Meiotic Nuclear Architecture in Distinct Mole Vole Hybrids with Robertsonian Translocations: Chromosome Chains, Stretched Centromeres, and Distorted Recombination

Genome functioning in hybrids faces inconsistency. This mismatch is manifested clearly in meiosis during chromosome synapsis and recombination. Species with chromosomal variability can be a model for exploring genomic battles with high visibility due to the use of advanced immunocytochemical methods...

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Main Authors: Sergey Matveevsky, Artemii Tretiakov, Anna Kashintsova, Irina Bakloushinskaya, Oxana Kolomiets
Format: Article
Language:English
Published: MDPI AG 2020-10-01
Series:International Journal of Molecular Sciences
Subjects:
Online Access:https://www.mdpi.com/1422-0067/21/20/7630
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author Sergey Matveevsky
Artemii Tretiakov
Anna Kashintsova
Irina Bakloushinskaya
Oxana Kolomiets
author_facet Sergey Matveevsky
Artemii Tretiakov
Anna Kashintsova
Irina Bakloushinskaya
Oxana Kolomiets
author_sort Sergey Matveevsky
collection DOAJ
description Genome functioning in hybrids faces inconsistency. This mismatch is manifested clearly in meiosis during chromosome synapsis and recombination. Species with chromosomal variability can be a model for exploring genomic battles with high visibility due to the use of advanced immunocytochemical methods. We studied synaptonemal complexes (SC) and prophase I processes in 44-chromosome intraspecific (<i>Ellobius tancrei</i> × <i>E. tancrei</i>) and interspecific (<i>Ellobius talpinus</i> × <i>E. tancrei</i>) hybrid mole voles heterozygous for 10 Robertsonian translocations. The same pachytene failures were found for both types of hybrids. In the intraspecific hybrid, the chains were visible in the pachytene stage, then 10 closed SC trivalents formed in the late pachytene and diplotene stage. In the interspecific hybrid, as a rule, SC trivalents composed the SC chains and rarely could form closed configurations. Metacentrics involved with SC trivalents had stretched centromeres in interspecific hybrids. Linkage between neighboring SC trivalents was maintained by stretched centromeric regions of acrocentrics. This centromeric plasticity in structure and dynamics of SC trivalents was found for the first time. We assume that stretched centromeres were a marker of altered nuclear architecture in heterozygotes due to differences in the ancestral chromosomal territories of the parental species. Restructuring of the intranuclear organization and meiotic disturbances can contribute to the sterility of interspecific hybrids, and lead to the reproductive isolation of studied species.
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spelling doaj.art-398bc04e9dee4e078808fb30191f43fd2023-11-20T17:13:03ZengMDPI AGInternational Journal of Molecular Sciences1661-65961422-00672020-10-012120763010.3390/ijms21207630Meiotic Nuclear Architecture in Distinct Mole Vole Hybrids with Robertsonian Translocations: Chromosome Chains, Stretched Centromeres, and Distorted RecombinationSergey Matveevsky0Artemii Tretiakov1Anna Kashintsova2Irina Bakloushinskaya3Oxana Kolomiets4Laboratory of Cytogenetics, Vavilov Institute of General Genetics, Russian Academy of Sciences, 119991 Moscow, RussiaLaboratory of Cytogenetics, Vavilov Institute of General Genetics, Russian Academy of Sciences, 119991 Moscow, RussiaLaboratory of Cytogenetics, Vavilov Institute of General Genetics, Russian Academy of Sciences, 119991 Moscow, RussiaLaboratory of Genome Evolution and Mechanisms of Speciation, Koltzov Institute of Developmental Biology, Russian Academy of Sciences, 119334 Moscow, RussiaLaboratory of Cytogenetics, Vavilov Institute of General Genetics, Russian Academy of Sciences, 119991 Moscow, RussiaGenome functioning in hybrids faces inconsistency. This mismatch is manifested clearly in meiosis during chromosome synapsis and recombination. Species with chromosomal variability can be a model for exploring genomic battles with high visibility due to the use of advanced immunocytochemical methods. We studied synaptonemal complexes (SC) and prophase I processes in 44-chromosome intraspecific (<i>Ellobius tancrei</i> × <i>E. tancrei</i>) and interspecific (<i>Ellobius talpinus</i> × <i>E. tancrei</i>) hybrid mole voles heterozygous for 10 Robertsonian translocations. The same pachytene failures were found for both types of hybrids. In the intraspecific hybrid, the chains were visible in the pachytene stage, then 10 closed SC trivalents formed in the late pachytene and diplotene stage. In the interspecific hybrid, as a rule, SC trivalents composed the SC chains and rarely could form closed configurations. Metacentrics involved with SC trivalents had stretched centromeres in interspecific hybrids. Linkage between neighboring SC trivalents was maintained by stretched centromeric regions of acrocentrics. This centromeric plasticity in structure and dynamics of SC trivalents was found for the first time. We assume that stretched centromeres were a marker of altered nuclear architecture in heterozygotes due to differences in the ancestral chromosomal territories of the parental species. Restructuring of the intranuclear organization and meiotic disturbances can contribute to the sterility of interspecific hybrids, and lead to the reproductive isolation of studied species.https://www.mdpi.com/1422-0067/21/20/7630nuclear architecturestretched centromeresynaptonemal complexchromatinmeiosishybrid sterility
spellingShingle Sergey Matveevsky
Artemii Tretiakov
Anna Kashintsova
Irina Bakloushinskaya
Oxana Kolomiets
Meiotic Nuclear Architecture in Distinct Mole Vole Hybrids with Robertsonian Translocations: Chromosome Chains, Stretched Centromeres, and Distorted Recombination
International Journal of Molecular Sciences
nuclear architecture
stretched centromere
synaptonemal complex
chromatin
meiosis
hybrid sterility
title Meiotic Nuclear Architecture in Distinct Mole Vole Hybrids with Robertsonian Translocations: Chromosome Chains, Stretched Centromeres, and Distorted Recombination
title_full Meiotic Nuclear Architecture in Distinct Mole Vole Hybrids with Robertsonian Translocations: Chromosome Chains, Stretched Centromeres, and Distorted Recombination
title_fullStr Meiotic Nuclear Architecture in Distinct Mole Vole Hybrids with Robertsonian Translocations: Chromosome Chains, Stretched Centromeres, and Distorted Recombination
title_full_unstemmed Meiotic Nuclear Architecture in Distinct Mole Vole Hybrids with Robertsonian Translocations: Chromosome Chains, Stretched Centromeres, and Distorted Recombination
title_short Meiotic Nuclear Architecture in Distinct Mole Vole Hybrids with Robertsonian Translocations: Chromosome Chains, Stretched Centromeres, and Distorted Recombination
title_sort meiotic nuclear architecture in distinct mole vole hybrids with robertsonian translocations chromosome chains stretched centromeres and distorted recombination
topic nuclear architecture
stretched centromere
synaptonemal complex
chromatin
meiosis
hybrid sterility
url https://www.mdpi.com/1422-0067/21/20/7630
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