On the origin and evolution of germline chromosomes in songbirds

Hansson, Bengt

doi:10.1073/pnas.1906803116

Cited by 15 publications

(20 citation statements)

References 20 publications

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“…The phylogeny of the trim71 gene (Supplementary Fig. 9a) even suggests emergence of the GRC in the common ancestor of Passeriformes, earlier than recently suggested through cytogenetic GRC presence in oscine songbirds 9,27 . Therefore, we predict the GRC to be present in half of all bird species.…”

Section: Discussionmentioning

confidence: 70%

Programmed DNA elimination of germline development genes in songbirds

et al. 2019

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In some eukaryotes, germline and somatic genomes differ dramatically in their composition. Here we characterise a major germline-soma dissimilarity caused by a germline-restricted chromosome (GRC) in songbirds. We show that the zebra finch GRC contains >115 genes paralogous to single-copy genes on 18 autosomes and the Z chromosome, and is enriched in genes involved in female gonad development. Many genes are likely functional, evidenced by expression in testes and ovaries at the RNA and protein level. Using comparative genomics, we show that genes have been added to the GRC over millions of years of evolution, with embryonic development genes bicc1 and trim71 dating to the ancestor of songbirds and dozens of other genes added very recently. The somatic elimination of this evolutionarily dynamic chromosome in songbirds implies a unique mechanism to minimise genetic conflict between germline and soma, relevant to antagonistic pleiotropy, an evolutionary process underlying ageing and sexual traits.

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Section: Discussionmentioning

confidence: 70%

Programmed DNA elimination of germline development genes in songbirds

et al. 2019

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“…Songbirds are an exception. In their germ cells, they have an additional chromosome called "Germline Restricted Chromosome" (GRC), which is not present in somatic cells 1 . The GRC has been described first in the zebra finch 2,3 and then in the Bengalese finch 4 .…”

Section: All Songbirds Studied To Date Have An Additional Germline Rementioning

confidence: 99%

Germline-restricted chromosome (GRC) in the sand martin and the pale martin (Hirundinidae, Aves): synapsis, recombination and copy number variation

Malinovskaya

Zadesenets

Карамышева

et al. 2020

Sci Rep

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GmbH, Germany). The location of each captured immunostained spread was recorded so that it could be relocated on the slide after FISH. Electron microscopy was carried out using a JEM-1400 electron microscope (JEOL, Tokyo, Japan) at 80 kV. All microscopy studies were carried out at the Center for Microscopic Analysis of Biological Objects of SD RAS (Novosibirsk, Russia). Corel PaintShop Pro X6 (Corel) was used for a correction of image brightness and contrast. Chromosome measurements and generation of recombination maps of GRCs. Centromeres were identified by ACA foci. MLH1 signals were only scored if they were localized on SCs. The length of the SC was measured in micrometers and the positions of MLH1 foci in relation to the centromere were recorded using MicroMeasure 3.3 30. SCs of GRC and macrochromosomes were identified by their relative lengths and centromeric indexes. SC1 is the largest submetacentric. SC2 and SC3 are large subacrocentrics of similar sizes but different centromeric indexes. SC4 is middle size metacentric, SC5 and SC6 are subacrocentrics of the same size, which differ from each other in the centromeric indexes. On bone marrow metaphase chromosome spreads, Z and W are identified as a pair of non-matching macrochromosomes: metacentric and submetacentric (correspondingly). At SC spreads, ZW is identified as macrobivalent with misaligned centromeres and/or asynapsed ends of the axial elements. GRC is identified as the only acrocentric macrobivalent or univalent. To generate recombination maps, we divided the length of the SC into equal intervals approximately equal to 1 µm and plotted the proportion of MLH1 foci located in each interval. STATISTICA 6.0 software package (StatSoft, Tulsa, OK, USA) was used for descriptive statistics. All results were expressed as mean ± SD; p < 0.05 was considered as statistically significant.

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“…In sexually reproducing eukaryotes, the stable inheritance of the nuclear DNA typically requires recombination and segregation of pairs of homologous chromosomes that come from both parents. The songbird germline-restricted chromosome, GRC, is an intriguing exception 1,9,13 . As the name indicates, the GRC is only found in cells of the germline in all songbirds examined to date, but is absent from any somatic tissue 4,6,8,9 , presumably due to its elimination from somatic cells during early embryogenesis.…”

Section: Mainmentioning

confidence: 99%

“…Based on observations from multiple species [5][6][7] , it has been concluded that the avian GRC is exclusively maternally inherited. Yet to date, the mode of inheritance of the GRC remains untested genetically, implying that suggestions about the evolutionary significance of the GRC 5,8,13 remain speculative. In this study, we used the two zebra finch subspecies T. g. castanotis of Australia (hereafter castanotis) and T. g. guttata of the Indonesian islands such as Timor (hereafter guttata) to address the issue of inheritance.…”

mentioning

confidence: 99%

Occasional paternal inheritance of the germline-restricted chromosome in songbirds

Pei

Forstmeier

Ruiz‐Ruano

et al. 2021

Preprint

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All songbirds have one special accessory chromosome1–4, the so-called germline-restricted chromosome (GRC)4–7, which is only present in germline cells and absent from all somatic tissues. Earlier work on the zebra finch (Taeniopygia guttata castanotis) showed that the GRC is inherited only through the female line4,6,8,9 – like mitochondrial DNA7,9–12 – and is eliminated from the sperm during spermatogenesis5,7,9–11. Here we show that the GRC can also be paternally inherited. Confocal microscopy using GRC-specific FISH probes indicated that a considerable fraction of sperm heads (1-19%) in zebra finch ejaculates still contained the GRC. In line with these cytogenetic data, sequencing of ejaculates revealed that individual males from two families differed strongly and consistently in the number of GRCs in their ejaculates. Examining a captive-bred population of hybrids of the two zebra finch subspecies (T. g. guttata and T. g. castanotis) revealed that the descendants inherited their mitochondria from a castanotis mother but their GRC from a guttata father. Moreover, GRC haplotypes across nine different castanotis matrilines showed at best a weak tendency to be co-inherited with mtDNA haplotypes. Within castanotis, the GRC showed little variability, while the mtDNA of matrilines was highly divergent. This suggests that a single GRC haplotype has recently spread across the entire castanotis population, crossing the matriline boundaries via paternal spillover. Our findings raise the possibility that certain GRC haplotypes could selfishly spread through the population, via additional paternal transmission, thereby outcompeting other GRC haplotypes that were limited to strict maternal inheritance, even if this was partly detrimental to organismal fitness.

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On the origin and evolution of germline chromosomes in songbirds

Cited by 15 publications

References 20 publications

Programmed DNA elimination of germline development genes in songbirds

Programmed DNA elimination of germline development genes in songbirds

Germline-restricted chromosome (GRC) in the sand martin and the pale martin (Hirundinidae, Aves): synapsis, recombination and copy number variation

Occasional paternal inheritance of the germline-restricted chromosome in songbirds

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