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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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Suggested additional mechanisms of oogenesis in two triploid frogs with RRL genotype and one diploid hybrid frog.(a) During oogenesis of one triploid frog with RRL genotype neither elimination nor endoreplication occurred to form oocytes with 39 univalents (at the top), endoreplication of all genomes took place to form oocytes with 39 bivalents (in the middle), individual chromosomes from L genome (blue) were lost to form oocytes with aneuploid chromosomal sets (at the bottom). (b) During oogenesis of another triploid frog with RRL genotype elimination of L genome (blue) occurred to form oocytes with 13 bivalents (at the top), premeiotic elimination and endoreplication were absent to form oocytes with 39 univalents (in the middle), endoreplication of all genomes took place to form oocytes with 39 bivalents (at the bottom). (c) During oogenesis of one diploid hybrid frog L genome (blue) was eliminated in all observed oocytes. One round of R genome (orange) endoreplication occurred but bivalents formation was incomplete to form oocytes with both univalents and bivalents (at the top). Two rounds of endoreplication of R genome took place to form oocytes 26 bivalents (in the middle). One round of R genome endoreplication occurred but bivalents could not form that led to formation of oocytes with 26 univalents (at the bottom).
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pone.0123304.g005: Suggested additional mechanisms of oogenesis in two triploid frogs with RRL genotype and one diploid hybrid frog.(a) During oogenesis of one triploid frog with RRL genotype neither elimination nor endoreplication occurred to form oocytes with 39 univalents (at the top), endoreplication of all genomes took place to form oocytes with 39 bivalents (in the middle), individual chromosomes from L genome (blue) were lost to form oocytes with aneuploid chromosomal sets (at the bottom). (b) During oogenesis of another triploid frog with RRL genotype elimination of L genome (blue) occurred to form oocytes with 13 bivalents (at the top), premeiotic elimination and endoreplication were absent to form oocytes with 39 univalents (in the middle), endoreplication of all genomes took place to form oocytes with 39 bivalents (at the bottom). (c) During oogenesis of one diploid hybrid frog L genome (blue) was eliminated in all observed oocytes. One round of R genome (orange) endoreplication occurred but bivalents formation was incomplete to form oocytes with both univalents and bivalents (at the top). Two rounds of endoreplication of R genome took place to form oocytes 26 bivalents (in the middle). One round of R genome endoreplication occurred but bivalents could not form that led to formation of oocytes with 26 univalents (at the bottom).

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)

Suggested additional mechanisms of oogenesis in two triploid frogs with RRL genotype and one diploid hybrid frog.(a) During oogenesis of one triploid frog with RRL genotype neither elimination nor endoreplication occurred to form oocytes with 39 univalents (at the top), endoreplication of all genomes took place to form oocytes with 39 bivalents (in the middle), individual chromosomes from L genome (blue) were lost to form oocytes with aneuploid chromosomal sets (at the bottom). (b) During oogenesis of another triploid frog with RRL genotype elimination of L genome (blue) occurred to form oocytes with 13 bivalents (at the top), premeiotic elimination and endoreplication were absent to form oocytes with 39 univalents (in the middle), endoreplication of all genomes took place to form oocytes with 39 bivalents (at the bottom). (c) During oogenesis of one diploid hybrid frog L genome (blue) was eliminated in all observed oocytes. One round of R genome (orange) endoreplication occurred but bivalents formation was incomplete to form oocytes with both univalents and bivalents (at the top). Two rounds of endoreplication of R genome took place to form oocytes 26 bivalents (in the middle). One round of R genome endoreplication occurred but bivalents could not form that led to formation of oocytes with 26 univalents (at the bottom).
© Copyright Policy
Related In: Results  -  Collection

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

pone.0123304.g005: Suggested additional mechanisms of oogenesis in two triploid frogs with RRL genotype and one diploid hybrid frog.(a) During oogenesis of one triploid frog with RRL genotype neither elimination nor endoreplication occurred to form oocytes with 39 univalents (at the top), endoreplication of all genomes took place to form oocytes with 39 bivalents (in the middle), individual chromosomes from L genome (blue) were lost to form oocytes with aneuploid chromosomal sets (at the bottom). (b) During oogenesis of another triploid frog with RRL genotype elimination of L genome (blue) occurred to form oocytes with 13 bivalents (at the top), premeiotic elimination and endoreplication were absent to form oocytes with 39 univalents (in the middle), endoreplication of all genomes took place to form oocytes with 39 bivalents (at the bottom). (c) During oogenesis of one diploid hybrid frog L genome (blue) was eliminated in all observed oocytes. One round of R genome (orange) endoreplication occurred but bivalents formation was incomplete to form oocytes with both univalents and bivalents (at the top). Two rounds of endoreplication of R genome took place to form oocytes 26 bivalents (in the middle). One round of R genome endoreplication occurred but bivalents could not form that led to formation of oocytes with 26 univalents (at the bottom).
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