Germline-restricted chromosome shows remarkable variation in size among closely related passerine species

Sotelo-Muñoz, Manuelita; Poignet, Manon; Albrecht, Tomáš; Kauzál, Ondřej; Dedukh, Dmitrij; Schlebusch, Stephen A; Janko, Karel; Reifová, Radka

doi:10.1007/s00412-022-00771-6

Cited by 8 publications

(11 citation statements)

References 36 publications

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“…However, some micro-GRCs were much smaller than the smallest microchromosomes of the basic set that can be inferred from the size of the chromatin cloud labeled by anticentromere and H3K9me2/3 antibodies. This variation and the lack of phylogenetic clustering by size confirm the highly dynamic nature of GRCs [Kinsella et al, 2019;Sotelo-Muñoz et al, 2022]. It was shown that GRCs of different species contain different multiply repeated sequences, which probably can be accumulated and/or be lost rather quickly [Torgasheva et al, 2019].…”

Section: Discussionmentioning

confidence: 80%

“…It is unclear if this feature is related to the different properties of GRCs in different species (its genetic content, the degree of heterochromatinization) or the intercellular and interindividual variation in the effectiveness of cohesin loading and SC polymerization since for most birds studied to date, only one sample was analyzed. The interindividual variation in GRC appearance was observed in pachytene spermatocytes of the great tit [Torgasheva et al, 2021a] and several species of the genus Lonchura [Sotelo-Muñoz et al, 2022]. The intense chromatin labeling with antibodies to centromere proteins and H3K9-modified histone allowed us to distinguish between GRC and accidental autosomal univalents.…”

Section: Discussionmentioning

confidence: 97%

“…Analysis of pachytene chromosomes led to the discovery of the germline-restricted chromosome (GRC) [Pigozzi and Solari, 1998]. The GRC was present in germline cells and absent in somatic cells in all 22 species of passerine birds examined so far [Torgasheva et al, 2019;Poignet et al, 2021;Sotelo-Muñoz et al, 2022]. It has not been found in any non-passerine bird [Torgasheva et al, 2019].…”

Section: Introductionmentioning

confidence: 99%

“…The GRC univalents in male pachytene cells are always surrounded by dense chromatin clouds heavily labeled by anticentromere antibodies. Among the Passeriformes, the GRC varies in size and morphology [Pigozzi and Solari, 1998;Torgasheva et al, 2019Torgasheva et al, , 2021aMalinovskaya et al, 2020;Sotelo-Muñoz et al, 2022].…”

Section: Introductionmentioning

confidence: 99%

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Germline-Restricted Chromosomes and Autosomal Variants Revealed by Pachytene Karyotyping of 17 Avian Species

Malinovskaya

Slobodchikova

Grishko

et al. 2022

Cytogenet Genome Res

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Karyotypes of less than 10% of bird species are known. Using immunolocalization of the synaptonemal complex, the core structure of meiotic chromosomes at the pachytene stage, and centromere proteins, we describe male pachytene karyotypes of 17 species of birds. This method enables higher resolution than the conventional analyses of metaphase chromosomes. We provide the first descriptions of the karyotypes of 3 species (rook, Blyth’s reed warbler, and European pied flycatcher), correct the published data on the karyotypes of 10 species, and confirm them for 4 species. All passerine species examined have highly conservative karyotypes, 2n = 80–82 with 7 pairs of macrochromosomes (including the ZZ sex chromosome pair which was not unambiguously distinguished from other macrochromosomes in most species) and 33–34 pairs of microchromosomes. In all of them, but not in the common cuckoo, we revealed single copies of the germline-restricted chromosomes varying in size and morphology even between closely related species. This indicates a fast evolution of this additional chromosome. The interspecies differences concern the sizes of the macrochromosomes, morphology of the microchromosomes, and sizes of the centromeres. The pachytene cells of the gouldian finch, brambling, and common linnet contain heteromorphic synaptonemal complexes indicating heterozygosity for inversions or centromere shifts. The European pied flycatcher, gouldian finch, and domestic canary have extended centromeres in several macro- and microchromosomes.

