Parallel Evolution of Two dmrt1-Derived Genes, dmy and dm-W, for Vertebrate Sex Determination
Animal sex-determining genes, which bifurcate for female and male development, are diversified even among closely related species. Most of these genes emerged independently from various sex-related genes during species diversity as neofunctionalization-type genes. However, the common mechanisms of t...
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| Published in: | iScience Vol. 23; no. 1; p. 100757 |
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| Abstract | Animal sex-determining genes, which bifurcate for female and male development, are diversified even among closely related species. Most of these genes emerged independently from various sex-related genes during species diversity as neofunctionalization-type genes. However, the common mechanisms of this divergent evolution remain poorly understood. Here, we compared the molecular evolution of two sex-determining genes, the medaka dmy and the clawed frog dm-W, which independently evolved from the duplication of the transcription factor-encoding masculinization gene dmrt1. Interestingly, we detected parallel amino acid substitutions, from serine (S) to threonine (T), on the DNA-binding domains of both ancestral DMY and DM-W, resulting from positive selection. Two types of DNA-protein binding experiments and a luciferase reporter assay demonstrated that these S-T substitutions could strengthen the DNA-binding abilities and enhance the transcriptional regulation function. These findings suggest that the parallel S-T substitutions may have contributed to the establishment of dmy and dm-W as sex-determining genes.
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•We detected parallel amino acid substitutions in two sex-determining genes, dmy and dm-W•Both the substitutions from dmrt1 duplication are under positive selection•These substitutions enhanced their DNA-binding activity as transcription factors•These substitutions might have contributed to the establishment of dmy and dm-W
Biological Sciences; Genetics; Evolutionary Biology |
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| AbstractList | Animal sex-determining genes, which bifurcate for female and male development, are diversified even among closely related species. Most of these genes emerged independently from various sex-related genes during species diversity as neofunctionalization-type genes. However, the common mechanisms of this divergent evolution remain poorly understood. Here, we compared the molecular evolution of two sex-determining genes, the medaka dmy and the clawed frog dm-W, which independently evolved from the duplication of the transcription factor-encoding masculinization gene dmrt1. Interestingly, we detected parallel amino acid substitutions, from serine (S) to threonine (T), on the DNA-binding domains of both ancestral DMY and DM-W, resulting from positive selection. Two types of DNA-protein binding experiments and a luciferase reporter assay demonstrated that these S-T substitutions could strengthen the DNA-binding abilities and enhance the transcriptional regulation function. These findings suggest that the parallel S-T substitutions may have contributed to the establishment of dmy and dm-W as sex-determining genes.
[Display omitted]
•We detected parallel amino acid substitutions in two sex-determining genes, dmy and dm-W•Both the substitutions from dmrt1 duplication are under positive selection•These substitutions enhanced their DNA-binding activity as transcription factors•These substitutions might have contributed to the establishment of dmy and dm-W
Biological Sciences; Genetics; Evolutionary Biology Animal sex-determining genes, which bifurcate for female and male development, are diversified even among closely related species. Most of these genes emerged independently from various sex-related genes during species diversity as neofunctionalization-type genes. However, the common mechanisms of this divergent evolution remain poorly understood. Here, we compared the molecular evolution of two sex-determining genes, the medaka dmy and the clawed frog dm-W, which independently evolved from the duplication of the transcription factor-encoding masculinization gene dmrt1. Interestingly, we detected parallel amino acid substitutions, from serine (S) to threonine (T), on the DNA-binding domains of both ancestral DMY and DM-W, resulting from positive selection. Two types of DNA-protein binding experiments and a luciferase reporter assay demonstrated that these S-T substitutions could strengthen the DNA-binding abilities and enhance the transcriptional regulation function. These findings suggest that the parallel S-T substitutions may have contributed to the establishment of dmy and dm-W as sex-determining genes. Animal sex-determining genes, which bifurcate for female and male development, are diversified even among closely related species. Most of these genes emerged independently from various sex-related genes during species diversity as neofunctionalization-type genes. However, the common mechanisms of this divergent evolution remain poorly understood. Here, we compared the molecular evolution of two sex-determining genes, the medaka dmy and the clawed frog dm-W, which independently evolved from the duplication of the transcription factor-encoding masculinization gene dmrt1. Interestingly, we detected parallel amino acid substitutions, from serine (S) to threonine (T), on the DNA-binding domains of both ancestral DMY and DM-W, resulting from positive selection. Two types of DNA-protein binding experiments and a luciferase reporter assay demonstrated that these S-T substitutions could strengthen the DNA-binding abilities and enhance the transcriptional regulation function. These findings suggest that the parallel S-T substitutions may have contributed to the establishment of dmy and dm-W as sex-determining genes. : Biological Sciences; Genetics; Evolutionary