Mendelian nightmares: the germline-restricted chromosome of songbirds

Borodin, Pavel M.; Chen, Augustin; Forstmeier, Wolfgang; Fouché, Simone; Malinovskaya, Lyubov P.; Pei, Yifan; Reifová, Radka; Ruiz‐Ruano, Francisco J.; Schlebusch, Stephen A; Sotelo-Muñoz, Manuelita; Torgasheva, Anna A.; Vontzou, Niki; Suh, Alexander

doi:10.1007/s10577-022-09688-3

Cited by 15 publications

(24 citation statements)

References 62 publications

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“…Another factor that may contribute to heritable variation is the presence of the germline-restricted chromosome (GRC) in female birds (Torgasheva et al . 2019; Borodin et al . 2022).…”

Section: Discussionmentioning

confidence: 99%

“…Another factor that may contribute to heritable variation is the presence of the germline-restricted chromosome (GRC) in female birds (Torgasheva et al 2019;Borodin et al 2022). This large chromosome was discovered in the late 1990s, is likely present in all passerines, can comprise around 10% of the genome, but is not present in somatic cells (Pigozzi and Solari 1998;Warren et al 2010).…”

Section: Variation In Crossover Count and Intra-chromosomal Shufflingmentioning

confidence: 99%

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The genetic architecture of recombination rates is polygenic and differs between the sexes in wild house sparrows (Passer domesticus)

McAuley

Servin

Peters

et al. 2023

Preprint

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Meiotic recombination is a fundamental feature of sex and an important driver of diversity in eukaryotic genomes. It ensures proper chromosome disjunction, increases responses to selection, and prevents mutation accumulation; however, it is also mutagenic and can break up favourable haplotypes built up by selection. This cost/benefit dynamic is likely to vary depending on mechanistic and evolutionary contexts, and indeed, recombination rates show huge variation within and between chromosomes, individuals, sexes, populations and species. Identifying the genetic architecture of recombination rates is a key step in understanding the causes and consequences of this variation. Here, we investigate broad-scale recombination landscapes and individual crossover (CO) rates in a wild population of house sparrows (Passer domesticus). We integrated pedigree data with ~61K SNPs to identify autosomal crossover counts (ACC) and intra-chromosomal allelic shuffling (r¯intra) in 2,802 gametes. Females had longer autosomal genetic maps (2,558.1cM vs 2,069.6cM), 1.37 times higher ACC, and 1.46 times higherr¯intrathan males. ACC was heritable in females (h2= 0.23) but not in males, indicating genetic independence of male and female crossover rates. Conversely,r¯intrawas heritable in males (h2= 0.07), but not in females. Neither measure was associated with age or common environment effects. Genome-wide association studies of female ACC and maler¯intrafound no loci explaining more than XX% of additive genetic variation, but ~2% of SNPs had non-zero effects on female ACC. Our results suggest that recombination rates in house sparrows are polygenic and driven by many small-effect loci that may act in cis (e.g. local recombination hotspots) or trans (global recombination modifiers). This work shows that recombination rates have evolutionary potential in wild birds, and provides a foundation for understanding associations between recombination rates, genome architecture, and individual fitness.

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“…Another factor that may contribute to heritable variation is the presence of the germline-restricted chromosome (GRC) in female birds (Torgasheva et al . 2019; Borodin et al . 2022).…”

Section: Discussionmentioning

confidence: 99%

Section: Variation In Crossover Count and Intra-chromosomal Shufflingmentioning

confidence: 99%

The genetic architecture of recombination rates is polygenic and differs between the sexes in wild house sparrows (Passer domesticus)

McAuley

Servin

Peters

et al. 2023

Preprint

View full text Add to dashboard Cite

show abstract

“…However, the mechanisms and machinery associated with the DNA breaks in metazoans remain largely unknown. More general descriptions and discussions on PDE in diverse organisms have been summarized in recent reviews [40,43,45,[49][50][51][52].…”

