Disassembly of the synaptonemal complex in chicken oocytes analyzed by super-resolution microscopy

Abstract

The synaptonemal complex is an evolutionarily conserved, supramolecular structure that holds the homologous chromosomes together during the pachytene stage of the first meiotic prophase. Among vertebrates, synaptonemal complex dynamics has been analyzed in mouse spermatocytes following the assembly of its components from leptotene to pachytene stages. With few exceptions, a detailed study of the disassembly of SCs and the behavior of SC components at recombination sites at the onset of diplotene has not been accomplished. Here, we describe for the first time the progressive disassembly of the SC in chicken oocytes during the initial steps of desynapsis using immunolocalization of specific SC proteins and super-resolution microscopy. We found that transverse filament protein SYCP1 and central element component SYCE3 remain associated with the lateral elements at the beginning of chromosomal axis separation. As the separation between lateral elements widens, these proteins eventually disappear, without any evidence of subsequent association. Our observations support the idea that post-translational modifications of the central region components have a role at the initial phases of the SC disassembly. At the crossover sites, signaled by persistent MLH1 foci, the central region proteins are no longer detected when the SYCP3-positive lateral elements are widely separated. These findings are indicative that SC disassembly follows a general pattern along the desynaptic bivalents. The present work shows that the use of avian oocytes at prophase I provides a valuable model to explore the time course and chromosomal localization of SC proteins and its relationship with local changes along meiotic bivalents.