Programmed DNA elimination of germline development genes in songbirds

Abstract

24Genomes can vary within individual organisms. Programmed DNA elimination leads to dramatic 25 changes in genome organisation during the germline-soma differentiation of ciliates 1 , lampreys 2 , 26 nematodes 3,4 , and various other eukaryotes 5 . A particularly remarkable example of tissue-specific 27 genome differentiation is the germline-restricted chromosome (GRC) in the zebra finch which is 28 consistently absent from somatic cells 6 . Although the zebra finch is an important animal model 29 system 7 , molecular evidence from its large GRC (>150 megabases) is limited to a short intergenic 30 region 8 and a single mRNA 9 . Here, we combined cytogenetic, genomic, transcriptomic, and 31 proteomic evidence to resolve the evolutionary origin and functional significance of the GRC. 32First, by generating tissue-specific de-novo linked-read genome assemblies and re-sequencing 33 two additional germline and soma samples, we found that the GRC contains at least 115 genes 34 which are paralogous to single-copy genes on 18 autosomes and the Z chromosome. We detected 35 an amplification of ≥38 GRC-linked genes into high copy numbers (up to 308 copies) but, 36 surprisingly, no enrichment of transposable elements on the GRC. Second, transcriptome and 37 proteome data provided evidence for functional expression of GRC genes at the RNA and protein 38 levels in testes and ovaries. Interestingly, the GRC is enriched for genes with highly expressed 39 orthologs in chicken gonads and gene ontologies involved in female gonad development. Third, 40 we detected evolutionary strata of GRC-linked genes. Developmental genes such as bicc1 and 41 trim71 have resided on the GRC for tens of millions of years, whereas dozens have become 42 GRC-linked very recently. The GRC is thus likely widespread in songbirds (half of all bird 43 species) and its rapid evolution may have contributed to their diversification. Together, our 44 results demonstrate a highly dynamic evolutionary history of the songbird GRC leading to 45 dramatic germline-soma genome differences as a novel mechanism to minimise genetic conflict 46 between germline and soma. Text 48 Not all cells of an organism must contain the same genome. Some eukaryotes exhibit dramatic 49 differences between their germline and somatic genomes, resulting from programmed DNA 50 elimination of chromosomes or fragments thereof during germline-soma differentiation 5 . Here 51 we present the first comprehensive analyses of a germline-restricted chromosome (GRC). The 52 zebra finch (Taeniopygia guttata) GRC is the largest chromosome of this songbird 6 and likely 53 comprises >10% of the genome (>150 megabases) 7,10 . Cytogenetic evidence suggests the GRC is 54 inherited through the female germline, expelled late during spermatogenesis, and eliminated from 55 the soma during early embryo development 6,11 . Previous analyses of a 19-kb intergenic region 56 suggested that the GRC contains sequences with high similarity to regular chromosomes ('A 57 chromosomes') 8 . 58 59In order to reliably ide...

Evolution of gene-rich germline restricted chromosomes in black-winged fungus gnats through introgression (Diptera: Sciaridae)

“…However, to the contrary, the sequence data presented here have revealed that there are many genes on the B. coprophila GRCs and they are paralogs of genes on the other chromosomes. Recently it has also been reported for other plants and animals that genes on eliminated DNA have paralogs in the other chromosomes [10,45]. Although it remains to be seen whether the multitude of B. coprophila GRC genes are transcribed and play an important role, with GRC genes now identified, future studies can elucidate when and where their transcription occurs and determine whether these chromosomes are necessary in B. coprophila.…”

“…Recent genomic work on lampreys and nematodes (with chromatin diminution) and songbirds (with chromosome elimination) have found that the germline restricted portions of the genome often carry protein coding genes involved in germ tissue maturation and function [8][9][10][11]. Therefore, a leading hypothesis is that germline restricted DNA may help resolve intralocus conflict between the germline and somatic cells [10,12]. However, although chromatin diminution and chromosome elimination have similar consequences, the initial evolution of these systems probably differs, as the mechanism of elimination is substantially different in these two systems.…”

“…the chromosomes which are found in the somatic cells as well as the germ cells), with greater variation in presence/number of chromosomes than the core chromosome set. However, while B chromosomes are non-essential, recent genomic work in songbirds suggests that GRCs likely play an important, and perhaps fundamental role in zebra finches [10] and are evolutionarily conserved across songbirds [15]. Furthermore, there is no clear evidence that GRCs spread through drive and therefore unlike B chromosomes most likely persist due to their functional importance, rather than as reproductive parasites.…”

Specific Features of Sex Determination in Birds on the Example ofGallus gallusdomesticus

“…Germline-restricted chromosomes are probably widespread in the highly dynamic evolutionary history of songbirds, which leads to significant differences between the genome of germline cells and the genome of somatic cells. This is a new mechanism for minimizing the genetic conflict between germ line cells and somatic cells [20,21].…”

Transcribed germline-limited coding sequences inOxytricha trifallax

“…Protein coding sequences are discarded in all these cases, and genes eliminated from somatic lineage cells are typically predicted to have functions in the germline and embryogenesis (Smith et al 2012;Bryant et al 2016). The songbird Taeniopygia guttata has a germline-limited chromosome that is deleted from somatic lineage cells (Pigozzi and Solari 1998;Pigozzi and Solari 2005;Itoh et al 2009;Biederman et al 2018;Kinsella et al 2019;Torgasheva et al 2019).…”