Programmed DNA elimination of germline development genes in songbirds
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AuthorKinsella, Cormac; Ruiz-Ruano, Francisco J.; Cabrero Hurtado, Josefa; Martínez Camacho, Juan Pedro
Kinsella, C. M., Ruiz-Ruano, F. J., Dion-Côté, A. M., Charles, A. J., Gossmann, T. I., Cabrero, J., ... & Forstmeier, W. (2019). Programmed DNA elimination of germline development genes in songbirds. Nature Communications, 10(1), 1-10.
SponsorshipA.S. was supported by grants from the Swedish Research Council Formas (2017-01597), the Swedish Research Council Vetenskapsrådet (2016–05139), and the SciLifeLab Swedish Biodiversity Program (2015- R14). The Swedish Biodiversity Program has been made available by support from the Knut and Alice Wallenberg Foundation. A.S. acknowledges funding from the Knut and Alice Wallenberg Foundation via Hans Ellegren. F.J.R.R., J.C., and J.P.M.C. were supported by the Spanish Secretaría de Estado de Investigación, Desarrollo e Innovación (CGL2015–70750-P), including FEDER funds, and F.J.R.R. was also supported by a Junta de Andalucía fellowship and a postdoctoral fellowship from Sven och Lilly Lawskis fond. A.M.D.C was supported by a postdoctoral fellowship from Sven och Lilly Lawskis fond, the Fonds de Recherche du Québec – Santé (FRQ-S 33616) and the National Sciences and Engineering Research Council of Canada (NSERC PDF-51651-2018). T.I.G. was supported by a Leverhulme Early Career Fellowship Grant (ECF-2015-453). T.I.G., A.J.C. (CABM DTP), and M.J.P.S. (Sir Henry Wellcome and Vice-Chancellor’s Fellowships) were supported by a NERC grant (NE/N013832/1). N.H. was supported by a Patrick & Irwin-Packington Fellowship from the University of Sheffield and a Royal Society Dorothy Hodgkin Fellowship. D.K. was supported by the National Research Foundation Singapore and the Singapore Ministry of Education under its Research Centres of Excellence initiative. W.F. was supported by the Max Planck Society. Some of the computations were performed on resources provided by the Swedish National Infrastructure for Computing (SNIC) through Uppsala Multidisciplinary Center for Advanced Computational Science (UPPMAX). The authors acknowledge support from the National Genomics Infrastructure in Stockholm funded by Science for Life Laboratory, the Knut and Alice Wallenberg Foundation and the Swedish Research Council.
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.