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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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Interstitial (TTAGGG)n repeat sites mapping allows to identify parental chromosomes in oocytes of hybrid frogs.(a-c) FISH mapping of (TTAGGG)n repeat on metaphase chromosomes of P. lessonae (a, a`), P. ridibundus (b), and diploid P. esculentus (c). One or two interstitial (TTAGGG)n repeat sites distinguish parental NOR-bearing chromosomes H (arrows). Asterisks indicate enlarged fragment with two NOR-bearing chromosomes of P. lessonae. Arrows indicate interstitial (TTAGGG)n repeat sites. (d1–f1`) Lampbrush chromosomes from oocytes of triploid hybrid frogs with RRL (d1–d6`) and LLR (e1–f1`) genotypes. FISH mapping of (TTAGGG)n repeat revealed lampbrush chromosome H corresponding to P. ridibundus (d6) or P. lessonae (e1) LBC H. Interstitial (TTAGGG)n repeat sites are shown by square brackets. Lampbrush chromosomes corresponding to P. ridibundus LBC F (d1,d1`), G (d2,d2`), D (d3,d3`), I (d4,d4`), B (d5,d5`), and P. lessonae LBC B (e2,b2`), F (e3,b3`), L (f1,f1`) are shown. Chromosomes on micrographs (d1–d6`) were taken from the full lampbrush chromosome set represented on Fig 1a,a`. Chromosomes on micrographs (e1–e3`) were taken from the from the full lampbrush chromosome set represented on Fig 1c,c`. Various marker structures are shown by arrows. Chromosomes were counterstained with DAPI. Corresponding phase-contrast micrographs are shown (d1`,d2`,d3`,d4`,d5`,d6`,e1`,e2`,e3`,f1`). Arrowheads indicate centromeres. Scale bars = 10 μm for all panels except a`, where scale bar = 2 μm.
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pone.0123304.g002: Interstitial (TTAGGG)n repeat sites mapping allows to identify parental chromosomes in oocytes of hybrid frogs.(a-c) FISH mapping of (TTAGGG)n repeat on metaphase chromosomes of P. lessonae (a, a`), P. ridibundus (b), and diploid P. esculentus (c). One or two interstitial (TTAGGG)n repeat sites distinguish parental NOR-bearing chromosomes H (arrows). Asterisks indicate enlarged fragment with two NOR-bearing chromosomes of P. lessonae. Arrows indicate interstitial (TTAGGG)n repeat sites. (d1–f1`) Lampbrush chromosomes from oocytes of triploid hybrid frogs with RRL (d1–d6`) and LLR (e1–f1`) genotypes. FISH mapping of (TTAGGG)n repeat revealed lampbrush chromosome H corresponding to P. ridibundus (d6) or P. lessonae (e1) LBC H. Interstitial (TTAGGG)n repeat sites are shown by square brackets. Lampbrush chromosomes corresponding to P. ridibundus LBC F (d1,d1`), G (d2,d2`), D (d3,d3`), I (d4,d4`), B (d5,d5`), and P. lessonae LBC B (e2,b2`), F (e3,b3`), L (f1,f1`) are shown. Chromosomes on micrographs (d1–d6`) were taken from the full lampbrush chromosome set represented on Fig 1a,a`. Chromosomes on micrographs (e1–e3`) were taken from the from the full lampbrush chromosome set represented on Fig 1c,c`. Various marker structures are shown by arrows. Chromosomes were counterstained with DAPI. Corresponding phase-contrast micrographs are shown (d1`,d2`,d3`,d4`,d5`,d6`,e1`,e2`,e3`,f1`). Arrowheads indicate centromeres. Scale bars = 10 μm for all panels except a`, where scale bar = 2 μm.

Mentions: In R-E population system, we analyzed genome composition in oocytes of 9 diploid, 13 triploid P. esculentus females with RRL genotype (including females with RLX genotype) and 5 triploid females with LLR genotype. Algorithm to identify the type of genome transmitted in oocytes of hybrid frogs is represented in S1 Material. At first, we describe the chromosomal sets in oocytes of triploid frogs with RRL genotype. We found that 11 females with RRL genotype produced only one type of oocytes with 13 bivalents corresponding to P. ridibundus bivalents (Figs 1a,a` and 2d1–d6`; S1 Movie). Combining the data on hybrid females ploidy and oocyte genome composition, we evaluated appearance of genome elimination and endoreplication events during gametogenesis. We suggest that to form typical oocytes with 13 bivalents corresponding to P. ridibundus bivalents, elimination of L genome occurred premeiotically while two remaining R genomes presumably conjugated during meiosis (Fig 3a).


