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Genome elimination from the germline cells in diploid and triploid male water frogs Pelophylax esculentus

Hybridogenesis is a hemiclonal reproductive strategy in diploid and triploid hybrids. Our study model is a frog P. esculentus (diploid RL and triploids RLL and RRL), a natural hybrid between P. lessonae (LL) and P. ridibundus (RR). Hybridogenesis relies on elimination of one genome (L or R) from gon...

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Autores principales: Chmielewska, Magdalena, Kaźmierczak, Mikołaj, Rozenblut-Kościsty, Beata, Kolenda, Krzysztof, Dudzik, Anna, Dedukh, Dmitrij, Ogielska, Maria
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9615423/
https://www.ncbi.nlm.nih.gov/pubmed/36313575
http://dx.doi.org/10.3389/fcell.2022.1008506
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author Chmielewska, Magdalena
Kaźmierczak, Mikołaj
Rozenblut-Kościsty, Beata
Kolenda, Krzysztof
Dudzik, Anna
Dedukh, Dmitrij
Ogielska, Maria
author_facet Chmielewska, Magdalena
Kaźmierczak, Mikołaj
Rozenblut-Kościsty, Beata
Kolenda, Krzysztof
Dudzik, Anna
Dedukh, Dmitrij
Ogielska, Maria
author_sort Chmielewska, Magdalena
collection PubMed
description Hybridogenesis is a hemiclonal reproductive strategy in diploid and triploid hybrids. Our study model is a frog P. esculentus (diploid RL and triploids RLL and RRL), a natural hybrid between P. lessonae (LL) and P. ridibundus (RR). Hybridogenesis relies on elimination of one genome (L or R) from gonocytes (G) in tadpole gonads during prespermatogenesis, but not from spermatogonial stem cells (SSCs) in adults. Here we provide the first comprehensive study of testis morphology combined with chromosome composition in the full spectrum of spermatogenic cells. Using genomic in situ hybridization (GISH) and FISH we determined genomes in metaphase plates and interphase nuclei in Gs and SSCs. We traced genomic composition of SSCs, spermatocytes and spermatozoa in individual adult males that were crossed with females of the parental species and gave progeny. Degenerating gonocytes (24%–39%) and SSCs (18%–20%) led to partial sterility of juvenile and adult gonads. We conclude that elimination and endoreplication not properly completed during prespermatogenesis may be halted when gonocytes become dormant in juveniles. After resumption of mitotic divisions by SSCs in adults, these 20% of cells with successful genome elimination and endoreplication continue spermatogenesis, while in about 80% spermatogenesis is deficient. Majority of abnormal cells are eliminated by cell death, however some of them give rise to aneuploid spermatocytes and spermatozoa which shows that hybridogenesis is a wasteful process.
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spelling pubmed-96154232022-10-29 Genome elimination from the germline cells in diploid and triploid male water frogs Pelophylax esculentus Chmielewska, Magdalena Kaźmierczak, Mikołaj Rozenblut-Kościsty, Beata Kolenda, Krzysztof Dudzik, Anna Dedukh, Dmitrij Ogielska, Maria Front Cell Dev Biol Cell and Developmental Biology Hybridogenesis is a hemiclonal reproductive strategy in diploid and triploid hybrids. Our study model is a frog P. esculentus (diploid RL and triploids RLL and RRL), a natural hybrid between P. lessonae (LL) and P. ridibundus (RR). Hybridogenesis relies on elimination of one genome (L or R) from gonocytes (G) in tadpole gonads during prespermatogenesis, but not from spermatogonial stem cells (SSCs) in adults. Here we provide the first comprehensive study of testis morphology combined with chromosome composition in the full spectrum of spermatogenic cells. Using genomic in situ hybridization (GISH) and FISH we determined genomes in metaphase plates and interphase nuclei in Gs and SSCs. We traced genomic composition of SSCs, spermatocytes and spermatozoa in individual adult males that were crossed with females of the parental species and gave progeny. Degenerating gonocytes (24%–39%) and SSCs (18%–20%) led to partial sterility of juvenile and adult gonads. We conclude that elimination and endoreplication not properly completed during prespermatogenesis may be halted when gonocytes become dormant in juveniles. After resumption of mitotic divisions by SSCs in adults, these 20% of cells with successful genome elimination and endoreplication continue spermatogenesis, while in about 80% spermatogenesis is deficient. Majority of abnormal cells are eliminated by cell death, however some of them give rise to aneuploid spermatocytes and spermatozoa which shows that hybridogenesis is a wasteful process. Frontiers Media S.A. 2022-10-14 /pmc/articles/PMC9615423/ /pubmed/36313575 http://dx.doi.org/10.3389/fcell.2022.1008506 Text en Copyright © 2022 Chmielewska, Kaźmierczak, Rozenblut-Kościsty, Kolenda, Dudzik, Dedukh and Ogielska. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Cell and Developmental Biology
Chmielewska, Magdalena
Kaźmierczak, Mikołaj
Rozenblut-Kościsty, Beata
Kolenda, Krzysztof
Dudzik, Anna
Dedukh, Dmitrij
Ogielska, Maria
Genome elimination from the germline cells in diploid and triploid male water frogs Pelophylax esculentus
title Genome elimination from the germline cells in diploid and triploid male water frogs Pelophylax esculentus
title_full Genome elimination from the germline cells in diploid and triploid male water frogs Pelophylax esculentus
title_fullStr Genome elimination from the germline cells in diploid and triploid male water frogs Pelophylax esculentus
title_full_unstemmed Genome elimination from the germline cells in diploid and triploid male water frogs Pelophylax esculentus
title_short Genome elimination from the germline cells in diploid and triploid male water frogs Pelophylax esculentus
title_sort genome elimination from the germline cells in diploid and triploid male water frogs pelophylax esculentus
topic Cell and Developmental Biology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9615423/
https://www.ncbi.nlm.nih.gov/pubmed/36313575
http://dx.doi.org/10.3389/fcell.2022.1008506
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