and maintenance while foxl2/foxl3 and cyp19a1a are critical in the female development pathway. The current studies provide an insight into the expression patterns of sex and gonadal-related genes in differentiating gonads of spotted scat.

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“…Fortunately, technological advancements such as transcriptome analysis have made identifying gonadal sexual biased genes easy. Numerous sex-biased genes have since been identified in many other species [ 41 , 42 , 53 , 54 , 55 ], including Nile tilapia [ 40 ] and spotted scat [ 36 ]. Meanwhile, most of these studies have focused on gonadal gene expression, with little or no interest in the possible mechanism leading to sex difference.…”

Section: Discussionmentioning

confidence: 99%

“…We analyzed various transcriptome data for gonadal tissues to understand the expression patterns of the Dmrt2a & b in different species. Either zebrafish or spotted scat Dmrt1 , Dmrt2a , and Dmrt2b transcripts were used as query sequences to blast the transcriptome data (cds) of spotted scat [ 36 ], Hainan medaka ( Oryzias curvinotus ) [ 38 ], silver sillago ( Sillago sihama ) [ 39 ], Nile tilapia ( Oreochromis niloticus ) [ 40 ], Hong Kong catfish ( Clarias fuscus ) [ 41 ], and spot-fin porcupine fish ( Diodon hystrix ) [ 42 ]. For confirmation, the results with different transcript numbers and maximum hits were blasted using NCBI nucleotide blast ( , accessed on 15 October 2021).…”

Section: Methodsmentioning

confidence: 99%

“… Gene expression in RPKM/FPKM obtained from gonad transcriptome data of ( A , a ) spotted scat [ 36 ], ( B , b ) Hainan medaka [ 38 ], ( C , c ) silver sillago [ 39 ], ( D , d ) Nile tilapia [ 40 ], ( E ) Hong Kong catfish [ 41 ], and ( F ) spot-fine porcupine fish [ 42 ]. Dmrt1 is consistently expressed at higher levels in all testes.…”

Section: Figurementioning

confidence: 99%

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High Polymorphism in the Dmrt2a Gene Is Incompletely Sex-Linked in Spotted Scat, Scatophagus argus

Mustapha

Assan

Huang

et al. 2022

Animals

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Unlike mammals and birds, many fishes have young sex chromosomes, providing excellent models to study sex chromosome differentiation at early stages. Previous studies showed that spotted scat possesses an XX-XY sex determination system. The X has a complete Dmrt3 copy (termed normal) and a truncated copy of Dmrt1 (called Dmrt1b), while the Y has the opposite (normal Dmrt1, which is male-specific, and a truncated Dmrt3 called Dmrt3△-Y). Dmrt1 is the candidate sex determination gene, while the differentiation of other sex-linked genes remains unknown. The spotted scat has proven to be a good model to study the evolution of sex chromosomes in vertebrates. Herein, we sequenced a neighbor gene of this family, Dmrt2, positioned farther from Dmrt1 and closer to Dmrt3 in the spotted scat, and analyzed its sequence variation and expression profiles. The physical locations of the three genes span across an estimated size of >40 kb. The open reading frames of Dmrt2a and its paralog Dmrt2b are 1578 bp and 1311 bp, encoding peptides of 525 and 436 amino acid residues, respectively. Dmrt2a is positioned close to Dmrt3 but farther from Dmrt1 on the same chromosome, while Dmrt2b is not. Sequence analysis revealed several mutations; insertions, and deletions (indels) on Dmrt2a non-coding regions and single-nucleotide polymorphisms (SNPs) on the Dmrt2a transcript. These indels and SNPs are sex-linked and showed high male heterogeneity but do not affect gene translation. The markers designed to span the mutation sites tested on four different populations showed varied concordance with the genetic sexes. Dmrt2a is transcribed solely in the gonads and gills, while Dmrt2b exists in the gonads, hypothalamus, gills, heart, and spleen. The Dmrt2a and Dmrt2b transcripts are profoundly expressed in the male gonads. Analyses of the transcriptome data from five other fish species (Hainan medaka (Oryzias curvinotus), silver sillago (Sillago sihama), Nile tilapia (Oreochromis niloticus), Hong Kong catfish (Clarias fuscus), and spot-fin porcupine fish (Diodon hystrix)) revealed testes-biased expression of Dmrt1 in all, similar to spotted scat. Additionally, the expression of Dmrt2a is higher in the testes than the ovaries in spotted scat and Hainan medaka. The Dmrt2a transcript was not altered in the coding regions as found in Dmrt1 and Dmrt3 in spotted scat. This could be due to the functional importance of Dmrt2a in development. Another possibility is that because Dmrt2a is positioned farther from Dmrt1 and the chromosome is still young, meaning it is only a matter of time before it differentiates. This study undeniably will aid in understanding the functional divergence of the sex-linked genes in fish.

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Comparison of Gonadal Transcriptomes Uncovers Reproduction-Related Genes with Sexually Dimorphic Expression Patterns in Diodon hystrix

Cited by 12 publications

References 73 publications

The Important Role of Sex-Related Sox Family Genes in the Sex Reversal of the Chinese Soft-Shelled Turtle (Pelodiscus sinensis)

The Important Role of Sex-Related Sox Family Genes in the Sex Reversal of the Chinese Soft-Shelled Turtle (Pelodiscus sinensis)

Comparative transcriptome analysis of the differentiating gonads in Scatophagus argus

High Polymorphism in the Dmrt2a Gene Is Incompletely Sex-Linked in Spotted Scat, Scatophagus argus

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