Abstract
In most organisms, cells typically maintain genome integrity, as radical genome reorganization leads to dramatic consequences. However, certain organisms, ranging from unicellular ciliates to vertebrates, are able to selectively eliminate specific parts of their genome during certain stages of development. Moreover, partial or complete elimination of one of the parental genomes occurs in interspecies hybrids reproducing asexually. Although several examples of this phenomenon are known, the molecular and cellular processes involved in selective elimination of genetic material remain largely undescribed for the majority of such organisms. Here, we elucidate the process of selective genome elimination in water frog hybrids from the Pelophylax esculentus complex reproducing through hybridogenesis. Specifically, in the gonads of diploid and triploid hybrids, but not those of the parental species, we revealed micronuclei in the cytoplasm of germ cells. In each micronucleus, only one centromere was detected with antibodies against kinetochore proteins, suggesting that each micronucleus comprises a single chromosome. Using 3D-FISH with species-specific centromeric probe, we determined the role of micronuclei in selective genome elimination. We found that in triploid LLR hybrids, micronuclei preferentially contain P. ridibundus chromosomes, while in diploid hybrids, micronuclei preferentially contain P. lessonae chromosomes. The number of centromere signals in the nuclei suggested that germ cells were aneuploid until they eliminate the whole chromosomal set of one of the parental species. Furthermore, in diploid hybrids, misaligned P. lessonae chromosomes were observed during the metaphase stage of germ cells division, suggesting their possible elimination due to the inability to attach to the spindle and segregate properly. Additionally, we described gonocytes with an increased number of P. ridibundus centromeres, indicating duplication of the genetic material. We conclude that selective genome elimination from germ cells of diploid and triploid hybrids occurs via the gradual elimination of individual chromosomes of one of the parental genomes, which are enclosed within micronuclei.
Highlights
In most organisms, cells typically maintain genome integrity, as radical genome reorganization leads to dramatic consequences
Diploid tadpoles were produced from various crossings of diploid and triploid hybrids as well as P. lessonae and P. ridibundus individuals, involving both females and males of all taxa: (1) both parents were hybrids, one 2n and one 3n (5 crosses); (2) one parent was a 2n (10 crosses) or 3n (2 crosses) hybrid, while the second parent came from a parental species; or (3) both parents came from the parental species
In the gonads of hybrid tadpoles and P. ridibundus individuals, gonocytes were identified with antibodies against the Vasa protein (Fig. S1a,b) and appeared as large cells with multiple nucleoli and less intensive chromatin staining compared to somatic cells
Summary
Cells typically maintain genome integrity, as radical genome reorganization leads to dramatic consequences. The number of centromere signals in the nuclei suggested that germ cells were aneuploid until they eliminate the whole chromosomal set of one of the parental species. We conclude that selective genome elimination from germ cells of diploid and triploid hybrids occurs via the gradual elimination of individual chromosomes of one of the parental genomes, which are enclosed within micronuclei. Interspecies hybrids exploit selective genome elimination to reproduce and are known to occur among animals that reproduce without recombination, collectively termed asexuals[12,13,14] In such animals, gametogenesis is modified to produce gametes with an unreduced genome composition, and in the vast majority of these cases the genome of one parental species (usually paternal) is selectively excluded after www.nature.com/scientificreports fertilization (androgenesis, kleptogenesis, gynogenesis) or during gonocyte multiplication (hybridogenesis and triploid hybridogenesis)[11,13,15,16]. The obtained results allowed us to estimate the number and origin of the eliminated chromosomes in each micronucleus in the gonads of hybrid tadpoles
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