A cyclical switch of gametogenic pathways in hybrids depends on the ploidy level
Abstract The cellular and molecular mechanisms governing sexual reproduction are conserved across eukaryotes. Nevertheless, hybridization can disrupt these mechanisms, leading to asexual reproduction, often accompanied by polyploidy. In this study, we investigate how ploidy level and ratio of parent...
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| Format: | Article |
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Nature Portfolio
2024-04-01
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| Series: | Communications Biology |
| Online Access: | https://doi.org/10.1038/s42003-024-05948-6 |
| _version_ | 1797209157581930496 |
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| author | Dmitrij Dedukh Anatolie Marta Ra-Yeon Myung Myeong-Hun Ko Da-Song Choi Yong-Jin Won Karel Janko |
| author_facet | Dmitrij Dedukh Anatolie Marta Ra-Yeon Myung Myeong-Hun Ko Da-Song Choi Yong-Jin Won Karel Janko |
| author_sort | Dmitrij Dedukh |
| collection | DOAJ |
| description | Abstract The cellular and molecular mechanisms governing sexual reproduction are conserved across eukaryotes. Nevertheless, hybridization can disrupt these mechanisms, leading to asexual reproduction, often accompanied by polyploidy. In this study, we investigate how ploidy level and ratio of parental genomes in hybrids affect their reproductive mode. We analyze the gametogenesis of sexual species and their diploid and triploid hybrids from the freshwater fish family Cobitidae, using newly developed cytogenetic markers. We find that diploid hybrid females possess oogonia and oocytes with original (diploid) and duplicated (tetraploid) ploidy. Diploid oocytes cannot progress beyond pachytene due to aberrant pairing. However, tetraploid oocytes, which emerge after premeiotic genome endoreplication, exhibit normal pairing and result in diploid gametes. Triploid hybrid females possess diploid, triploid, and haploid oogonia and oocytes. Triploid and haploid oocytes cannot progress beyond pachytene checkpoint due to aberrant chromosome pairing, while diploid oocytes have normal pairing in meiosis, resulting in haploid gametes. Diploid oocytes emerge after premeiotic elimination of a single-copied genome. Triploid hybrid males are sterile due to aberrant pairing and the failure of chromosomal segregation during meiotic divisions. Thus, changes in ploidy and genome dosage may lead to cyclical alteration of gametogenic pathways in hybrids. |
| first_indexed | 2024-04-24T09:50:14Z |
| format | Article |
| id | doaj.art-bd30c7fd2a05481fb24b76a99925b9e7 |
| institution | Directory Open Access Journal |
| issn | 2399-3642 |
| language | English |
| last_indexed | 2024-04-24T09:50:14Z |
| publishDate | 2024-04-01 |
| publisher | Nature Portfolio |
| record_format | Article |
| series | Communications Biology |
| spelling | doaj.art-bd30c7fd2a05481fb24b76a99925b9e72024-04-14T11:25:22ZengNature PortfolioCommunications Biology2399-36422024-04-017111410.1038/s42003-024-05948-6A cyclical switch of gametogenic pathways in hybrids depends on the ploidy levelDmitrij Dedukh0Anatolie Marta1Ra-Yeon Myung2Myeong-Hun Ko3Da-Song Choi4Yong-Jin Won5Karel Janko6Laboratory of Non-Mendelian Evolution, Institute of Animal Physiology and Genetics of the CASLaboratory of Non-Mendelian Evolution, Institute of Animal Physiology and Genetics of the CASDivision of EcoScience, Ewha Womans UniversityKosoo Ecology InstituteDivision of EcoScience, Ewha Womans UniversityDivision of EcoScience, Ewha Womans UniversityLaboratory of Non-Mendelian Evolution, Institute of Animal Physiology and Genetics of the CASAbstract The cellular and molecular mechanisms governing sexual reproduction are conserved across eukaryotes. Nevertheless, hybridization can disrupt these mechanisms, leading to asexual reproduction, often accompanied by polyploidy. In this study, we investigate how ploidy level and ratio of parental genomes in hybrids affect their reproductive mode. We analyze the gametogenesis of sexual species and their diploid and triploid hybrids from the freshwater fish family Cobitidae, using newly developed cytogenetic markers. We find that diploid hybrid females possess oogonia and oocytes with original (diploid) and duplicated (tetraploid) ploidy. Diploid oocytes cannot progress beyond pachytene due to aberrant pairing. However, tetraploid oocytes, which emerge after premeiotic genome endoreplication, exhibit normal pairing and result in diploid gametes. Triploid hybrid females possess diploid, triploid, and haploid oogonia and oocytes. Triploid and haploid oocytes cannot progress beyond pachytene checkpoint due to aberrant chromosome pairing, while diploid oocytes have normal pairing in meiosis, resulting in haploid gametes. Diploid oocytes emerge after premeiotic elimination of a single-copied genome. Triploid hybrid males are sterile due to aberrant pairing and the failure of chromosomal segregation during meiotic divisions. Thus, changes in ploidy and genome dosage may lead to cyclical alteration of gametogenic pathways in hybrids.https://doi.org/10.1038/s42003-024-05948-6 |
| spellingShingle | Dmitrij Dedukh Anatolie Marta Ra-Yeon Myung Myeong-Hun Ko Da-Song Choi Yong-Jin Won Karel Janko A cyclical switch of gametogenic pathways in hybrids depends on the ploidy level Communications Biology |
| title | A cyclical switch of gametogenic pathways in hybrids depends on the ploidy level |
| title_full | A cyclical switch of gametogenic pathways in hybrids depends on the ploidy level |
| title_fullStr | A cyclical switch of gametogenic pathways in hybrids depends on the ploidy level |
| title_full_unstemmed | A cyclical switch of gametogenic pathways in hybrids depends on the ploidy level |
| title_short | A cyclical switch of gametogenic pathways in hybrids depends on the ploidy level |
| title_sort | cyclical switch of gametogenic pathways in hybrids depends on the ploidy level |
| url | https://doi.org/10.1038/s42003-024-05948-6 |
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