Scheduled release of chromatin-nuclear periphery contact during meiotic chromosome movements preserves genome integrity

Correct chromosome segregation in meiosis requires side-by-side alignment of the parental homologous chromosomes. This is facilitated by rapid prophase chromosome movements, which are driven by cytoplasmic forces and transmitted by the attachment of chromosome ends to the nuclear periphery through membrane-spanning proteins. Aligned chromosome pairs become connected through the synaptonemal complex (SC). However, whether the chromatin is removed from the nuclear periphery as a consequence of chromosome motions or by a dedicated mechanism is not fully understood. Here, we describe a dedicated mechanism to remove chromatin from the nuclear periphery through vaccinia related kinase (VRK-1) and phosphorylation of its downstream target Barrier to Autointegration Factor 1 (BAF-1) in Caenorhabditis elegans early prophase of meiosis. Interfering with chromatin removal leads to delayed chromosome pairing, impaired synapsis, oocytes with abnormal chromosomes and elevated apoptosis. Long read sequencing revealed the accumulation of deletions and duplications in the offspring in the absence of VRK-1 underscoring the importance of the BAF-1 - VRK-1 module in preserving genome stability in gametes during rapid chromosome movements.