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Optional Endoreplication and Selective Elimination of Parental Genomes during Oogenesis in Diploid and Triploid Hybrid European Water Frogs.

Dedukh D, Litvinchuk S, Rosanov J, Mazepa G, Saifitdinova A, Shabanov D, Krasikova A - PLoS ONE (2015)

Bottom Line: Obtained results allowed us to suggest that during oogenesis the endoreplication involves all genomes occurring before the selective genome elimination.We accepted the hypothesis that only elimination of one copied genome occurs premeiotically in most of triploid hybrid females.Diploid hybrid frogs demonstrate an enlarged frequency of deviations in oogenesis comparatively to triploid hybrids.

View Article: PubMed Central - PubMed

Affiliation: Saint-Petersburg State University, Saint-Petersburg, Russia.

ABSTRACT
Incompatibilities between parental genomes decrease viability of interspecific hybrids; however, deviations from canonical gametogenesis such as genome endoreplication and elimination can rescue hybrid organisms. To evaluate frequency and regularity of genome elimination and endoreplication during gametogenesis in hybrid animals with different ploidy, we examined genome composition in oocytes of di- and triploid hybrid frogs of the Pelophylax esculentus complex. Obtained results allowed us to suggest that during oogenesis the endoreplication involves all genomes occurring before the selective genome elimination. We accepted the hypothesis that only elimination of one copied genome occurs premeiotically in most of triploid hybrid females. At the same time, we rejected the hypothesis stating that the genome of parental species hybrid frogs co-exist with is always eliminated during oogenesis in diploid hybrids. Diploid hybrid frogs demonstrate an enlarged frequency of deviations in oogenesis comparatively to triploid hybrids. Typical for hybrid frogs deviations in gametogenesis increase variability of produced gametes and provide a mechanism for appearance of different forms of hybrids.

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Unusual lampbrush chromosome sets from oocytes of triploid hybrid frogs with RRL genotype and two diploid hybrid frogs.(a,a`,b,b`) Lampbrush chromosome sets from oocytes of some triploid hybrid frogs with RRL genotype represented by 39 bivalents (a,a`) and 39 univalents (b,b`), with 26 bi- or univalents corresponding to P. ridibundus lampbrush chromosomes and 13 bi- or univalents corresponding to P. lessonae lampbrush chromosomes. (c,c`) Lampbrush chromosome set from oocyte of one diploid hybrid frog represented by 26 univalents. Some univalents are similar to P. ridibundus lampbrush chromosomes, while other univalents are similar to P. lessonae lampbrush chromosomes. (d,d`) Lampbrush chromosome set from oocyte of one diploid hybrid frog represented by 26 bivalents corresponding to P. ridibundus lampbrush chromosomes. Letter symbols indicate alphabetic numbering of all lampbrush chromosomes; italic type shows correspondence of identified chromosomes to genotype of parental species: r—to P. ridibundus, l—to P. lessonae. Chromosomes were counterstained with DAPI (a,b,c,d). Corresponding phase-contrast micrographs are shown (a`,b`,c`,d`). Scale bars = 50 μm.
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pone.0123304.g004: Unusual lampbrush chromosome sets from oocytes of triploid hybrid frogs with RRL genotype and two diploid hybrid frogs.(a,a`,b,b`) Lampbrush chromosome sets from oocytes of some triploid hybrid frogs with RRL genotype represented by 39 bivalents (a,a`) and 39 univalents (b,b`), with 26 bi- or univalents corresponding to P. ridibundus lampbrush chromosomes and 13 bi- or univalents corresponding to P. lessonae lampbrush chromosomes. (c,c`) Lampbrush chromosome set from oocyte of one diploid hybrid frog represented by 26 univalents. Some univalents are similar to P. ridibundus lampbrush chromosomes, while other univalents are similar to P. lessonae lampbrush chromosomes. (d,d`) Lampbrush chromosome set from oocyte of one diploid hybrid frog represented by 26 bivalents corresponding to P. ridibundus lampbrush chromosomes. Letter symbols indicate alphabetic numbering of all lampbrush chromosomes; italic type shows correspondence of identified chromosomes to genotype of parental species: r—to P. ridibundus, l—to P. lessonae. Chromosomes were counterstained with DAPI (a,b,c,d). Corresponding phase-contrast micrographs are shown (a`,b`,c`,d`). Scale bars = 50 μm.

