TY - JOUR

T1 - The programmed DNA elimination and formation of micronuclei in germ line cells of the natural hybridogenetic water frog Pelophylax esculentus

AU - Chmielewska, Magdalena

AU - Dedukh, Dmitry

AU - Haczkiewicz, Katarzyna

AU - Rozenblut-Kościsty, Beata

AU - Kaźmierczak, Mikołaj

AU - Kolenda, Krzysztof

AU - Serwa, Ewa

AU - Pietras-Lebioda, Agnieszka

AU - Krasikova, Alla

AU - Ogielska, Maria

PY - 2018/5/18

Y1 - 2018/5/18

N2 - 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.

AB - 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.

KW - UNIPARENTAL CHROMOSOME ELIMINATION

KW - HYBRID RANA-ESCULENTA

KW - GENOME ELIMINATION

KW - NUCLEAR-ENVELOPE

KW - PROGRESSIVE HETEROCHROMATINIZATION

KW - SCIARA-COPROPHILA

KW - MISGURNUS LOACH

KW - PLOIDY LEVELS

KW - REPRODUCTION

KW - MEIOSIS

UR - http://www.scopus.com/inward/record.url?scp=85047209728&partnerID=8YFLogxK

UR - http://www.mendeley.com/research/programmed-dna-elimination-formation-micronuclei-germ-line-cells-natural-hybridogenetic-water-frog-p

U2 - 10.1038/s41598-018-26168-z

DO - 10.1038/s41598-018-26168-z

M3 - Article

AN - SCOPUS:85047209728

VL - 8

JO - Scientific Reports

JF - Scientific Reports

SN - 2045-2322

IS - 1

M1 - 7870

ER -