Extensive Amplification of Telomeric Repeats in the Karyotypically Highly Diverse African Pygmy Mice

Abstract

Telomeres are ribonucleoprotein structures protecting the physical ends of eukaryotic chromosomes. However, telomeric sequences can also occur at non-terminal regions of chromosomes, forming the so-called interstitial telomeric sequences (ITSs). Some ITSs are considered as relics of past chromosomal rearrangements and as such provide important insights into karyotype evolution. By FISH, we explored the distribution of telomeric motifs in the genome of a complex of mammalian species that has long been recognized for its extraordinary karyotypic diversity: the African pygmy mice. This survey involved 5 species, representing 10 highly diverse karyotypes with or without autosomal and sex-autosome robertsonian (Rb) fusions. The study revealed that in species with an ancestral-like karyotype (i.e., no fusions; Mus mattheyi and M. indutus), only terminal telomeres were observed, whereas in species experiencing intense chromosomal evolution (e.g., M. minutoides, M. musculoides), a large amplification of telomeric repeats was also identified in the pericentromeric region of acrocentrics and most metacentrics. We concluded that (i) the mechanism of Rb fusion in the African pygmy mice is different than the one highlighted in the house mouse; (ii) the intensity of the ITS hybridization signal could be a signature of the age of formation of the Rb fusion; (iii) the large amplification of pericentromeric telomeric sequences in acrocentrics may mediate the formation of Rb fusions, and (iv) the ITSs on the sex-autosome fusion Rb(X.1) may participate to the insulation buffer between the sexual and autosomal arms to prevent X inactivation from spreading and silencing autosomal genes and allow the independent regulation of replication timing of both segments.

X inactivation in a mammal species with three sex chromosomes

“…These results are even more interesting in M. minutoides since no blocks of C-positive heterochromatin were found near the centromeres of Rb(X.1) and Rb(X*.16) (Veyrunes et al 2004), and there is no pseudoautosomal region that could create a natural barrier preventing the spreading (the sex chromosomes being asynaptic; Britton-Davidian et al 2012). These observations support our assumption that in this species, the isolation of the X and autosomal compartments may involve other types of repetitive sequences to act as a buffer (Veyrunes et al 2004;Colomina et al 2017), or some genomic characteristics, such as a low density of LINE-1 elements, as they are suggested to act as booster elements of the X inactivation propagation (Lyon 1998;Bala Tannan et al 2014;Cotton et al 2014).…”

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

“…banding pattern (Fig 1A and 1B) [50]. During meiosis, chromosomes show highly extended centromeres ( Fig 1C and 1D), a feature that is not present in the Rb chromosomes of other mouse species, including Mus musculus domesticus [54], suggesting it is specific to the Rb translocation mechanism in pygmy mice [50,55,56]. The extended centromeres, which vary in length, do not assemble any components of the SC, neither the axial/lateral elements (AEs/ LEs) nor the transverse filaments (TFs) (S1 Fig, S2 Fig).…”

Meiotic Behavior of Achiasmate Sex Chromosomes in the African Pygmy Mouse Mus mattheyi Offers New Insights into the Evolution of Sex Chromosome Pairing and Segregation in Mammals

“…This subgenus is characterized by a great karyotypic diversity mainly due to autosomal centric fusions, but also to sex-autosome fusions. Thus, diploid numbers that range from 2 n = 16 to 2 n = 36 [ 50 ]. M. mattheyi [ 51 ] is one of the 18 species of the subgenus Nannomys , with an ancestral-like 2 n = 36 karyotype where all chromosomes are acrocentric, meaning no centric fusions between autosomes nor between sex chromosomes and autosomes [ 52 ].…”