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- Title
Two duplicated gsdf homeologs cooperatively regulate male differentiation by inhibiting cyp19a1a transcription in a hexaploid fish.
- Authors
Wang, Ming-Tao; Li, Zhi; Ding, Miao; Yao, Tian-Zi; Yang, Sheng; Zhang, Xiao-Juan; Miao, Chun; Du, Wen-Xuan; Shi, Qian; Li, Shun; Mei, Jie; Wang, Yang; Wang, Zhong-Wei; Zhou, Li; Li, Xi-Yin; Gui, Jian-Fang
- Abstract
Although evolutionary fates and expression patterns of duplicated genes have been extensively investigated, how duplicated genes co-regulate a biological process in polyploids remains largely unknown. Here, we identified two gsdf (gonadal somatic cell-derived factor) homeologous genes (gsdf-A and gsdf-B) in hexaploid gibel carp (Carassius gibelio), wherein each homeolog contained three highly conserved alleles. Interestingly, gsdf-A and gsdf-B transcription were mainly activated by dmrt1-A (dsx- and mab-3-related transcription factor 1) and dmrt1-B, respectively. Loss of either gsdf-A or gsdf-B alone resulted in partial male-to-female sex reversal and loss of both caused complete sex reversal, which could be rescued by a nonsteroidal aromatase inhibitor. Compensatory expression of gsdf-A and gsdf-B was observed in gsdf-B and gsdf-A mutants, respectively. Subsequently, we determined that in tissue culture cells, Gsdf-A and Gsdf-B both interacted with Ncoa5 (nuclear receptor coactivator 5) and blocked Ncoa5 interaction with Rora (retinoic acid-related orphan receptor-alpha) to repress Rora/Ncoa5-induced activation of cyp19a1a (cytochrome P450, family 19, subfamily A, polypeptide 1a). These findings illustrate that Gsdf-A and Gsdf-B can regulate male differentiation by inhibiting cyp19a1a transcription in hexaploid gibel carp and also reveal that Gsdf-A and Gsdf-B can interact with Ncoa5 to suppress cyp19a1a transcription in vitro. This study provides a typical case of cooperative mechanism of duplicated genes in polyploids and also sheds light on the conserved evolution of sex differentiation. Author summary: Polyploidy generates extra chromosome sets and duplicated genes. However, how the duplicated genes co-regulate a biological process in polyploids remains largely unknown. Here, we reveal that two gsdf (gonadal somatic cell-derived factor) homeologs (gsdf-A and gsdf-B) cooperatively induce male differentiation by inhibiting cyp19a1a (cytochrome P450, family 19, subfamily A, polypeptide 1a) transcription in hexaploid gibel carp (Carassius gibelio). Loss of either gsdf-A or gsdf-B alone results in partial male-to-female sex reversal and loss of both causes complete sex reversal, which can be rescued by a nonsteroidal aromatase inhibitor. Compensatory expression of gsdf-A and gsdf-B is observed in gsdf-B and gsdf-A mutants, respectively. Moreover, we determine that in vitro, Gsdf-A and Gsdf-B both interact with Ncoa5 (nuclear receptor coactivator 5) and block Ncoa5 interaction with Rora (retinoic acid-related orphan receptor-alpha) to repress Rora/Ncoa5-induced activation of cyp19a1a. These findings reveal the potential molecular mechanisms underlying gsdf homeologs-mediated male differentiation in polyploid fish.
- Subjects
SEX reversal; CRUCIAN carp; POLYPLOIDY; SEX differentiation (Embryology); CYTOCHROME P-450; NUCLEAR receptors (Biochemistry); CELL culture
- Publication
PLoS Genetics, 2022, Vol 18, Issue 6, p1
- ISSN
1553-7390
- Publication type
Article
- DOI
10.1371/journal.pgen.1010288