Rapid gene content turnover on the germline-restricted chromosome in songbirds

Schlebusch, Stephen A.; Rídl, Jakub; Poignet, Manon; Ruiz-Ruano, Francisco J.; Reif, Jiří; Pajer, Petr; Pačes, Jan; Albrecht, Tomáš; Suh, Alexander; Reifová, Radka

doi:10.1038/s41467-023-40308-8

Cited by 6 publications

(4 citation statements)

References 68 publications

(109 reference statements)

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“…Interestingly, one CBR in Parascaris appears to have diverged into seven CBRs in Ascaris since the split of these species. Notably, the alternative CBRs appear to be the least conserved CBRs between the species, supporting a model that the eliminated DNA is more flexible and may be undergoing more rapid evolution (1,46,47). In sum, while the closely related Ascaris and Parascaris share many PDE features, there are notable variations in the sequences of the CBRs and their positions in the chromosomes, suggesting flexibility in the genomic location and the amount of sequence eliminated in nematode PDE.…”

Section: Resultsmentioning

confidence: 56%

End resection and telomere healing of DNA double-strand breaks during nematode programmed DNA elimination

Estrem,

Davis,

Wang

2024

Preprint

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Most DNA double-strand breaks (DSBs) are harmful to genome integrity. However, some forms of DSBs are essential to biological processes, such as meiotic recombination and V(D)J recombination. DSBs are also required for programmed DNA elimination (PDE) in ciliates and nematodes. In nematodes, the DSBs are healed with telomere addition. While telomere addition sites have been well-characterized, little is known regarding the DSBs that fragment nematode chromosomes. Here, we used embryos from the nematode Ascaris to study the timing of PDE breaks and examine the DSBs and their end processing. Using END-seq, we characterize the DSB ends and demonstrate that DNA breaks are introduced before mitosis, followed by extensive end resection. The resection profile is unique for each break site, and the resection generates 3' overhangs before the addition of telomeres. Interestingly, telomere healing occurs much more frequently on retained DSB ends than on eliminated ends. This biased repair of the DSB ends in Ascaris may be due to the sequestration of the eliminated DNA into micronuclei, preventing their ends from telomere healing. Additional DNA breaks occur within the eliminated DNA in both Ascaris and Parascaris, ensuring chromosomal breakage and providing a fail-safe mechanism for nematode PDE.

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Section: Resultsmentioning

confidence: 56%

End resection and telomere healing of DNA double-strand breaks during nematode programmed DNA elimination

Estrem,

Davis,

Wang

2024

Preprint

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“…For example, nearly half of the GRC of the common nightingale consists of a large, albeit fragmented, segment homologous to the undivided segment of A-chromosome 2. This genetic material has not been identified in the western nightingale at all (Schlebusch et al, 2023).…”

Section: Evolution Of the Grcmentioning

confidence: 83%

“…What does GRC contain that makes it an obligate element of the germline genome of all songbirds? At the time of writing this article, the results of genomic analysis of GRC have been published for only four species of songbirds: the zebra finch (Kinsella et al, 2019), two species of nightingales: western, Luscinia megarhynchos and eastern, L. luscinia (Schlebusch et al, 2023), and the Eurasian blue tit, Cyanistes caeruleus (Mueller et al, 2023).…”

Section: Genetic Content Of Grcmentioning

confidence: 99%

Germline-restricted chromosomes of the songbirds

Borodin

2023

Vestn. VOGiS

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Germline-restricted chromosomes (GRCs) are present in the genomes of germline cells and absent from somatic cells. A GRC is found in all species of the songbirds (Passeri) and in none of the other bird orders studied to date. This indicates that GRC originated in the common ancestor of the songbirds. The germline-restricted chromosome is permanently absent from somatic cells of the songbird, while female germline cells usually contain two copies of GRC and male ones have one copy. In females, GRCs undergo synapsis and restricted recombination in their terminal regions during meiotic prophase. In males, it is almost always eliminated from spermatocytes. Thus, GRC is inherited almost exclusively through the maternal lineage. The germline-restricted chromosome is a necessary genomic element in the germline cells of songbirds. To date, the GRC genetic composition has been studied in four species only. Some GRC genes are actively expressed in female and male gonads, controlling the development of germline cells and synthesis of the proteins involved in the organization of meiotic chromosomes. Songbird species vary in GRC size and genetic composition. The GRC of each bird species consists of amplified and modified copies of genes from the basic genome of that species. The level of homology between GRCs of different species is relatively low, indicating a high rate of genetic evolution of this chromosome. Transmission through the maternal lineage and suppression of the recombination contribute significantly to the accelerated evolution of GRCs. One may suggest that the rapid coordinated evolution between the GRC genes and the genes of the basic genome in the songbirds might be responsible for the explosive speciation and adaptive radiation of this most species-rich and diverse infraorder of birds.

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“…The relaxed constraint for the eliminated DNA supports a hypothesis that eliminated regions can serve as a reservoir where novel genes are better tolerated, and their divergence by rapid mutation promotes the speed of gene selection and evolution. 2,30,31…”

Section: Pde Breaks the Parascaris Germline Chromosome And Silences G...mentioning

confidence: 99%

Chromosome fusion and programmed DNA elimination shape karyotypes of parasitic nematodes

Simmons,

Estrem,

Zagoskin

et al. 2023

Preprint

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A growing list of metazoans undergo programmed DNA elimination (PDE), where a significant amount of DNA is selectively lost from the somatic genome during development. In some nematodes, PDE leads to the removal and remodeling of the ends of all germline chromosomes. In several species, PDE also generates internal breaks that lead to sequence loss and an increased number of somatic chromosomes. The biological significance of these karyotype changes associated with PDE and the origin and evolution of nematode PDE remain largely unknown. Here, we assembled the single germline chromosome of the horse parasiteParascaris univalensand compared the karyotypes, chromosomal gene organization, and PDE features among ascarid nematodes. We show that PDE inParascarisconverts an XX/XY sex-determination system in the germline into an XX/XO system in the somatic cells. Comparisons ofAscaris, Parascaris,andBaylisascarisascarid chromosomes suggest that PDE existed in the ancestor of these parasites, and their current distinct germline karyotypes were derived from fusion events of smaller ancestral chromosomes. The DNA breaks involved in PDE resolve these fused germline chromosomes into their pre-fusion karyotypes, leading to alterations in genome architecture and gene expression in the somatic cells. Cytological and genomic analyses further suggest that satellite DNA and the heterochromatic chromosome arms play a dynamic role in theParascarisgermline chromosome during meiosis. Overall, our results show that chromosome fusion and PDE have been harnessed in these ascarids to sculpt their karyotypes, altering the genome organization and serving specific functions in the germline and somatic cells.

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Rapid gene content turnover on the germline-restricted chromosome in songbirds

Cited by 6 publications

References 68 publications

End resection and telomere healing of DNA double-strand breaks during nematode programmed DNA elimination

End resection and telomere healing of DNA double-strand breaks during nematode programmed DNA elimination

Germline-restricted chromosomes of the songbirds

Chromosome fusion and programmed DNA elimination shape karyotypes of parasitic nematodes

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