# New insights into the molecular basis of gametogenesis in the hybridogenetic water frog Pelophylax esculentus

**Authors:** Marcela Plötner, Martin Meixner, Albert J. Poustka, José H. Grau, Sabrina Theusner, Karsten Liere, Tino Schüllermann, Marie Doležálková‑Kaštánková, Lukas Choleva, Jörg Plötner

PMC · DOI: 10.1038/s41598-026-37515-w · Scientific Reports · 2026-02-04

## TL;DR

This study explores how certain genes contribute to the unique reproductive process in hybrid water frogs, shedding light on how genomes are excluded during gamete formation.

## Contribution

The study provides the first characterization of gametogenic gene sequences and their SNPs in hybrid water frogs, linking them to inheritance patterns.

## Key findings

- Ten gametogenic genes are associated with inheritance modes and genome exclusion in hybrid water frogs.
- These genes are involved in processes like spindle formation, epigenetic silencing, and DNA repair.
- Bidirectional gene flow between species has influenced the evolution of clonal inheritance in P. esculentus.

## Abstract

The molecular mechanisms underlying genome exclusion and clonal gamete formation in the germline of hybridogenetic water frog hybrids are poorly understood. Here, we characterize for the first time the coding sequences of 160 gametogenic genes from the European water frog species Pelophylax lessonae (LL) and Pelophylax ridibundus (RR). In addition, single nucleotide polymorphisms (SNPs) in 52 of these genes were analyzed in both parental species (60 LL, 252 RR) and in 340 diploid hybrids, Pelophylax esculentus (LR), sampled from population systems differing in genotypic composition, sex ratio, and inheritance modes. Ten of these genes showed associations with the population system and may therefore be related to the mode of inheritance, namely the exclusion of the ridibundus (R) genome in the lessonae–esculentus system and/or the lessonae (L) genome in the ridibundus–esculentus system. These genes are involved in diverse cellular processes, including spindle formation and chromosome movement during mitosis and meiosis, epigenetic silencing, cell cycle regulation, double-strand break repair and homologous recombination, including transposable element silencing.

Our results are consistent with the clonal inheritance patterns described for P. esculentus and suggest that genome exclusion is governed by complex genomic networks involving multiple genes and molecular factors. Furthermore, our data indicate that bidirectional gene flow between the L and R gene pools has played an important role in the evolution of the different clonal inheritance modes in P. esculentus, thereby contributing to the emergence of distinct population systems.

The online version contains supplementary material available at 10.1038/s41598-026-37515-w.

## Linked entities

- **Species:** Pelophylax lessonae (taxon 45623), Pelophylax ridibundus (taxon 8406)