Section: Overview Of Pdementioning

confidence: 99%

Programmed DNA elimination in the parasitic nematode Ascaris

Estrem

Wang

2023

PLoS Pathog

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In most organisms, the whole genome is maintained throughout the life span. However, exceptions occur in some species where the genome is reduced during development through a process known as programmed DNA elimination (PDE). In the human and pig parasite Ascaris, PDE occurs during the 4 to 16 cell stages of embryogenesis, when germline chromosomes are fragmented and specific DNA sequences are reproducibly lost in all somatic cells. PDE was identified in Ascaris over 120 years ago, but little was known about its molecular details until recently. Genome sequencing revealed that approximately 1,000 germline-expressed genes are eliminated in Ascaris, suggesting PDE is a gene silencing mechanism. All germline chromosome ends are removed and remodeled during PDE. In addition, PDE increases the number of chromosomes in the somatic genome by splitting many germline chromosomes. Comparative genomics indicates that these germline chromosomes arose from fusion events. PDE separates these chromosomes at the fusion sites. These observations indicate that PDE plays a role in chromosome karyotype and evolution. Furthermore, comparative analysis of PDE in other parasitic and free-living nematodes illustrates conserved features of PDE, suggesting it has important biological significance. We summarize what is known about PDE in Ascaris and its relatives. We also discuss other potential functions, mechanisms, and the evolution of PDE in these parasites of humans and animals of veterinary importance.

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“…PDE was first discovered in the horse parasite Parascaris in the 1880s by Theodor Boveri. 10 It has since been found in single-cell ciliates, 11,12 a variety of multicellular organisms across animal phyla, 5,[13][14][15][16] and in plants. 17,18 Initial discoveries of PDE were largely dependent on careful cytological observations, and thus early models for PDE tend to have large genomes and/or discard a large amount of DNA.…”

Section: Introductionmentioning

confidence: 99%

“…19 Genomics has been used to characterize metazoan PDE in depth, including the nature of eliminated sequences [20][21][22][23][24][25][26][27] and DNA breaks, [20][21][22] as well as the evolution of PDE. 15,16,28 A common theme emerging from these recent genomics studies is the removal of both germline-expressed genes and repetitive sequences during PDE. [5][6][7][8][9] This suggests that one function of PDE in metazoa is to permanently silence certain germline sequences potentially harmful to somatic cells.…”

mentioning

confidence: 99%

The Nematode Oscheius tipulae as A Genetic Model for Programmed DNA Elimination

Dockendorff

Estrem

Reed

et al. 2022

Preprint

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Programmed DNA elimination (PDE) is a notable exception to the paradigm of genome integrity. In metazoa, PDE often occurs during early embryogenesis, coincident with germline to somatic cell differentiation. During PDE, portions of genomic DNA are lost, resulting in reduced somatic genomes. Recent studies have described the sequences lost and chromosome behavior in metazoa. However, a system for studying the mechanisms and consequences of PDE in metazoa is lacking. Here, we established a functional and genetic model for PDE in the free-living nematode Oscheius tipulae, a member of the Rhabditidae family, which includes Caenorhabditis elegans. O. tipulae was recently suggested to eliminate DNA. Using staged embryos, we show that O. tipulae PDE occurs during embryogenesis at the 2-16 cell stages, similar to the human/pig parasitic nematode Ascaris. We identified a conserved motif, named Sequence For Elimination (SFE), for all 12 break sites on the six chromosomes at the junction of retained and eliminated DNA. SFE mutants exhibit a "fail-to-eliminate" phenotype only at the modified sites. END-seq revealed that breaks can occur at multiple positions within the SFE, with extensive end resection followed by telomere addition to both retained and eliminated ends. We identified through END-seq in the wild-type embryos, genome sequencing of SFE mutants, and comparative genomics of 23 wild isolates a large number of functional SFEs at the chromosome ends. We suggest these alternative SFEs provide flexibility in the sequences eliminated and a fail-safe mechanism for PDE. These studies establish O. tipulae as a new, attractive model to study the mechanisms and consequences of PDE in a metazoan.

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Mendelian nightmares: the germline-restricted chromosome of songbirds

Cited by 15 publications

References 62 publications

The genetic architecture of recombination rates is polygenic and differs between the sexes in wild house sparrows (Passer domesticus)

The genetic architecture of recombination rates is polygenic and differs between the sexes in wild house sparrows (Passer domesticus)

Programmed DNA elimination in the parasitic nematode Ascaris

The Nematode Oscheius tipulae as A Genetic Model for Programmed DNA Elimination

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