Biology Subject Areas: Biological Sciences, Genetics, Evolutionary Biology Animal sex-determining genes, which bifurcate for female and male development, are diversified even among closely related species. Most of these genes emerged independently from various sex-related genes during species diversity as neofunctionalization-type genes. However, the common mechanisms of this divergent evolution remain poorly understood. Here, we compared the molecular evolution of two sex-determining genes, the medaka dmy and the clawed frog dm-W , which independently evolved from the duplication of the transcription factor-encoding masculinization gene dmrt1 . Interestingly, we detected parallel amino acid substitutions, from serine (S) to threonine (T), on the DNA-binding domains of both ancestral DMY and DM-W, resulting from positive selection. Two types of DNA-protein binding experiments and a luciferase reporter assay demonstrated that these S-T substitutions could strengthen the DNA-binding abilities and enhance the transcriptional regulation function. These findings suggest that the parallel S-T substitutions may have contributed to the establishment of dmy and dm-W as sex-determining genes. • We detected parallel amino acid substitutions in two sex-determining genes, dmy and dm-W • Both the substitutions from dmrt1 duplication are under positive selection • These substitutions enhanced their DNA-binding activity as transcription factors • These substitutions might have contributed to the establishment of dmy and dm-W Biological Sciences; Genetics; Evolutionary Biology |
| ArticleNumber | 100757 |
| Author | Watanabe, Go Tamura, Kei Nakasako, Kei Yoneda, Shigetaka Takamatsu, Nobuhiko Mawaribuchi, Shuuji Ogita, Yusaku Oota, Hiroki Matsuda, Masaru Ito, Michihiko Katsumura, Takafumi |
| AuthorAffiliation | 1 Department of Bioscience, School of Science, Kitasato University, 1-15-1 Kitasato, Minamiku, Sagamihara, Kanagawa 252-0373, Japan 4 Laboratory of Genome Anthropology, Department of Anatomy, Kitasato University School of Medicine, Kitasato 1-15-1, Minamiku, Sagamihara 252-0674, Japan 3 Center for Bioscience Research and Education, Utsunomiya University, Utsunomiya 321-8505, Japan 5 School of Science, The University of Tokyo, 7-3-1 Hongo, Bunkyoku, Tokyo 113-0032, Japan 2 Biotechnology Research Institute for Drug Discovery, National Institute of AIST, Central 6, 1-1-1 Higashi, Tsukuba 305-8566, Japan 6 Department of Physics, School of Science, Kitasato University, 1-15-1 Kitasato, Minamiku, Sagamihara, Kanagawa 252-0373, Japan |
| AuthorAffiliation_xml | – name: 6 Department of Physics, School of Science, Kitasato University, 1-15-1 Kitasato, Minamiku, Sagamihara, Kanagawa 252-0373, Japan – name: 1 Department of Bioscience, School of Science, Kitasato University, 1-15-1 Kitasato, Minamiku, Sagamihara, Kanagawa 252-0373, Japan – name: 4 Laboratory of Genome Anthropology, Department of Anatomy, Kitasato University School of Medicine, Kitasato 1-15-1, Minamiku, Sagamihara 252-0674, Japan – name: 2 Biotechnology Research Institute for Drug Discovery, National Institute of AIST, Central 6, 1-1-1 Higashi, Tsukuba 305-8566, Japan – name: 3 Center for Bioscience Research and Education, Utsunomiya University, Utsunomiya 321-8505, Japan – name: 5 School of Science, The University of Tokyo, 7-3-1 Hongo, Bunkyoku, Tokyo 113-0032, Japan |
| Author_xml | – sequence: 1 givenname: Yusaku surname: Ogita fullname: Ogita, Yusaku organization: Department of Bioscience, School of Science, Kitasato University, 1-15-1 Kitasato, Minamiku, Sagamihara, Kanagawa 252-0373, Japan – sequence: 2 givenname: Shuuji surname: Mawaribuchi fullname: Mawaribuchi, Shuuji organization: Biotechnology Research Institute for Drug Discovery, National Institute of AIST, Central 6, 1-1-1 Higashi, Tsukuba 305-8566, Japan – sequence: 3 givenname: Kei surname: Nakasako fullname: Nakasako, Kei organization: Department of Bioscience, School of Science, Kitasato University, 1-15-1 Kitasato, Minamiku, Sagamihara, Kanagawa 252-0373, Japan – sequence: 4 givenname: Kei surname: Tamura fullname: Tamura, Kei organization: Department of Bioscience, School of Science, Kitasato University, 1-15-1 Kitasato, Minamiku, Sagamihara, Kanagawa 252-0373, Japan – sequence: 5 givenname: Masaru surname: Matsuda fullname: Matsuda, Masaru organization: Center for Bioscience Research and Education, Utsunomiya University, Utsunomiya 321-8505, Japan – sequence: 6 givenname: Takafumi surname: Katsumura fullname: Katsumura, Takafumi organization: Laboratory of Genome Anthropology, Department of Anatomy, Kitasato University School of Medicine, Kitasato 1-15-1, Minamiku, Sagamihara 252-0674, Japan – sequence: 7 givenname: Hiroki surname: Oota fullname: Oota, Hiroki organization: School of Science, The University of Tokyo, 7-3-1 Hongo, Bunkyoku, Tokyo 113-0032, Japan – sequence: 8 givenname: Go surname: Watanabe fullname: Watanabe, Go organization: Department of Physics, School of Science, Kitasato University, 1-15-1 Kitasato, Minamiku, Sagamihara, Kanagawa 252-0373, Japan – sequence: 9 givenname: Shigetaka surname: Yoneda fullname: Yoneda, Shigetaka organization: Department of Physics, School of Science, Kitasato University, 1-15-1 Kitasato, Minamiku, Sagamihara, Kanagawa 252-0373, Japan – sequence: 10 givenname: Nobuhiko surname: Takamatsu fullname: Takamatsu, Nobuhiko organization: Department of Bioscience, School of Science, Kitasato University, 1-15-1 Kitasato, Minamiku, Sagamihara, Kanagawa 252-0373, Japan – sequence: 11 givenname: Michihiko surname: Ito fullname: Ito, Michihiko email: ito@sci.kitasato-u.ac.jp organization: Department of Bioscience, School of Science, Kitasato University, 1-15-1 Kitasato, Minamiku, Sagamihara, Kanagawa 252-0373, Japan |
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| Title | Parallel Evolution of Two dmrt1-Derived Genes, dmy and dm-W, for Vertebrate Sex Determination |
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