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Section: Discussionmentioning

confidence: 80%

Section: Discussionmentioning

confidence: 97%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Germline-Restricted Chromosomes and Autosomal Variants Revealed by Pachytene Karyotyping of 17 Avian Species

Malinovskaya

Slobodchikova

Grishko

et al. 2022

Cytogenet Genome Res

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“…Although a germline-restricted chromosome (GRC) was discovered in the zebra finch ( Taeniopygia guttata ) already 25 years ago ( Pigozzi and Solari 1998 ), it has only recently been recognized that such an extra chromosome is likely present in all songbird species ( Torgasheva et al 2019 ; Kinsella et al 2019 ). Despite its conserved presence throughout ∼50 million years of songbird evolution, the chromosome is highly dynamic in size ( Torgasheva et al 2019 ; Sotelo–Muñoz et al 2022 ) and in genetic content ( Kinsella et al 2019 ; Schlebusch et al 2022 ). Thus, in comparison with the standard set of autosomes and sex chromosomes (together referred to as A chromosomes; “A-chrs” hereafter) which are largely syntenic and collinear ( Waters et al 2021 ), the GRC is by far the most dynamic chromosome in birds ( Bravo et al 2021 ; Borodin et al 2022 ; Schlebusch et al 2022 ), similar to the gene-poor and repeat-rich W chromosome ( Zhou et al 2014 ; Peona et al 2021 ).…”

Section: Introductionmentioning

confidence: 99%

Micro Germline-Restricted Chromosome in Blue Tits: Evidence for Meiotic Functions

Mueller¹,

Schlebusch

Pei³

et al. 2023

Molecular Biology and Evolution

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The germline-restricted chromosome (GRC) is likely present in all songbird species, but differs widely in size and gene content. This extra chromosome has been described as either a microchromosome with only limited basic gene content or a macrochromosome with enriched gene functions related to female gonad and embryo development. Here, we assembled, annotated and characterized the first micro-GRC in the blue tit (Cyanistes caeruleus) using high-fidelity long-read sequencing data. Although some genes on the blue tit GRC show signals of pseudogenization, others potentially have important functions, either currently or in the past. We highlight the GRC gene paralog BMP15, which is among the highest expressed GRC genes both in blue tits and in zebra finches (Taeniopygia guttata), and is known to play a role in oocyte and follicular maturation in other vertebrates. The GRC genes of the blue tit are further enriched for functions related to the synaptonemal complex. We found a similar functional enrichment when analyzing published data on GRC genes from two nightingale species (Luscinia spp.). We hypothesize that these genes play a role in maintaining standard maternal inheritance or in recombining maternal and paternal GRCs during potential episodes of biparental inheritance.

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Mendelian nightmares: the germline-restricted chromosome of songbirds

et al. 2022

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Germline-restricted chromosomes (GRCs) are accessory chromosomes that occur only in germ cells. They are eliminated from somatic cells through programmed DNA elimination during embryo development. GRCs have been observed in several unrelated animal taxa and show peculiar modes of non-Mendelian inheritance and within-individual elimination. Recent cytogenetic and phylogenomic evidence suggests that a GRC is present across the species-rich songbirds, but absent in non-passerine birds, implying that over half of all 10,500 bird species have extensive germline/soma genome differences. Here, we review recent insights gained from genomic, transcriptomic, and cytogenetic approaches with regard to the genetic content, phylogenetic distribution, and inheritance of the songbird GRC. While many questions remain unsolved in terms of GRC inheritance, elimination, and function, we discuss plausible scenarios and future directions for understanding this widespread form of programmed DNA elimination.

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Germline-restricted chromosome shows remarkable variation in size among closely related passerine species

Cited by 8 publications

References 36 publications

Germline-Restricted Chromosomes and Autosomal Variants Revealed by Pachytene Karyotyping of 17 Avian Species

Germline-Restricted Chromosomes and Autosomal Variants Revealed by Pachytene Karyotyping of 17 Avian Species

Micro Germline-Restricted Chromosome in Blue Tits: Evidence for Meiotic Functions

Mendelian nightmares: the germline-restricted chromosome of songbirds

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