Programmed Genome Elimination Is Evolutionarily Conserved Across Pelophylax Hybrids-As Evidenced by P. grafi Hybridogenetic Reproduction

Kód výsledku v IS VaVaI

<a href="https://www.isvavai.cz/riv?ss=detail&h=RIV%2F67985904%3A_____%2F25%3A00642525" target="_blank" >RIV/67985904:_____/25:00642525 - isvavai.cz</a>

Nalezeny alternativní kódy

RIV/61988987:17310/25:A2603DOS

Výsledek na webu

<a href="https://www.mdpi.com/2079-7737/14/11/1526" target="_blank" >https://www.mdpi.com/2079-7737/14/11/1526</a>

DOI - Digital Object Identifier

<a href="http://dx.doi.org/10.3390/biology14111526" target="_blank" >10.3390/biology14111526</a>

Jazyk výsledku

angličtina

Název v původním jazyce

Programmed Genome Elimination Is Evolutionarily Conserved Across Pelophylax Hybrids-As Evidenced by P. grafi Hybridogenetic Reproduction

Popis výsledku v původním jazyce

Simple Summary Hybrids are organisms that result from the crossing of two different species. While plant hybrids are relatively common, like bread wheats and orchids, animal hybrids are rare and often sterile, because the chromosomes from the two parental species cannot pair correctly during the formation of eggs and sperm. Some animal hybrids, however, have developed unusual ways to reproduce. One such strategy is hybridogenesis, where the genetic material of one parent is selectively discarded in the cells that give rise to gametes. As a result, hybrids clonally transmit only the chromosomes from one parental species, while eliminating those of the other. The frog Pelophylax grafi is a natural hybrid between the Iberian water frog (P. perezi) and the marsh frog (P. ridibundus). To understand how this hybrid reproduces, we studied its germ cells at different stages of development. We found that the chromosomes of P. perezi are selectively eliminated before the formation of eggs and sperm, while those of P. ridibundus are retained and passed on to the next generation. This process explains how P. grafi maintains fertile populations in nature and reveals a conserved mechanism that may underlie reproduction in other hybrid animals.Abstract Gametogenesis is a fundamental biological process that ensures both genetic recombination and the continuity of successive generations. Interspecific hybrids can reproduce through modified mechanisms, such as hybridogenesis, by transmitting clonal, unrecombined genomes of only one of the parental species via their gametes. Pelophylax grafi (RP) is a natural hybrid frog composed of mixed genomes (subgenomes) of two related species, Pelophylax perezi (P) and Pelophylax ridibundus (R), and coexists in populations with P. perezi. This study tested the involvement of programmed genome elimination in gamete production of P. grafi, providing new insight into reproductive mechanisms of hybrid vertebrates. Using comparative genomic hybridization (CGH) and fluorescent in situ hybridization (FISH), we examined the genomic constitution of germline cells in tadpoles and adult male and female P. grafi. Controlled crosses between P. perezi and P. grafi produced F1 hybrid tadpoles, whose genotypes confirmed that P. grafi parents transmitted the R subgenome through their gametes. In the early germline cells (gonocytes) of these tadpoles, P chromosomes were selectively eliminated via micronuclei formation during interphase. The occasional presence of the R genome and mixed R/P genome micronuclei suggests variability and imperfect fidelity in the elimination process. In adult hybrids, the majority of diplotene oocytes, spermatogonial stem cells (SSC) and spermatocytes carried R subgenomes. We demonstrated that programmed genome rearrangement in Pelophylax hybrids is an evolutionarily conserved mechanism underlying this unique reproductive strategy.

Název v anglickém jazyce

Programmed Genome Elimination Is Evolutionarily Conserved Across Pelophylax Hybrids-As Evidenced by P. grafi Hybridogenetic Reproduction

Popis výsledku anglicky

Simple Summary Hybrids are organisms that result from the crossing of two different species. While plant hybrids are relatively common, like bread wheats and orchids, animal hybrids are rare and often sterile, because the chromosomes from the two parental species cannot pair correctly during the formation of eggs and sperm. Some animal hybrids, however, have developed unusual ways to reproduce. One such strategy is hybridogenesis, where the genetic material of one parent is selectively discarded in the cells that give rise to gametes. As a result, hybrids clonally transmit only the chromosomes from one parental species, while eliminating those of the other. The frog Pelophylax grafi is a natural hybrid between the Iberian water frog (P. perezi) and the marsh frog (P. ridibundus). To understand how this hybrid reproduces, we studied its germ cells at different stages of development. We found that the chromosomes of P. perezi are selectively eliminated before the formation of eggs and sperm, while those of P. ridibundus are retained and passed on to the next generation. This process explains how P. grafi maintains fertile populations in nature and reveals a conserved mechanism that may underlie reproduction in other hybrid animals.Abstract Gametogenesis is a fundamental biological process that ensures both genetic recombination and the continuity of successive generations. Interspecific hybrids can reproduce through modified mechanisms, such as hybridogenesis, by transmitting clonal, unrecombined genomes of only one of the parental species via their gametes. Pelophylax grafi (RP) is a natural hybrid frog composed of mixed genomes (subgenomes) of two related species, Pelophylax perezi (P) and Pelophylax ridibundus (R), and coexists in populations with P. perezi. This study tested the involvement of programmed genome elimination in gamete production of P. grafi, providing new insight into reproductive mechanisms of hybrid vertebrates. Using comparative genomic hybridization (CGH) and fluorescent in situ hybridization (FISH), we examined the genomic constitution of germline cells in tadpoles and adult male and female P. grafi. Controlled crosses between P. perezi and P. grafi produced F1 hybrid tadpoles, whose genotypes confirmed that P. grafi parents transmitted the R subgenome through their gametes. In the early germline cells (gonocytes) of these tadpoles, P chromosomes were selectively eliminated via micronuclei formation during interphase. The occasional presence of the R genome and mixed R/P genome micronuclei suggests variability and imperfect fidelity in the elimination process. In adult hybrids, the majority of diplotene oocytes, spermatogonial stem cells (SSC) and spermatocytes carried R subgenomes. We demonstrated that programmed genome rearrangement in Pelophylax hybrids is an evolutionarily conserved mechanism underlying this unique reproductive strategy.

Druh

J_imp - Článek v periodiku v databázi Web of Science

CEP obor

—

OECD FORD obor

10613 - Zoology

Projekt

<a href="/cs/project/GF23-07028K" target="_blank" >GF23-07028K: Porušení pravidel: modifikované způsoby sexuální reprodukce u obratlovců</a><br>

Návaznosti

I - Institucionalni podpora na dlouhodoby koncepcni rozvoj vyzkumne organizace

Rok uplatnění

2025

Kód důvěrnosti údajů

S - Úplné a pravdivé údaje o projektu nepodléhají ochraně podle zvláštních právních předpisů

Název periodika

Biology

ISSN

2079-7737

e-ISSN

2079-7737

Svazek periodika

14

Číslo periodika v rámci svazku

11

Stát vydavatele periodika

CH - Švýcarská konfederace

Počet stran výsledku

27

Strana od-do

1526

Kód UT WoS článku

001624038900001

EID výsledku v databázi Scopus

2-s2.0-105023850411