Chromosome mobility during meiotic prophase in Saccharomyces cerevisiae

Abstract

In many organisms, a synaptonemal complex (SC) intimately connects each pair of homologous chromosomes during much of the first meiotic prophase and is thought to play a role in regulating recombination. In the yeast Saccharomyces cerevisiae, the central element of each SC contains Zip1, a protein orthologous to mammalian SYCP1. To study the dynamics of SCs in living meiotic cells, a functional ZIP1::GFP fusion was introduced into yeast and analyzed by fluorescence video microscopy. During pachytene, SCs exhibited dramatic and continuous movement throughout the nucleus, traversing relatively large distances while twisting, folding, and unfolding. Chromosomal movements were accompanied by changes in the shape of the nucleus, and all movements were reversibly inhibited by the actin antagonist Latrunculin B. Normal movement required the NDJ1 gene, which encodes a meiosisspecific telomere protein needed for the attachment of telomeres to the nuclear periphery and for normal kinetics of recombination and meiosis. These results show that SC movements involve telomere attachment to the nuclear periphery and are actindependent and suggest these movements could facilitate completion of meiotic recombination.actin ͉ meiosis ͉ recombination ͉ synaptonemal complex ͉ yeast S porulation of diploid cells in the ascomycete Saccharomyces cerevisiae is accompanied by a typical meiotic cell cycle that culminates with the production of four haploid ascospores. Chromosomes pair, undergo recombination, and then segregate from each other in two successive divisions. Reciprocal recombination between homologous chromosomes takes place during prophase of the first meiotic division (prophase I) and is essential for proper segregation. In S. cerevisiae, prophase I can be divided into leptotene-, zygotene-, pachytene-, and diplotene-like substages defined by the state of chromosome pairing and condensation. During leptotene, chromosomes organize on proteinaceous axial elements, and double-strand breaks (DSBs) begin to appear in DNA, initiating recombination. At the same time, perinuclear telomeres begin to cluster near the spindle pole body (the yeast centrosome), pushing chromosomes into a bouquetlike configuration at the leptotene/zygotene transition. At zygotene, the axial elements pair or synapse at the sites of DSBs, and tripartite proteinaceous structures called synaptonemal complexes (SCs) begin to form between homologous chromosomes (1-3). At pachytene, the SCs have matured by a zipper-like mechanism into ribbon-like structures that are embedded at each end in the nuclear envelope and intimately connect each pair of homologues from end to end (3-5). Mature SCs are present for at least 1 h in strain SK1 and longer in other strains, so that pachytene accounts for a relatively large part of prophase I (6-8). In S. cerevisiae, DNA strand invasion and Holliday junction recombination intermediates are observed throughout zygotene and pachytene (9-12), suggesting that recombination is completed during pachytene, presumably when chromosomes...

Live imaging of rapid chromosome movements in meiotic prophase I in maize

“…In fission yeast, nuclear motility was highly dynamic throughout prophase and movements of all chromosomes were coordinated (11). In budding yeast, in contrast, chromosomes moved independently from each other (9,10,26), and although the chromosome movements were also observed throughout prophase, they were most complex in early prophase when two distinct classes of chromosome velocity could be identified (10). In mouse spermatocytes, rotational chromatin movements and more subtle movements of individual chromosome segments were observed in zygonema and pachynema (14).…”

“…The detailed analyses of nuclear motility in early meiotic prophase in yeasts (8)(9)(10)(11)(12)20) and maize (this study), and the more fragmentary studies in mouse (14) and rat (13), have shown that patterns of meiotic chromosome movements exhibit immense diversity among species. In fission yeast, nuclear motility was highly dynamic throughout prophase and movements of all chromosomes were coordinated (11).…”

“…At least some of these differences may stem from differences in the cytoskeletal forces that are responsible for prophase movements in each species. In fission yeast and rat, the microtubule cytoskeleton is involved in chromosome motility (25,27), whereas in budding yeast, the actin cytoskeleton is used, but microtubules are not essential (9,20). In maize, both actin and tubulin appear to be involved in prophase chromosome movements.…”

“…To examine whether components of the cytoskeleton are required for chromosome movements in meiotic prophase in maize, we tested the effects of an actin-depolymerizing drug latrunculin B and a tubulin-depolymerizing drug colchicine (9,17). An hour-long incubation of anthers in latrunculin B (at concentrations 0.5 or 1 M) or colchicine (1 or 5 mM) resulted in cessation of all chromosome movements as well as NE deformations in both zygonema and pachynema (Movies S29 and S30).…”

“…Observations of live meiocytes in budding and fission yeasts have shown that during meiotic prophase chromosomes exhibit unexpectedly dynamic motility: the ''horse-tail'' chromosome movements in fission yeast and the rapid prophase movements (RPMs) in budding yeast (8)(9)(10)(11). In fission yeast, these movements are particularly dramatic, with the entire nucleus moving violently back and forth (11,12).…”