Meiotic behavior of a complex hexavalent in heterozygous mice for Robertsonian translocations: insights for synapsis dynamics

Ribagorda, Marta; Berríos, Soledad; Solano, Emanuela; Ayarza, Eliana; Martín‐Ruíz, Marta; Gil-Fernández, Ana; Parra, María Teresa; Viera, Alberto; Rufas, Julio S.; Capanna, Ernesto; Castiglia, Riccardo; Fernández-Donoso, Raúl; Page, Jesús

doi:10.1007/s00412-019-00695-8

Cited by 18 publications

(24 citation statements)

References 77 publications

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“…Structural constrains may influence these processes. The length of the neo-PAR, the extreme size difference of the non-homologous segments of the X and Y chromosomes and the fact that all chromosome ends remain attached to the nuclear envelope force the X chromosome to bend significantly (see Fig 2F), which may be the cause of the synapsis delay, as has been reported for other chromosomal rearrangements [70,71]. Furthermore, other type of synapsis impairments have been described in other mammalian species with neo-sex chromosomes (e.g., heterologous synapsis, asynapsis, desynapsis) [20,[72][73][74].…”

Section: The Neo-par In M Minutoides Already Displays Some But Not mentioning

confidence: 69%

Meiosis reveals the early steps in the evolution of a neo-XY sex chromosome pair in the African pygmy mouse Mus minutoides

et al. 2020

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Sex chromosomes of eutherian mammals are highly different in size and gene content, and share only a small region of homology (pseudoautosomal region, PAR). They are thought to have evolved through an addition-attrition cycle involving the addition of autosomal segments to sex chromosomes and their subsequent differentiation. The events that drive this process are difficult to investigate because sex chromosomes in almost all mammals are at a very advanced stage of differentiation. Here, we have taken advantage of a recent translocation of an autosome to both sex chromosomes in the African pygmy mouse Mus minutoides, which has restored a large segment of homology (neo-PAR). By studying meiotic sex chromosome behavior and identifying fully sex-linked genetic markers in the neo-PAR, we demonstrate that this region shows unequivocal signs of early sex-differentiation. First, synapsis and resolution of DNA damage intermediates are delayed in the neo-PAR during meiosis. Second, recombination is suppressed or largely reduced in a large portion of the neo-PAR. However, the inactivation process that characterizes sex chromosomes during meiosis does not extend to this region. Finally, the sex chromosomes show a dual mechanism of association at metaphase-I that involves the formation of a chiasma in the neo-PAR and the preservation of an ancestral achiasmate mode of association in the non-homologous segments. We show that the study of meiosis is crucial to apprehend the onset of sex chromosome differentiation, as it introduces structural and functional constrains to sex chromosome evolution. Synapsis and DNA repair dynamics are the first processes affected in the incipient differentiation of X and Y chromosomes, and they may be involved in accelerating their evolution. This provides one of the very first reports of early steps in neo-sex chromosome differentiation in mammals, and for the first time a cellular framework for the addition-attrition model of sex chromosome evolution.

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Section: The Neo-par In M Minutoides Already Displays Some But Not mentioning

confidence: 69%

Meiosis reveals the early steps in the evolution of a neo-XY sex chromosome pair in the African pygmy mouse Mus minutoides

et al. 2020

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“…As a result, the nuclear architecture in meiotic prophase I is determined by the SC structure and dynamics, types of chromosomes (single-armed or bi-armed), their length, the heterochromatin amount, the specificity of centromeric regions, the “chromosome–nuclear envelop” interactions, the ability to form chromocenters and nucleoli, and sex chromosome organization and behavior [ 134 ]. It should be emphasized that if the parental genomes differ significantly, then complex chromosome compounds are formed in hybrid and mutant meiotic nuclei (for example, [ 21 , 135 , 136 , 137 ]), and the processes of repair, recombination, and meiotic silencing are disrupted (for example, [ 24 , 138 , 139 , 140 ]), which can cause an imbalance in the nuclear architecture.…”

Section: Discussionmentioning

confidence: 99%

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

Matveevsky

Tretiakov

Kashintsova

et al. 2020

IJMS

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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 (Ellobius tancrei × E. tancrei) and interspecific (Ellobius talpinus × E. tancrei) 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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“…Because of rearrangements 32 , these non-terminal regions may lack homology, suggesting extensive heterosynapsis in this anuran species. This type of synaptic adjustment is widely found in mammals [41][42][43] , as it prevents the dangerous effects of transcriptional inactivation and of the action of www.nature.com/scientificreports/ meiotic checkpoint proteins 44 . Heterosinapses between centromeres, as observed in L. pentadactylus (Fig.…”

Section: Discussionmentioning

confidence: 99%

“…In contrast, γH2AX in L. pentadactylus persists until diplotene, albeit in reduced quantities, on all chromatins of the ring and the bivalents. The fact, that γH2AX is expressed in asynaptic regions of meiotic multiples 43,52 , may be due to the delay associated with synapsis and in DSBs repair, as they recruit silencing factors such as ATR for these regions 22 . Proto-XY has been identified in meiotic rings of L. pentadactylus 34 .…”

Section: Discussionmentioning

confidence: 99%

Meiotic analyses show adaptations to maintenance of fertility in X1Y1X2Y2X3Y3X4Y4X5Y5 system of amazon frog Leptodactylus pentadactylus (Laurenti, 1768)

Noronha

Almeida

Costa

et al. 2020

Sci Rep

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Heterozygous chromosomal rearrangements can result in failures during the meiotic cycle and the apoptosis of germline, making carrier individuals infertile. The Amazon frog Leptodactylus pentadactylus has a meiotic multivalent, composed of 12 sex chromosomes. The mechanisms by which this multi-chromosome system maintains fertility in males of this species remain undetermined. In this study we investigated the meiotic behavior of this multivalent to understand how synapse, recombination and epigenetic modifications contribute to maintaining fertility and chromosomal sexual determination in this species. Our sample had 2n = 22, with a ring formed by ten chromosomes in meiosis, indicating a new system of sex determination for this species (X1Y1X2Y2X3Y3X4Y4X5Y5). Synapsis occurs in the homologous terminal portion of the chromosomes, while part of the heterologous interstitial regions performed synaptic adjustment. The multivalent center remains asynaptic until the end of pachytene, with interlocks, gaps and rich-chromatin in histone H2A phosphorylation at serine 139 (γH2AX), suggesting transcriptional silence. In late pachytene, paired regions show repair of double strand-breaks (DSBs) with RAD51 homolog 1 (Rad51). These findings suggest that Rad51 persistence creates positive feedback at the pachytene checkpoint, allowing meiosis I to progress normally. Additionally, histone H3 trimethylation at lysine 27 in the pericentromeric heterochromatin of this anuran can suppress recombination in this region, preventing failed chromosomal segregation. Taken together, these results indicate that these meiotic adaptations are required for maintenance of fertility in L. pentadactylus.

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Meiotic behavior of a complex hexavalent in heterozygous mice for Robertsonian translocations: insights for synapsis dynamics

Cited by 18 publications

References 77 publications

Meiosis reveals the early steps in the evolution of a neo-XY sex chromosome pair in the African pygmy mouse Mus minutoides

Meiosis reveals the early steps in the evolution of a neo-XY sex chromosome pair in the African pygmy mouse Mus minutoides

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

Meiotic analyses show adaptations to maintenance of fertility in X1Y1X2Y2X3Y3X4Y4X5Y5 system of amazon frog Leptodactylus pentadactylus (Laurenti, 1768)

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