Dose-dependent role of AMH and AMHR2 signaling in male differentiation and regulation of sex determination in Spotted knifejaw (Oplegnathus punctatus) with X1X1X2X2/X1X2Y chromosome system
Abstract Sex determination mechanisms vary significantly across different chromosomal systems and evolutionary contexts. Nonetheless, the regulatory framework governing the multi-sex chromosome system (X1X1X2X2/X1X2Y) remains enigmatic. Through an examination of sex-related genes (dmrt1, hsd11b2, am...
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BMC
2025-02-01
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| Series: | Cell Communication and Signaling |
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| Online Access: | https://doi.org/10.1186/s12964-025-02038-w |
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| author | Haixia Zhao Jun Li Zhizhong Xiao Yongshuang Xiao |
| author_facet | Haixia Zhao Jun Li Zhizhong Xiao Yongshuang Xiao |
| author_sort | Haixia Zhao |
| collection | DOAJ |
| description | Abstract Sex determination mechanisms vary significantly across different chromosomal systems and evolutionary contexts. Nonetheless, the regulatory framework governing the multi-sex chromosome system (X1X1X2X2/X1X2Y) remains enigmatic. Through an examination of sex-related genes (dmrt1, hsd11b2, amh, sox9a, sox9b, foxl2, cyp19a), hormonal influences (E2, 11-KT), and histological analyses of gonadal development, we demonstrate that the critical period for sexual differentiation occurs between 35 to 60 days post-hatching (dph). Our multi-omics analysis identified amhr2 as a candidate sex-determining gene, revealing that the males possess three distinct amhr2 transcripts (amhr2ay, amhr2by, amhr2cy), whereas females express only one (amhr2a). In situ hybridization assays demonstrated that amhr2 is predominantly localized to primary spermatocyte and Sertoli cells of male testes. Notably, the specific mRNA expression of amhr2 is significantly enriched in amhr2cy, whose extracellular domain exhibits the highest binding affinity for Amh protein, with sexual expression differences manifesting as early as 5 dph. The outcomes of amhr2 interference (RNAi) experiments indicate that amhr2 knockdown leads to a reduction in the expression of male-related gene (dmrt1, amh, sox9a, sox9b), androgen synthesis genes (hsd11b2, cyp11a), and female-related genes (wnt4, foxl2, cyp19a, cyp19b). Conversely, overexpression of amhr2 yielded contrasting results. Our research supports the role of amhr2 as a pivotal candidate sex-determining gene. Furthermore, the dosage effect of amhr2, reflected in transcript abundance, mRNA expression levels, and binding efficacy, serves as a fundamental mechanism driving male differentiation and regulatory processes in Spotted knifejaw. |
| format | Article |
| id | doaj-art-0f0befc7056e409d809963770b270a72 |
| institution | Kabale University |
| issn | 1478-811X |
| language | English |
| publishDate | 2025-02-01 |
| publisher | BMC |
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| series | Cell Communication and Signaling |
| spelling | doaj-art-0f0befc7056e409d809963770b270a722025-02-02T12:34:33ZengBMCCell Communication and Signaling1478-811X2025-02-0123112710.1186/s12964-025-02038-wDose-dependent role of AMH and AMHR2 signaling in male differentiation and regulation of sex determination in Spotted knifejaw (Oplegnathus punctatus) with X1X1X2X2/X1X2Y chromosome systemHaixia Zhao0Jun Li1Zhizhong Xiao2Yongshuang Xiao3State Key Laboratory of Breeding Biotechnology and Sustainable Aquaculture, Chinese Academy of Sciences (CAS)State Key Laboratory of Breeding Biotechnology and Sustainable Aquaculture, Chinese Academy of Sciences (CAS)State Key Laboratory of Breeding Biotechnology and Sustainable Aquaculture, Chinese Academy of Sciences (CAS)State Key Laboratory of Breeding Biotechnology and Sustainable Aquaculture, Chinese Academy of Sciences (CAS)Abstract Sex determination mechanisms vary significantly across different chromosomal systems and evolutionary contexts. Nonetheless, the regulatory framework governing the multi-sex chromosome system (X1X1X2X2/X1X2Y) remains enigmatic. Through an examination of sex-related genes (dmrt1, hsd11b2, amh, sox9a, sox9b, foxl2, cyp19a), hormonal influences (E2, 11-KT), and histological analyses of gonadal development, we demonstrate that the critical period for sexual differentiation occurs between 35 to 60 days post-hatching (dph). Our multi-omics analysis identified amhr2 as a candidate sex-determining gene, revealing that the males possess three distinct amhr2 transcripts (amhr2ay, amhr2by, amhr2cy), whereas females express only one (amhr2a). In situ hybridization assays demonstrated that amhr2 is predominantly localized to primary spermatocyte and Sertoli cells of male testes. Notably, the specific mRNA expression of amhr2 is significantly enriched in amhr2cy, whose extracellular domain exhibits the highest binding affinity for Amh protein, with sexual expression differences manifesting as early as 5 dph. The outcomes of amhr2 interference (RNAi) experiments indicate that amhr2 knockdown leads to a reduction in the expression of male-related gene (dmrt1, amh, sox9a, sox9b), androgen synthesis genes (hsd11b2, cyp11a), and female-related genes (wnt4, foxl2, cyp19a, cyp19b). Conversely, overexpression of amhr2 yielded contrasting results. Our research supports the role of amhr2 as a pivotal candidate sex-determining gene. Furthermore, the dosage effect of amhr2, reflected in transcript abundance, mRNA expression levels, and binding efficacy, serves as a fundamental mechanism driving male differentiation and regulatory processes in Spotted knifejaw.https://doi.org/10.1186/s12964-025-02038-wSpotted knifejawSex determinationamhr2Dosage compensationX1X1X2X2/X1X2Y system |
| spellingShingle | Haixia Zhao Jun Li Zhizhong Xiao Yongshuang Xiao Dose-dependent role of AMH and AMHR2 signaling in male differentiation and regulation of sex determination in Spotted knifejaw (Oplegnathus punctatus) with X1X1X2X2/X1X2Y chromosome system Cell Communication and Signaling Spotted knifejaw Sex determination amhr2 Dosage compensation X1X1X2X2/X1X2Y system |
| title | Dose-dependent role of AMH and AMHR2 signaling in male differentiation and regulation of sex determination in Spotted knifejaw (Oplegnathus punctatus) with X1X1X2X2/X1X2Y chromosome system |
| title_full | Dose-dependent role of AMH and AMHR2 signaling in male differentiation and regulation of sex determination in Spotted knifejaw (Oplegnathus punctatus) with X1X1X2X2/X1X2Y chromosome system |
| title_fullStr | Dose-dependent role of AMH and AMHR2 signaling in male differentiation and regulation of sex determination in Spotted knifejaw (Oplegnathus punctatus) with X1X1X2X2/X1X2Y chromosome system |
| title_full_unstemmed | Dose-dependent role of AMH and AMHR2 signaling in male differentiation and regulation of sex determination in Spotted knifejaw (Oplegnathus punctatus) with X1X1X2X2/X1X2Y chromosome system |
| title_short | Dose-dependent role of AMH and AMHR2 signaling in male differentiation and regulation of sex determination in Spotted knifejaw (Oplegnathus punctatus) with X1X1X2X2/X1X2Y chromosome system |
| title_sort | dose dependent role of amh and amhr2 signaling in male differentiation and regulation of sex determination in spotted knifejaw oplegnathus punctatus with x1x1x2x2 x1x2y chromosome system |
| topic | Spotted knifejaw Sex determination amhr2 Dosage compensation X1X1X2X2/X1X2Y system |
| url | https://doi.org/10.1186/s12964-025-02038-w |
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