Centromeres are an important part of chromosomes which direct chromosome segregation during cell division. Their modifications can therefore explain the unusual mitotic and meiotic behaviour of certain chromosomes, such as the germline-restricted chromosome (GRC) of songbirds. This chromosome is eliminated from somatic cells during early embryogenesis and later also from male germ cells during spermatogenesis. Although the mechanism of elimination is not yet known, it is possible that it involves a modification of the centromeric sequence on the GRC, resulting in problems with the attachment of this chromosome to the mitotic or meiotic spindle and its lagging during anaphase, which eventually leads to its elimination from the nucleus. However, the repetitive nature and rapid evolution of centromeres make their identification and comparative analysis across species and chromosomes challenging. Here, we used a combination of cytogenetic and genomic approaches to identify the centromeric sequences of two closely related songbird species, the common nightingale (Luscinia megarhynchos) and the thrush nightingale (L. luscinia). We found a 436-bp satellite repeat present in the centromeric regions of all regular chromosomes (i.e., autosomes and sex chromosomes), making it a strong candidate for the centromeric repeat. This centromeric repeat was highly similar between the two nightingale species. Interestingly, hybridization of the probe to this satellite repeat on meiotic spreads suggested that this repeat is missing on the GRC. Our results indicate that the change of the centromeric sequence may underlie the unusual inheritance and programmed DNA elimination of the GRC in songbirds.

• Publikační typ
• časopisecké články MeSH

Bird genomes are among the most stable in terms of synteny and gene content across vertebrates. However, germline-restricted chromosomes (GRCs) represent a striking exception where programmed DNA elimination confines large-scale genomic changes to the germline. GRCs are known to occur in songbirds (oscines), but have been studied only in a few species of Passerides such as the zebra finch, the key model for passerine genomics. Their presence and evolutionary dynamics in most major passerine lineages remain largely unexplored, with suboscines entirely unexamined by cytogenetic or genomic methods. Here, we present the most comprehensive comparative analysis of GRCs to date, spanning 44 million years of passerine evolution. By generating the first germline reference genomes of an oscine and a suboscine, 22 novel germline draft genomes spanning nearly all major passerine lineages and a germline draft genome of a parrot outgroup, we show that the GRC is likely present in 6,700 passerine species. Our results reveal that the GRC evolves rapidly and distinctly from the standard A chromosomes (autosomes and sex chromosomes), yet retains functionally important, selectively maintained genes. We observed gene and repeat turnover occuring orders of magnitude faster than on the A chromosomes. Some GRC genes, such as cpeb1 and pim1, are widespread from an ancient duplication. In contrast, other GRC genes, like mfsd2b and bmp15, have been independently duplicated onto the GRC multiple times, suggesting adaptive constraints. The discovery of zglp1 on the zebra finch GRC, initially copied from chromosome 30 and subsequently lost from it, indicates functional replacement, where the GRC permits gene loss from the standard genome. As the GRC harbors the only zglp1 copy in most of the ~4000 Passerides species, GRC loss would compromise essential germline functions. Our findings establish the GRC as a genomic innovator driving rapid germline evolution. This fact highlights its evolutionary significance for passerine diversification and suggests that programmed DNA elimination may be an overlooked yet phylogenetically widespread mechanism in many understudied animal lineages.

• Publikační typ
• časopisecké články MeSH
• preprinty MeSH

The germline-restricted chromosome (GRC) of songbirds represents a taxonomically widespread example of programmed DNA elimination. Despite its apparent indispensability, we still know very little about the GRC's genetic composition, function, and evolutionary significance. Here we assemble the GRC in two closely related species, the common and thrush nightingale. In total we identify 192 genes across the two GRCs, with many of them present in multiple copies. Interestingly, the GRC appears to be under little selective pressure, with the genetic content differing dramatically between the two species and many GRC genes appearing to be pseudogenized fragments. Only one gene, cpeb1, has a complete coding region in all examined individuals of the two species and shows no copy number variation. The acquisition of this gene by the GRC corresponds with the earliest estimates of the GRC origin, making it a good candidate for the functional indispensability of the GRC in songbirds.

• MeSH
• biologická evoluce MeSH
• chromozomy MeSH
• otevřené čtecí rámce MeSH
• zárodečné buňky MeSH
• zpěvní ptáci * genetika   MeSH
• zvířata MeSH
• Check Tag
• zvířata MeSH
• Publikační typ
• časopisecké články MeSH
• práce podpořená grantem MeSH

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.

• Klíčová slova
• B chromosome, Chromosome elimination, Germline-restricted chromosome, Germline/soma genome difference, Non-Mendelian inheritance,
• MeSH
• chromozomy genetika   MeSH
• DNA MeSH
• fylogeneze MeSH
• sny MeSH
• zárodečné buňky MeSH
• zpěvní ptáci * genetika   MeSH
• zvířata MeSH
• Check Tag
• zvířata MeSH
• Publikační typ
• časopisecké články MeSH
• práce podpořená grantem MeSH
• přehledy MeSH
• Názvy látek
• DNA MeSH

Passerine birds have a supernumerary chromosome in their germ cells called the germline-restricted chromosome (GRC). The GRC was first discovered more than two decades ago in zebra finch but recent studies have suggested that it is likely present in all passerines, the most species rich avian order, encompassing more than half of all modern bird species. Despite its wide taxonomic distribution, studies on this chromosome are still scarce and limited to a few species. Here, we cytogenetically analyzed the GRC in five closely related estrildid finch species of the genus Lonchura. We show that the GRC varies enormously in size, ranging from a tiny micro-chromosome to one of the largest macro-chromosomes in the cell, not only among recently diverged species but also within species and sometimes even between germ cells of a single individual. In Lonchura atricapilla, we also observed variation in GRC copy number among male germ cells of a single individual. Finally, our analysis of hybrids between two Lonchura species with noticeably different GRC size directly supported maternal inheritance of the GRC. Our results reveal the extraordinarily dynamic nature of the GRC, which might be caused by frequent gains and losses of sequences on this chromosome leading to substantial differences in genetic composition of the GRC between and even within species. Such differences might theoretically contribute to reproductive isolation between species and thus accelerate the speciation rate of passerine birds compared to other bird lineages.

• Klíčová slova
• Germline-restricted chromosome, Mosaicism, Programmed DNA elimination, Songbirds, Speciation, Spermatogenesis,
• MeSH
• chromozomy genetika   MeSH
• Passeriformes * genetika   MeSH
• pěnkavovití * genetika   MeSH
• zárodečné buňky MeSH
• zvířata MeSH
• Check Tag
• mužské pohlaví MeSH
• ženské pohlaví MeSH
• zvířata MeSH
• Publikační typ
• časopisecké články MeSH
• práce podpořená grantem MeSH