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Asymmetrical canina meiosis is accompanied by the expansion of a pericentromeric satellite in non-recombining univalent chromosomes in the genus Rosa

BACKGROUND AND AIMS: Despite their abundant odd-ploidy (2n = 5x = 35), dogroses (Rosa sect. Caninae) are capable of sexual reproduction due to their unique meiosis. During canina meiosis, two sets of chromosomes form bivalents and are transmitted by male and female gametes, whereas the remaining chr...

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Autores principales: Lunerová, Jana, Herklotz, Veit, Laudien, Melanie, Vozárová, Radka, Groth, Marco, Kovařík, Aleš, Ritz, Christiane M
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Oxford University Press 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7262465/
https://www.ncbi.nlm.nih.gov/pubmed/32095807
http://dx.doi.org/10.1093/aob/mcaa028
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author Lunerová, Jana
Herklotz, Veit
Laudien, Melanie
Vozárová, Radka
Groth, Marco
Kovařík, Aleš
Ritz, Christiane M
author_facet Lunerová, Jana
Herklotz, Veit
Laudien, Melanie
Vozárová, Radka
Groth, Marco
Kovařík, Aleš
Ritz, Christiane M
author_sort Lunerová, Jana
collection PubMed
description BACKGROUND AND AIMS: Despite their abundant odd-ploidy (2n = 5x = 35), dogroses (Rosa sect. Caninae) are capable of sexual reproduction due to their unique meiosis. During canina meiosis, two sets of chromosomes form bivalents and are transmitted by male and female gametes, whereas the remaining chromosomes form univalents and are exclusively transmitted by the egg cells. Thus, the evolution of chromosomes is expected to be driven by their behaviour during meiosis. METHODS: To gain insight into differential chromosome evolution, fluorescence in situ hybridization was conducted for mitotic and meiotic chromosomes in four dogroses (two subsections) using satellite and ribosomal DNA probes. By exploiting high-throughput sequencing data, we determined the abundance and diversity of the satellite repeats in the genus Rosa by analysing 20 pentaploid, tetraploid and diploid species in total. KEY RESULTS: A pericentromeric satellite repeat, CANR4, was found in all members of the genus Rosa, including the basal subgenera Hulthemia and Hesperhodos. The satellite was distributed across multiple chromosomes (5–20 sites per mitotic cell), and its genomic abundance was higher in pentaploid dogroses (2.3 %) than in non-dogrose species (1.3 %). In dogrose meiosis, univalent chromosomes were markedly enriched in CANR4 repeats based on both the number and the intensity of the signals compared to bivalent-forming chromosomes. Single-nucleotide polymorphisms and cluster analysis revealed high intragenomic homogeneity of the satellite in dogrose genomes. CONCLUSIONS: The CANR4 satellite arose early in the evolution of the genus Rosa. Its high content and extraordinary homogeneity in dogrose genomes is explained by its recent amplification in non-recombining chromosomes. We hypothesize that satellite DNA expansion may contribute to the divergence of univalent chromosomes in Rosa species with non-symmetrical meiosis.
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spelling pubmed-72624652020-06-04 Asymmetrical canina meiosis is accompanied by the expansion of a pericentromeric satellite in non-recombining univalent chromosomes in the genus Rosa Lunerová, Jana Herklotz, Veit Laudien, Melanie Vozárová, Radka Groth, Marco Kovařík, Aleš Ritz, Christiane M Ann Bot Original Articles BACKGROUND AND AIMS: Despite their abundant odd-ploidy (2n = 5x = 35), dogroses (Rosa sect. Caninae) are capable of sexual reproduction due to their unique meiosis. During canina meiosis, two sets of chromosomes form bivalents and are transmitted by male and female gametes, whereas the remaining chromosomes form univalents and are exclusively transmitted by the egg cells. Thus, the evolution of chromosomes is expected to be driven by their behaviour during meiosis. METHODS: To gain insight into differential chromosome evolution, fluorescence in situ hybridization was conducted for mitotic and meiotic chromosomes in four dogroses (two subsections) using satellite and ribosomal DNA probes. By exploiting high-throughput sequencing data, we determined the abundance and diversity of the satellite repeats in the genus Rosa by analysing 20 pentaploid, tetraploid and diploid species in total. KEY RESULTS: A pericentromeric satellite repeat, CANR4, was found in all members of the genus Rosa, including the basal subgenera Hulthemia and Hesperhodos. The satellite was distributed across multiple chromosomes (5–20 sites per mitotic cell), and its genomic abundance was higher in pentaploid dogroses (2.3 %) than in non-dogrose species (1.3 %). In dogrose meiosis, univalent chromosomes were markedly enriched in CANR4 repeats based on both the number and the intensity of the signals compared to bivalent-forming chromosomes. Single-nucleotide polymorphisms and cluster analysis revealed high intragenomic homogeneity of the satellite in dogrose genomes. CONCLUSIONS: The CANR4 satellite arose early in the evolution of the genus Rosa. Its high content and extraordinary homogeneity in dogrose genomes is explained by its recent amplification in non-recombining chromosomes. We hypothesize that satellite DNA expansion may contribute to the divergence of univalent chromosomes in Rosa species with non-symmetrical meiosis. Oxford University Press 2020-06 2020-02-25 /pmc/articles/PMC7262465/ /pubmed/32095807 http://dx.doi.org/10.1093/aob/mcaa028 Text en © The Author(s) 2020. Published by Oxford University Press on behalf of the Annals of Botany Company. http://creativecommons.org/licenses/by/4.0/ This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted reuse, distribution, and reproduction in any medium, provided the original work is properly cited.
spellingShingle Original Articles
Lunerová, Jana
Herklotz, Veit
Laudien, Melanie
Vozárová, Radka
Groth, Marco
Kovařík, Aleš
Ritz, Christiane M
Asymmetrical canina meiosis is accompanied by the expansion of a pericentromeric satellite in non-recombining univalent chromosomes in the genus Rosa
title Asymmetrical canina meiosis is accompanied by the expansion of a pericentromeric satellite in non-recombining univalent chromosomes in the genus Rosa
title_full Asymmetrical canina meiosis is accompanied by the expansion of a pericentromeric satellite in non-recombining univalent chromosomes in the genus Rosa
title_fullStr Asymmetrical canina meiosis is accompanied by the expansion of a pericentromeric satellite in non-recombining univalent chromosomes in the genus Rosa
title_full_unstemmed Asymmetrical canina meiosis is accompanied by the expansion of a pericentromeric satellite in non-recombining univalent chromosomes in the genus Rosa
title_short Asymmetrical canina meiosis is accompanied by the expansion of a pericentromeric satellite in non-recombining univalent chromosomes in the genus Rosa
title_sort asymmetrical canina meiosis is accompanied by the expansion of a pericentromeric satellite in non-recombining univalent chromosomes in the genus rosa
topic Original Articles
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7262465/
https://www.ncbi.nlm.nih.gov/pubmed/32095807
http://dx.doi.org/10.1093/aob/mcaa028
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