Evolutionary rates of mammalian telomere-stability genes correlate with karyotype features and female germline expression

Pontremoli, Chiara; Forni, Diego; Cagliani, Rachele; Clerici, Mario; Sironi, Manuela

doi:10.1093/nar/gky494

Cited by 10 publications

(12 citation statements)

References 94 publications

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“…For example, human centromeric dimeric arrays might be expanding due to their more efficient recruitment of centromeric protein shown by centromeric chromatin profiling [ 49 , 196 , 200 , 203 ]. Analogous to centromeric satellites, subtelomeric satellites of different organisms show no sequence similarity and have been proposed to be subjected to telomere drive in which rapid sequence changes in the subtelomeric DNA can trigger adaptation of telomeric proteins to restore telomere homeostasis [ 305 , 306 , 307 ].…”

Section: Satellite Evolutionmentioning

confidence: 99%

Sequence, Chromatin and Evolution of Satellite DNA

Thakur

Packiaraj

Henikoff

2021

IJMS

152

116

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Satellite DNA consists of abundant tandem repeats that play important roles in cellular processes, including chromosome segregation, genome organization and chromosome end protection. Most satellite DNA repeat units are either of nucleosomal length or 5–10 bp long and occupy centromeric, pericentromeric or telomeric regions. Due to high repetitiveness, satellite DNA sequences have largely been absent from genome assemblies. Although few conserved satellite-specific sequence motifs have been identified, DNA curvature, dyad symmetries and inverted repeats are features of various satellite DNAs in several organisms. Satellite DNA sequences are either embedded in highly compact gene-poor heterochromatin or specialized chromatin that is distinct from euchromatin. Nevertheless, some satellite DNAs are transcribed into non-coding RNAs that may play important roles in satellite DNA function. Intriguingly, satellite DNAs are among the most rapidly evolving genomic elements, such that a large fraction is species-specific in most organisms. Here we describe the different classes of satellite DNA sequences, their satellite-specific chromatin features, and how these features may contribute to satellite DNA biology and evolution. We also discuss how the evolution of functional satellite DNA classes may contribute to speciation in plants and animals.

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Section: Satellite Evolutionmentioning

confidence: 99%

Sequence, Chromatin and Evolution of Satellite DNA

Thakur

Packiaraj

Henikoff

2021

IJMS

152

116

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“…Furthermore, longer telomeres may be needed to protect longer chromosomes from end denaturation and rearrangements (Pampalona, Soler, Genescà, & Tusell, 2010; Slijepcevic, 1998). Supporting the connection between TL and chromosome size, Pontremoli et al (2018) found that positive selection on genes implicated in telomere homeostasis among mammals was related to the number of chromosome arms. Given that genome size is relatively conserved among mammals (Kapusta et al, 2017), the positive selection at these genes is likely driven by chromosome size and these genes might help calibrate specific telomeres to the corresponding chromosomes.…”

Section: Discussionmentioning

confidence: 86%

Early-life telomere length covaries with life-history traits and scales with chromosome length in birds

Pepke

Ringsby

Eisenberg

2021

Preprint

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Telomeres, the short DNA sequences that protect chromosome ends, are an ancient molecular structure, which is highly conserved across most eukaryotes. Species differ in their telomere lengths, but the causes of this variation are not well understood. Here, we demonstrate that mean early-life telomere length is an evolutionary labile trait across 58 bird species (representing 35 families in 12 orders) with the greatest trait diversity found among passerines. Among these species, telomere length is significantly negatively associated with the fast-slow axis of life-history variation, suggesting that telomere length may have evolved to mediate trade-offs between physiological requirements underlying the diversity of pace-of-life strategies in birds. Curiously, within some species, larger individual chromosome size predicts longer telomere lengths on that chromosome, leading to the suggestion that telomere length also covaries with chromosome length across species. We show that longer mean chromosome length or genome size tends to be associated with longer mean early-life telomere length (measured across all chromosomes) within a phylogenetic framework constituting up to 32 bird species. Combined, our analyses generalize patterns previously found within a few species and provide potential adaptive explanations for the 10-fold variation in telomere lengths observed among birds.

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“…Using large phylogenies of mammalian orthologues (Table ), we calculated the dN/dS parameter (Kosakovsky Pond & Frost, 2005; Table ). In particular, we compared the distribution of dN/dS for this centromere gene set to the one previously calculated for genes encoding CENP‐A and proteins involved in CENP‐A deposition (10 genes; Pontremoli et al, 2018). As a comparison, genes involved in telomere homeostasis (TEL genes), which have also been involved in an intragenomic genetic conflict, as well as a set of random genes were analysed (Pontremoli et al, 2018; Figure 2; Table ).…”

Section: Resultsmentioning

confidence: 99%

“…“Textmining,” “Experiments” and “Databases” string active interaction sources were selected. Proteins are coloured according to the observed selection pattern, either described herein or in a previous work (Pontremoli et al, 2018). The percentage of sites evolving with dN/dS > 1 was obtained from the codeml M8 model.…”

Section: Resultsmentioning

confidence: 99%

Kinetochore proteins and microtubule‐destabilizing factors are fast evolving in eutherian mammals

et al. 2021

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Centromeres have central functions in chromosome segregation, but centromeric DNA and centromere‐binding proteins evolve rapidly in most eukaryotes. The selective pressure(s) underlying the fast evolution of centromere‐binding proteins are presently unknown. An attractive possibility is that selfish centromeres promote their preferential inclusion in the oocyte and centromeric proteins evolve to suppress meiotic drive (centromere drive hypothesis). We analysed the selective patterns of mammalian genes that encode kinetochore proteins and microtubule (MT)‐destabilizing factors. We show that several of these proteins evolve at the same rate or faster than proteins with a role in centromere specification. Elements of the kinetochore that bind MTs or that bridge the interaction between MTs and the centromere represented the major targets of positive selection. These data are in line with the possibility that the genetic conflict fuelled by meiotic drive extends beyond genes involved in centromere specification. However, we cannot exclude that different selective pressures underlie the rapid evolution of MT‐destabilizing factors and kinetochore components. Whatever the nature of such pressures, they must have been constant during the evolution of eutherian mammals, as we found a surprisingly good correlation in dN/dS (ratio of the rate of nonsynonymous and synonymous substitutions) across orders/clades. Finally, when phylogenetic relationships were accounted for, we found little evidence that the evolutionary rates of these genes change with testes size, a proxy for sperm competition. Our data indicate that, in analogy to centromeric proteins, kinetochore components are fast evolving in mammals. This observation may imply that centromere drive plays out at multiple levels or that these proteins adapt to lineage‐specific centromeric features.

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Evolutionary rates of mammalian telomere-stability genes correlate with karyotype features and female germline expression

Cited by 10 publications

References 94 publications

Sequence, Chromatin and Evolution of Satellite DNA

Sequence, Chromatin and Evolution of Satellite DNA

Early-life telomere length covaries with life-history traits and scales with chromosome length in birds

Kinetochore proteins and microtubule‐destabilizing factors are fast evolving in eutherian mammals

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