Germline-restricted chromosome (GRC) is widespread among songbirds

Significance

We discovered that contrary to other bird species and most other animals, all examined songbird lineages contain a different number of chromosomes in the somatic and germline genomes. Their germ cells have an additional germline-restricted chromosome (GRC). GRCs contain highly duplicated genetic material represented by repetitive elements and sequences homologous to unique regions of the somatic genome. Surprisingly, GRCs even in very closely related species, vary drastically in size and show little homology. We hypothesize that the GRC was formed as an additional parasitic microchromosome in the songbird ancestor about 35 million years ago and subsequently underwent significant changes in size and genetic content, becoming an important component of the germline genome.

Abstract

An unusual supernumerary chromosome has been reported for two related avian species, the zebra and Bengalese finches. This large, germline-restricted chromosome (GRC) is eliminated from somatic cells and spermatids and transmitted via oocytes only. Its origin, distribution among avian lineages, and function were mostly unknown so far. Using immunolocalization of key meiotic proteins, we found that GRCs of varying size and genetic content are present in all 16 songbird species investigated and absent from germline genomes of all eight examined bird species from other avian orders. Results of fluorescent in situ hybridization of microdissected GRC probes and their sequencing indicate that GRCs show little homology between songbird species and contain a variety of repetitive elements and unique sequences with paralogs in the somatic genome. Our data suggest that the GRC evolved in the common ancestor of all songbirds and underwent significant changes in the extant descendant lineages.

• avian genome

• programmed DNA elimination

• meiosis

• Passeriformes

• chromosome evolution

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