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)

Interstitial (TTAGGG)n repeat sites mapping allows to identify parental chromosomes in oocytes of hybrid frogs.(a-c) FISH mapping of (TTAGGG)n repeat on metaphase chromosomes of P. lessonae (a, a`), P. ridibundus (b), and diploid P. esculentus (c). One or two interstitial (TTAGGG)n repeat sites distinguish parental NOR-bearing chromosomes H (arrows). Asterisks indicate enlarged fragment with two NOR-bearing chromosomes of P. lessonae. Arrows indicate interstitial (TTAGGG)n repeat sites. (d1–f1`) Lampbrush chromosomes from oocytes of triploid hybrid frogs with RRL (d1–d6`) and LLR (e1–f1`) genotypes. FISH mapping of (TTAGGG)n repeat revealed lampbrush chromosome H corresponding to P. ridibundus (d6) or P. lessonae (e1) LBC H. Interstitial (TTAGGG)n repeat sites are shown by square brackets. Lampbrush chromosomes corresponding to P. ridibundus LBC F (d1,d1`), G (d2,d2`), D (d3,d3`), I (d4,d4`), B (d5,d5`), and P. lessonae LBC B (e2,b2`), F (e3,b3`), L (f1,f1`) are shown. Chromosomes on micrographs (d1–d6`) were taken from the full lampbrush chromosome set represented on Fig 1a,a`. Chromosomes on micrographs (e1–e3`) were taken from the from the full lampbrush chromosome set represented on Fig 1c,c`. Various marker structures are shown by arrows. Chromosomes were counterstained with DAPI. Corresponding phase-contrast micrographs are shown (d1`,d2`,d3`,d4`,d5`,d6`,e1`,e2`,e3`,f1`). Arrowheads indicate centromeres. Scale bars = 10 μm for all panels except a`, where scale bar = 2 μm.
© Copyright Policy
Related In: Results  -  Collection

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

pone.0123304.g002: Interstitial (TTAGGG)n repeat sites mapping allows to identify parental chromosomes in oocytes of hybrid frogs.(a-c) FISH mapping of (TTAGGG)n repeat on metaphase chromosomes of P. lessonae (a, a`), P. ridibundus (b), and diploid P. esculentus (c). One or two interstitial (TTAGGG)n repeat sites distinguish parental NOR-bearing chromosomes H (arrows). Asterisks indicate enlarged fragment with two NOR-bearing chromosomes of P. lessonae. Arrows indicate interstitial (TTAGGG)n repeat sites. (d1–f1`) Lampbrush chromosomes from oocytes of triploid hybrid frogs with RRL (d1–d6`) and LLR (e1–f1`) genotypes. FISH mapping of (TTAGGG)n repeat revealed lampbrush chromosome H corresponding to P. ridibundus (d6) or P. lessonae (e1) LBC H. Interstitial (TTAGGG)n repeat sites are shown by square brackets. Lampbrush chromosomes corresponding to P. ridibundus LBC F (d1,d1`), G (d2,d2`), D (d3,d3`), I (d4,d4`), B (d5,d5`), and P. lessonae LBC B (e2,b2`), F (e3,b3`), L (f1,f1`) are shown. Chromosomes on micrographs (d1–d6`) were taken from the full lampbrush chromosome set represented on Fig 1a,a`. Chromosomes on micrographs (e1–e3`) were taken from the from the full lampbrush chromosome set represented on Fig 1c,c`. Various marker structures are shown by arrows. Chromosomes were counterstained with DAPI. Corresponding phase-contrast micrographs are shown (d1`,d2`,d3`,d4`,d5`,d6`,e1`,e2`,e3`,f1`). Arrowheads indicate centromeres. Scale bars = 10 μm for all panels except a`, where scale bar = 2 μm.
Mentions: In R-E population system, we analyzed genome composition in oocytes of 9 diploid, 13 triploid P. esculentus females with RRL genotype (including females with RLX genotype) and 5 triploid females with LLR genotype. Algorithm to identify the type of genome transmitted in oocytes of hybrid frogs is represented in S1 Material. At first, we describe the chromosomal sets in oocytes of triploid frogs with RRL genotype. We found that 11 females with RRL genotype produced only one type of oocytes with 13 bivalents corresponding to P. ridibundus bivalents (Figs 1a,a` and 2d1–d6`; S1 Movie). Combining the data on hybrid females ploidy and oocyte genome composition, we evaluated appearance of genome elimination and endoreplication events during gametogenesis. We suggest that to form typical oocytes with 13 bivalents corresponding to P. ridibundus bivalents, elimination of L genome occurred premeiotically while two remaining R genomes presumably conjugated during meiosis (Fig 3a).

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