GermlineChrom · Evolutionary origin and impact of germline-restricted chromosomes

Many multicellular organisms have a division between germline and soma. It has been long-standing dogma that all these cells have the same genome as they develop from a single cell. However, programmed DNA elimination can remove DNA during germline–soma differentiation and thereby lead to dramatic differences in genome organization between tissues. The evolution and function of programmed DNA elimination remains mysterious due to technological limitations and lack of an evolutionary framework. However, a role of this phenomenon in minimizing germline–soma genetic conflict has been suggested. This conflict arises when developmental gene expression is beneficial for the germline but deleterious for the soma. The aim of this proposal is to test whether programmed DNA elimination allows germline-specific expression of developmental genes to minimize germline–soma conflict. Using the germline-restricted chromosome (GRC) of the zebra finch as a unique study system, I have recently pioneered high-throughput genomics to overcome previous limitations. Combining my novel approach with transcriptomics, proteomics, cytogenetics, and developmental and functional genomics will provide unprecedented insights into the evolution and function of germline–soma genome differences. First, I will establish the so far first GRC study system by generating a zebra finch GRC reference assembly. Second, I will test how the GRC is inherited and maintained in zebra finch populations. Third, I will elucidate the long-term evolutionary history of GRCs across songbirds to reveal genes that are most conserved and thus candidates for GRC function. Fourth, I will trace GRC expression and elimination across zebra finch development, and functionally validate candidate genes. Altogether, I will establish an evolutionary framework which will significantly advance our understanding of programmed DNA elimination during germline–soma differentiation, a phenomenon likely widespread across the Tree of Life.