New insights into the molecular basis of gametogenesis of the hybridogenetic water frog Pelophylax esculentus
The molecular processes underlying genome exclusion and clonal gamete formation in the germline of hybridogenetic water frog hybrids are poorly understood. For the first time, we have characterized 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 species (60 LL, 252 RR) and their hybridogenetic hybrid, Pelophylax esculentus (340 LR), from population systems that differ in genotypic composition, sex ratio, and modes of inheritance. Ten gametogenic genes may be linked to the population system and, thus, indirectly to the reproductive mode, i.e., the premeiotic 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 various processes, including the control of 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. In addition, both the transcriptome and SNP data provide evidence for gene flow between the L and R genomes. The results are consistent with the clonal inheritance patterns described for P. esculentus and suggest that genome exclusion is based on complex genomic interactions involving multiple genes and molecular factors. Furthermore, our data suggest that interspecific gene flow has played an important role in the evolution of different inheritance modes in P. esculentus, leading to the emergence of distinct population systems.