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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Autores principales: Magdalena Chmielewska, Dmitry Dedukh, Katarzyna Haczkiewicz, Beata Rozenblut-Kościsty, Mikołaj Kaźmierczak, Krzysztof Kolenda, Ewa Serwa, Agnieszka Pietras-Lebioda, Alla Krasikova, Maria Ogielska
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spelling 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)
institution DOAJ
collection DOAJ
language EN
topic Medicine
R
Science
Q
spellingShingle 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
description 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.
format 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
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