The programmed DNA elimination and formation of micronuclei in germ line cells of the natural hybridogenetic water frog Pelophylax esculentus
Abstract DNA elimination is a radical form of gene silencing and occurs both in somatic and germ cells. The programmed DNA elimination occurs during gametogenesis in interspecies hybrids that reproduce by hybridogenesis (stick insects, fishes, and amphibians) and concerns removal of whole genomes of...
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oai:doaj.org-article:a00a62dd9d2e4960a106005f1b1671852021-12-02T15:08:43ZThe programmed DNA elimination and formation of micronuclei in germ line cells of the natural hybridogenetic water frog Pelophylax esculentus10.1038/s41598-018-26168-z2045-2322https://doaj.org/article/a00a62dd9d2e4960a106005f1b1671852018-05-01T00:00:00Zhttps://doi.org/10.1038/s41598-018-26168-zhttps://doaj.org/toc/2045-2322Abstract DNA elimination is a radical form of gene silencing and occurs both in somatic and germ cells. The programmed DNA elimination occurs during gametogenesis in interspecies hybrids that reproduce by hybridogenesis (stick insects, fishes, and amphibians) and concerns removal of whole genomes of one of the parental species and production of clonal gametes propagating the genome of the other species. The cellular mechanisms differ considerably in hybridogenetic insects and fishes but remains unknown in edible frogs Pelophylax esculentus, natural hybrids between Pelophylax lessonae and Pelophylax ridibundus. Here we report DNA elimination mechanism in early developing gonads of diploid and triploid hybrid frogs, studied by TEM, immunofluorescence, and cytochemistry. In gonocytes of both sexes (primary oogonia and prespermatogonia), micronuclei emerge as detached nuclear buds formed during interphase. We found depletion of nuclear pore complexes in micronuclear membrane and chromatin inactivation via heterochromatinization followed by degradation of micronuclei by autophagy. Micronuclei formation does not lead to apoptotic cell death showing that genome elimination is a physiological process. Chromatin elimination via micronuclei in P. esculentus is unique among hybridogenetic animals and contributes to broadening the knowledge about reproductive modes in animals.Magdalena ChmielewskaDmitry DedukhKatarzyna HaczkiewiczBeata Rozenblut-KościstyMikołaj KaźmierczakKrzysztof KolendaEwa SerwaAgnieszka Pietras-LebiodaAlla KrasikovaMaria OgielskaNature PortfolioarticleMedicineRScienceQENScientific Reports, Vol 8, Iss 1, Pp 1-19 (2018) |
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Medicine R Science Q Magdalena Chmielewska Dmitry Dedukh Katarzyna Haczkiewicz Beata Rozenblut-Kościsty Mikołaj Kaźmierczak Krzysztof Kolenda Ewa Serwa Agnieszka Pietras-Lebioda Alla Krasikova Maria Ogielska The programmed DNA elimination and formation of micronuclei in germ line cells of the natural hybridogenetic water frog Pelophylax esculentus |
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Abstract DNA elimination is a radical form of gene silencing and occurs both in somatic and germ cells. The programmed DNA elimination occurs during gametogenesis in interspecies hybrids that reproduce by hybridogenesis (stick insects, fishes, and amphibians) and concerns removal of whole genomes of one of the parental species and production of clonal gametes propagating the genome of the other species. The cellular mechanisms differ considerably in hybridogenetic insects and fishes but remains unknown in edible frogs Pelophylax esculentus, natural hybrids between Pelophylax lessonae and Pelophylax ridibundus. Here we report DNA elimination mechanism in early developing gonads of diploid and triploid hybrid frogs, studied by TEM, immunofluorescence, and cytochemistry. In gonocytes of both sexes (primary oogonia and prespermatogonia), micronuclei emerge as detached nuclear buds formed during interphase. We found depletion of nuclear pore complexes in micronuclear membrane and chromatin inactivation via heterochromatinization followed by degradation of micronuclei by autophagy. Micronuclei formation does not lead to apoptotic cell death showing that genome elimination is a physiological process. Chromatin elimination via micronuclei in P. esculentus is unique among hybridogenetic animals and contributes to broadening the knowledge about reproductive modes in animals. |
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article |
author |
Magdalena Chmielewska Dmitry Dedukh Katarzyna Haczkiewicz Beata Rozenblut-Kościsty Mikołaj Kaźmierczak Krzysztof Kolenda Ewa Serwa Agnieszka Pietras-Lebioda Alla Krasikova Maria Ogielska |
author_facet |
Magdalena Chmielewska Dmitry Dedukh Katarzyna Haczkiewicz Beata Rozenblut-Kościsty Mikołaj Kaźmierczak Krzysztof Kolenda Ewa Serwa Agnieszka Pietras-Lebioda Alla Krasikova Maria Ogielska |
author_sort |
Magdalena Chmielewska |
title |
The programmed DNA elimination and formation of micronuclei in germ line cells of the natural hybridogenetic water frog Pelophylax esculentus |
title_short |
The programmed DNA elimination and formation of micronuclei in germ line cells of the natural hybridogenetic water frog Pelophylax esculentus |
title_full |
The programmed DNA elimination and formation of micronuclei in germ line cells of the natural hybridogenetic water frog Pelophylax esculentus |
title_fullStr |
The programmed DNA elimination and formation of micronuclei in germ line cells of the natural hybridogenetic water frog Pelophylax esculentus |
title_full_unstemmed |
The programmed DNA elimination and formation of micronuclei in germ line cells of the natural hybridogenetic water frog Pelophylax esculentus |
title_sort |
programmed dna elimination and formation of micronuclei in germ line cells of the natural hybridogenetic water frog pelophylax esculentus |
publisher |
Nature Portfolio |
publishDate |
2018 |
url |
https://doaj.org/article/a00a62dd9d2e4960a106005f1b167185 |
work_keys_str_mv |
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