Mentions: Two females with RLX genotype produced oocytes with unusual chromosomal sets. In one triploid female with RLX genotype (S1 Table), presumably RRL one, 34 oocytes contained 39 univalents, where 26 ones corresponded to P. ridibundus lampbrush chromosomes and 13 ones corresponded to P. lessonae lampbrush chromosomes (Fig 4b,b`; S1c1–d2 Fig). Importantly, 26 univalents corresponding to P. ridibundus lampbrush chromosomes did not form bivalents. Apparently, to form such oocytes neither endoreplication nor elimination occurred during gametogenesis in this triploid female (Fig 5a). In this individual, we also described 4 oocytes with 39 bivalents, where 26 ones were similar to P. ridibundus bivalents, while 13 ones were similar to P. lessonae bivalents (Fig 4a,a`; S1a1–a6`,b1–b3` Fig). Premeiotic endoreplication of the whole triploid karyotype in germ cells without any elimination is required to form oocytes with 39 bivalents (Fig 5a). One oocyte contained 8 bivalents of P. ridibundus and 15 univalents corresponding to either P. ridibundus or P. lessonae lampbrush chromosomes (S2a1–a4 and S3b,b` Figs). Such oocytes indicate abnormalities in conjugation of certain chromosomes of P. ridibundus chromosomal set. In that case, individual chromosomes of P. ridibundus were lost during oogenesis and endoreplication did not occur (Fig 5a).


Optional Endoreplication and Selective Elimination of Parental Genomes during Oogenesis in Diploid and Triploid Hybrid European Water Frogs.

Dedukh D, Litvinchuk S, Rosanov J, Mazepa G, Saifitdinova A, Shabanov D, Krasikova A - PLoS ONE (2015)

Unusual lampbrush chromosome sets from oocytes of triploid hybrid frogs with RRL genotype and two diploid hybrid frogs.(a,a`,b,b`) Lampbrush chromosome sets from oocytes of some triploid hybrid frogs with RRL genotype represented by 39 bivalents (a,a`) and 39 univalents (b,b`), with 26 bi- or univalents corresponding to P. ridibundus lampbrush chromosomes and 13 bi- or univalents corresponding to P. lessonae lampbrush chromosomes. (c,c`) Lampbrush chromosome set from oocyte of one diploid hybrid frog represented by 26 univalents. Some univalents are similar to P. ridibundus lampbrush chromosomes, while other univalents are similar to P. lessonae lampbrush chromosomes. (d,d`) Lampbrush chromosome set from oocyte of one diploid hybrid frog represented by 26 bivalents corresponding to P. ridibundus lampbrush chromosomes. Letter symbols indicate alphabetic numbering of all lampbrush chromosomes; italic type shows correspondence of identified chromosomes to genotype of parental species: r—to P. ridibundus, l—to P. lessonae. Chromosomes were counterstained with DAPI (a,b,c,d). Corresponding phase-contrast micrographs are shown (a`,b`,c`,d`). Scale bars = 50 μm.
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4403867&req=5