## Full-text entities

- **Genes:** pms2 (PMS1 homolog 2, mismatch repair system component) [NCBI Gene 100490402], rad51 (RAD51 recombinase) [NCBI Gene 549147] {aka brcc5, rad51-a, rad51-b, rad51a, reca, xrad51}, snap91 (synaptosome associated protein 91kDa) [NCBI Gene 100170497] {aka ap180, calm}, NFKB1 (nuclear factor kappa B subunit 1) [NCBI Gene 4790] {aka CVID12, EBP-1, KBF1, NF-kB, NF-kB1, NF-kappa-B1}, mns1 (meiosis specific nuclear structural 1) [NCBI Gene 100125104], dnmt1 (DNA methyltransferase 1) [NCBI Gene 100151716] {aka cxxc9, dnmt, mcmt, xDnmt1}, KIF22 [NCBI Gene 101731068], ago2 (argonaute 2, RISC catalytic component) [NCBI Gene 448205] {aka Argonaute2, eif2c2}, ung (uracil DNA glycosylase) [NCBI Gene 549334], h3-3a (H3.3 histone A) [NCBI Gene 448680] {aka h3.3, h3.3a, h3f3a}, mnd1 (meiotic nuclear divisions 1) [NCBI Gene 548566], dmrta2 (DMRT like family A2) [NCBI Gene 100125187] {aka dmrt5}, sfr1 (SWI5-dependent homologous recombination repair protein 1) [NCBI Gene 100380037] {aka c10orf78, mei5, meir5}, hormad1 (HORMA domain containing 1) [NCBI Gene 100489965], dmrt2 (doublesex and mab-3 related transcription factor 2) [NCBI Gene 100101749] {aka Terra-like}, exd1 (exonuclease 3'-5' domain containing 1) [NCBI Gene 100489477] {aka exdl1}, zfp36 (ZFP36 ring finger protein) [NCBI Gene 100127733] {aka C3H-1, g0s24, gos24, nup475, rnf162a, tis11}, rad51ap1 (RAD51 associated protein 1) [NCBI Gene 100380022] {aka pir51}, skp1 (S-phase kinase-associated protein 1) [NCBI Gene 549273] {aka emc19, ocp-ii, ocp2, skp1a, tceb1l}, nbn (nibrin) [NCBI Gene 733826] {aka nbs, nbs1}, nusap1 (nucleolar and spindle associated protein 1) [NCBI Gene 594881] {aka ankt, bm037, lnp, nusap, nusap1-a, nusap1-b}, sycp1 (synaptonemal complex protein 1) [NCBI Gene 101734306], fbxo5 (F-box protein 5) [NCBI Gene 733555] {aka emi1, fbx5, fbxo5-a, fbxo5-b}, henmt1 (HEN methyltransferase 1) [NCBI Gene 550540] {aka hen1, si:ch211-199m3.6, zgc:110175}, rad50 (RAD50 homolog, double strand break repair protein) [NCBI Gene 779556], tdrd1 (tudor domain containing 1) [NCBI Gene 100216261] {aka ct41.1}, spata1 (spermatogenesis associated 1) [NCBI Gene 100498562] {aka spap1}, ago3 (argonaute 3, RISC catalytic component) [NCBI Gene 100486574] {aka Argonaute3, eif2c3}, bcar1 (BCAR1, Cas family scaffold protein) [NCBI Gene 447979] {aka CASB3b, Crkas, cas, p130cas}, adcy9 (adenylate cyclase 9) [NCBI Gene 100126441] {aka xlAC}, bub1 (BUB1 mitotic checkpoint serine/threonine kinase) [NCBI Gene 780291] {aka bub1a, bub1l, hbub1, xbub1}, rpa3 (replication protein A3) [NCBI Gene 549380] {aka repa3}
- **Diseases:** fertility (MESH:D007246), Meiosis (MESH:C536875), POPSYS (MESH:D015619), developmental defects (MESH:D000094602), developmental disorders (MESH:D002658)
- **Chemicals:** ethanol (MESH:D000431), C (MESH:D002244), chloroform (MESH:D002725), MS-222 (MESH:C003636), phenol (MESH:D019800), GC (MESH:C057580), nucleotide (MESH:D009711), water (MESH:D014867), nitrogen (MESH:D009584), 3-aminobenzoic acid ethyl ester (-), dUTP (MESH:C027078)
- **Species:** Pelophylax lessonae (edible frog, species) [taxon 45623], Lucida (genus) [taxon 509419], Phasmatodea (stick insects, order) [taxon 7020], Pelophylax [taxon 8401], Bufotes baturae (Batura glacier toad, species) [taxon 389299], Mus musculus (house mouse, species) [taxon 10090], Bacillus (genus) [taxon 55087], Homo sapiens (human, species) [taxon 9606], Cobitis (genus) [taxon 47718], Wallaconchis ater (species) [taxon 2231505], Pelophylax grafi (species) [taxon 1752047], Pelophylax ridibundus (European green frog, species) [taxon 8406], Pelophylax bergeri (Italian pool frog, species) [taxon 69490], Poeciliopsis monacha (headwater livebearer, species) [taxon 73161], Pelophylax shqipericus (Albanian pool frog, species) [taxon 44326], Danio rerio (leopard danio, species) [taxon 7955], Pelophylax kurtmuelleri (Balkan frog, species) [taxon 73493], Xenopus laevis (African clawed frog, species) [taxon 8355], Amphibia (amphibians, class) [taxon 8292], Pelophylax cf. ridibundus (species) [taxon 157238], Pelophylax perezi (Iberian green frog, species) [taxon 8403], Xenopus tropicalis (tropical clawed frog, species) [taxon 8364]
- **Cell lines:** PL88 — Homo sapiens (Human), Lung adenocarcinoma, Cancer cell line (CVCL_RA75)

## Full text

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## Figures

6 figures with captions in the complete paper: https://tomesphere.com/paper/PMC12876976/full.md

## References

19 references — full list in the complete paper: https://tomesphere.com/paper/PMC12876976/full.md

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Source: https://tomesphere.com/paper/PMC12876976