Germline-Restricted Chromosome (GRC) is Widespread among Songbirds

Abstract

The genome of flying birds, the smallest among amniotes, reflects overweight of the extensive DNA loss over the unrestricted proliferation of selfish genetic elements, resulted in a shortage of repeated sequences and lack of B-chromosomes. The only exception of this rule has been described in zebra finch, which possesses a large germ-line restricted chromosome (GRC), transmitted via oocytes, eliminated from male postmeiotic cells and absent in somatic cell. It is considered as a rarity and its origin, content and function remain unclear. We discovered that all songbirds possess GRC: in various size and genetic content it is present in all fifteen songbird species investigated and absent from germ-line genomes of all eight species of other bird orders examined. Our data based on fluorescent in situ hybridization of DNA probes derived from GRCs of four different Passeri species and their sequencing indicate that the GRCs show low homology between avian species. They contain fragments of the somatic genomes, which include various unique and repetitive sequences. We propose that the GRC has formed in the common ancestor of the extant songbirds and undergone subsequent divergence. GRC presence in the germ line of every songbird studied indicate that it could contain genetic element(s) indispensable for gametogenesis, which are yet to be discovered. Eukaryotic genomes harbors various selfish genetic elements (transposons, B chromosomes, etc), which enhance their own transmission and might serve as a motors for evolutionary change and innovation 1 . In flying birds, the natural selection led to a reduction of genome size at the expense of transposable elements, introns, constitutive heterochromatin, paralogous genes and other repeated sequences. Resulted genomic compaction provides an economy of bird body mass, improving their metabolic efficiency 2 . An interesting way of resolving a conflict between the body mass and genome size was found in two closely related pet species of Estrildidae birds: zebra and Bengalese finches 3,4 . In all germ We thank M.I. Rodionova for the help in chromosome preparation, A. Maslov, D. Taranenko, I. Korobitsyn, M. Scherbakova for the help in bird collecting and the Microscopic Center of the Siberian Department of the Russian Academy of Sciences for granting access to microscopic equipment.

Programmed DNA elimination of germline development genes in songbirds

“…The presence of at least 7 genes in these three strata implies that the GRC is tens of millions of years old and likely present across songbirds (Extended Data Fig. 7), consistent with a recent cytogenetics preprint 20 . Notably, stratum 4 is specific to the zebra finch species and stratum 5 to the Australian zebra finch subspecies (Fig.…”

New genome assembly of the barn owl (Tyto alba alba)

“…The zebra finch genome was one of the closest related species for which the genome was assembled at the chromosomal level. Although this species counts 40 pairs of chromosomes and one germline restricted chromosome (Biederman et al, ; Torgasheva et al, ), only 37 chromosomes and scaffolds were assembled in Ensembl zebra finch karyotype (Figure ).…”

Content of and interactions between repetitive elements in programmatically eliminated chromosomes of the sea lamprey (Petromyzon marinus)

“…The sea lamprey ( Petromyzon marinus ) possesses a distinctive mechanism of differentiating somatic and germline lineages that is achieved by discarding large portions of the genome during early stages of development [1, 2]. Similar largescale changes in genome content and structure have been described in several groups of phylogenetically diverse organisms [3] including: ciliates [4-6], nematodes [7, 8], sciarid flies (reviewed in [9]), copepods [10], chironomids [11], several hagfish species [12-15], songbirds [16, 17], and at least two lamprey species [18, 19]. These changes in genome content/structure are generally known as programmed genome rearrangement (PGR).…”

“…as observed in nematodes, copepods, chironomids, sciarid flies and lampreys). This general pattern can be divided into nonexclusive two categories: chromosome elimination per se that involves the removal of whole intact chromosomes (hagfish [20], sciarid flies [9] and song birds [16, 17, 21]) and chromatin diminution which includes steps of excision and rejoining, or telomere restoration (roundworms [22, 23], copepods [24, 25], chironomids [26] and some hagfish [27]).…”