Parallel Evolution of Sex-Linked Genes across XX/XY and ZZ/ZW Sex Chromosome Systems in the Frog <i>Glandirana rugosa</i>
Genetic sex-determination features male (XX/XY) or female heterogamety (ZZ/ZW). To identify similarities and differences in the molecular evolution of sex-linked genes between these systems, we directly compared the sex chromosome systems existing in the frog <i>Glandirana rugosa</i>. Th...
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MDPI AG
2023-01-01
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| Series: | Genes |
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| Online Access: | https://www.mdpi.com/2073-4425/14/2/257 |
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| author | Shuuji Mawaribuchi Michihiko Ito Mitsuaki Ogata Yuri Yoshimura Ikuo Miura |
| author_facet | Shuuji Mawaribuchi Michihiko Ito Mitsuaki Ogata Yuri Yoshimura Ikuo Miura |
| author_sort | Shuuji Mawaribuchi |
| collection | DOAJ |
| description | Genetic sex-determination features male (XX/XY) or female heterogamety (ZZ/ZW). To identify similarities and differences in the molecular evolution of sex-linked genes between these systems, we directly compared the sex chromosome systems existing in the frog <i>Glandirana rugosa</i>. The heteromorphic X/Y and Z/W sex chromosomes were derived from chromosomes 7 (2n = 26). RNA-Seq, de novo assembly, and BLASTP analyses identified 766 sex-linked genes. These genes were classified into three different clusters (XW/YZ, XY/ZW, and XZ/YW) based on sequence identities between the chromosomes, probably reflecting each step of the sex chromosome evolutionary history. The nucleotide substitution per site was significantly higher in the Y- and Z-genes than in the X- and W- genes, indicating male-driven mutation. The ratio of nonsynonymous to synonymous nucleotide substitution rates was higher in the X- and W-genes than in the Y- and Z-genes, with a female bias. Allelic expression in gonad, brain, and muscle was significantly higher in the Y- and W-genes than in the X- and Z-genes, favoring heterogametic sex. The same set of sex-linked genes showed parallel evolution across the two distinct systems. In contrast, the unique genomic region of the sex chromosomes demonstrated a difference between the two systems, with even and extremely high expression ratios of W/Z and Y/X, respectively. |
| first_indexed | 2024-03-11T08:48:10Z |
| format | Article |
| id | doaj.art-afe5bb29c4844f9fb86341d535a27892 |
| institution | Directory Open Access Journal |
| issn | 2073-4425 |
| language | English |
| last_indexed | 2024-03-11T08:48:10Z |
| publishDate | 2023-01-01 |
| publisher | MDPI AG |
| record_format | Article |
| series | Genes |
| spelling | doaj.art-afe5bb29c4844f9fb86341d535a278922023-11-16T20:40:28ZengMDPI AGGenes2073-44252023-01-0114225710.3390/genes14020257Parallel Evolution of Sex-Linked Genes across XX/XY and ZZ/ZW Sex Chromosome Systems in the Frog <i>Glandirana rugosa</i>Shuuji Mawaribuchi0Michihiko Ito1Mitsuaki Ogata2Yuri Yoshimura3Ikuo Miura4Cellular and Molecular Biotechnology Research Institute, National Institute of Advanced Industrial Science and Technology (AIST), Tsukuba 305-8568, JapanDepartment of Biosciences, School of Science, Kitasato University, Sagamihara 252-0373, JapanPreservation and Research Center, City of Yokohama, 155-1 Asahi Ward, Yokohama 241-0804, JapanDepartment of Biology, Faculty of Science, Kyushu University, Fukuoka 819-0395, JapanAmphibian Research Center, Hiroshima University, Higashi-Hiroshima 739-8526, JapanGenetic sex-determination features male (XX/XY) or female heterogamety (ZZ/ZW). To identify similarities and differences in the molecular evolution of sex-linked genes between these systems, we directly compared the sex chromosome systems existing in the frog <i>Glandirana rugosa</i>. The heteromorphic X/Y and Z/W sex chromosomes were derived from chromosomes 7 (2n = 26). RNA-Seq, de novo assembly, and BLASTP analyses identified 766 sex-linked genes. These genes were classified into three different clusters (XW/YZ, XY/ZW, and XZ/YW) based on sequence identities between the chromosomes, probably reflecting each step of the sex chromosome evolutionary history. The nucleotide substitution per site was significantly higher in the Y- and Z-genes than in the X- and W- genes, indicating male-driven mutation. The ratio of nonsynonymous to synonymous nucleotide substitution rates was higher in the X- and W-genes than in the Y- and Z-genes, with a female bias. Allelic expression in gonad, brain, and muscle was significantly higher in the Y- and W-genes than in the X- and Z-genes, favoring heterogametic sex. The same set of sex-linked genes showed parallel evolution across the two distinct systems. In contrast, the unique genomic region of the sex chromosomes demonstrated a difference between the two systems, with even and extremely high expression ratios of W/Z and Y/X, respectively.https://www.mdpi.com/2073-4425/14/2/257male-biased mutation<i>dN/dS</i> ratiogene expressionheterogametic sex |
| spellingShingle | Shuuji Mawaribuchi Michihiko Ito Mitsuaki Ogata Yuri Yoshimura Ikuo Miura Parallel Evolution of Sex-Linked Genes across XX/XY and ZZ/ZW Sex Chromosome Systems in the Frog <i>Glandirana rugosa</i> Genes male-biased mutation <i>dN/dS</i> ratio gene expression heterogametic sex |
| title | Parallel Evolution of Sex-Linked Genes across XX/XY and ZZ/ZW Sex Chromosome Systems in the Frog <i>Glandirana rugosa</i> |
| title_full | Parallel Evolution of Sex-Linked Genes across XX/XY and ZZ/ZW Sex Chromosome Systems in the Frog <i>Glandirana rugosa</i> |
| title_fullStr | Parallel Evolution of Sex-Linked Genes across XX/XY and ZZ/ZW Sex Chromosome Systems in the Frog <i>Glandirana rugosa</i> |
| title_full_unstemmed | Parallel Evolution of Sex-Linked Genes across XX/XY and ZZ/ZW Sex Chromosome Systems in the Frog <i>Glandirana rugosa</i> |
| title_short | Parallel Evolution of Sex-Linked Genes across XX/XY and ZZ/ZW Sex Chromosome Systems in the Frog <i>Glandirana rugosa</i> |
| title_sort | parallel evolution of sex linked genes across xx xy and zz zw sex chromosome systems in the frog i glandirana rugosa i |
| topic | male-biased mutation <i>dN/dS</i> ratio gene expression heterogametic sex |
| url | https://www.mdpi.com/2073-4425/14/2/257 |
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