Mammalian condensin I controls higher-order chromosome organization and homologous recombination in meiotic prophase I

Abstract

The meiotic chromosome structure, defined by the axis-chromatin loop organization, is essential for proper homologue synapsis through the formation of the synaptonemal complex, and faithful homologous recombination. Here, we show that the conserved SMC-condensin I complex, which shapes the genome through chromatin loop extrusion, plays a pivotal role in controlling the higher-order prophase I meiotic chromosome structure. By analyzing the NCAPD2 condensin I subunit, we found that this complex colocalizes with prophase I chromatin and is essential for male fertility. NCAPD2 restricts chromatin loop extension and controls the localization of chromosome structural proteins, including the axial component HORMAD1 and central element proteins (SYCP1, TEX12, SIX6OS1), thus regulating the synaptonemal complex width. Moreover, NCAPD2 promotes timely and efficient recombination by controlling {gamma}H2AX, DMC1 and pro-crossover proteins turnover. We propose that condensin I, by organizing chromatin loops in prophase I, controls synaptonemal complex organization and recombination outcome in mammals.