pone.0123304.g004: Unusual lampbrush chromosome sets from oocytes of triploid hybrid frogs with RRL genotype and two diploid hybrid frogs.(a,a`,b,b`) Lampbrush chromosome sets from oocytes of some triploid hybrid frogs with RRL genotype represented by 39 bivalents (a,a`) and 39 univalents (b,b`), with 26 bi- or univalents corresponding to P. ridibundus lampbrush chromosomes and 13 bi- or univalents corresponding to P. lessonae lampbrush chromosomes. (c,c`) Lampbrush chromosome set from oocyte of one diploid hybrid frog represented by 26 univalents. Some univalents are similar to P. ridibundus lampbrush chromosomes, while other univalents are similar to P. lessonae lampbrush chromosomes. (d,d`) Lampbrush chromosome set from oocyte of one diploid hybrid frog represented by 26 bivalents corresponding to P. ridibundus lampbrush chromosomes. Letter symbols indicate alphabetic numbering of all lampbrush chromosomes; italic type shows correspondence of identified chromosomes to genotype of parental species: r—to P. ridibundus, l—to P. lessonae. Chromosomes were counterstained with DAPI (a,b,c,d). Corresponding phase-contrast micrographs are shown (a`,b`,c`,d`). Scale bars = 50 μm.
Mentions: Two females with RLX genotype produced oocytes with unusual chromosomal sets. In one triploid female with RLX genotype (S1 Table), presumably RRL one, 34 oocytes contained 39 univalents, where 26 ones corresponded to P. ridibundus lampbrush chromosomes and 13 ones corresponded to P. lessonae lampbrush chromosomes (Fig 4b,b`; S1c1–d2 Fig). Importantly, 26 univalents corresponding to P. ridibundus lampbrush chromosomes did not form bivalents. Apparently, to form such oocytes neither endoreplication nor elimination occurred during gametogenesis in this triploid female (Fig 5a). In this individual, we also described 4 oocytes with 39 bivalents, where 26 ones were similar to P. ridibundus bivalents, while 13 ones were similar to P. lessonae bivalents (Fig 4a,a`; S1a1–a6`,b1–b3` Fig). Premeiotic endoreplication of the whole triploid karyotype in germ cells without any elimination is required to form oocytes with 39 bivalents (Fig 5a). One oocyte contained 8 bivalents of P. ridibundus and 15 univalents corresponding to either P. ridibundus or P. lessonae lampbrush chromosomes (S2a1–a4 and S3b,b` Figs). Such oocytes indicate abnormalities in conjugation of certain chromosomes of P. ridibundus chromosomal set. In that case, individual chromosomes of P. ridibundus were lost during oogenesis and endoreplication did not occur (Fig 5a).

Bottom Line: Obtained results allowed us to suggest that during oogenesis the endoreplication involves all genomes occurring before the selective genome elimination.We accepted the hypothesis that only elimination of one copied genome occurs premeiotically in most of triploid hybrid females.Diploid hybrid frogs demonstrate an enlarged frequency of deviations in oogenesis comparatively to triploid hybrids.

View Article: PubMed Central - PubMed

Affiliation: Saint-Petersburg State University, Saint-Petersburg, Russia.

ABSTRACT
Incompatibilities between parental genomes decrease viability of interspecific hybrids; however, deviations from canonical gametogenesis such as genome endoreplication and elimination can rescue hybrid organisms. To evaluate frequency and regularity of genome elimination and endoreplication during gametogenesis in hybrid animals with different ploidy, we examined genome composition in oocytes of di- and triploid hybrid frogs of the Pelophylax esculentus complex. Obtained results allowed us to suggest that during oogenesis the endoreplication involves all genomes occurring before the selective genome elimination. We accepted the hypothesis that only elimination of one copied genome occurs premeiotically in most of triploid hybrid females. At the same time, we rejected the hypothesis stating that the genome of parental species hybrid frogs co-exist with is always eliminated during oogenesis in diploid hybrids. Diploid hybrid frogs demonstrate an enlarged frequency of deviations in oogenesis comparatively to triploid hybrids. Typical for hybrid frogs deviations in gametogenesis increase variability of produced gametes and provide a mechanism for appearance of different forms of hybrids.

Show MeSH
Related in: MedlinePlus