Rapid Telomere Movement in Meiotic Prophase Is Promoted By NDJ1, MPS3, and CSM4 and Is Modulated by Recombination

Abstract

Haploidization of the genome in meiosis requires that chromosomes be sorted exclusively into pairs stabilized by synaptonemal complexes (SCs) and crossovers. This sorting and pairing is accompanied by active chromosome positioning in meiotic prophase in which telomeres cluster near the spindle pole to form the bouquet before dispersing around the nuclear envelope. We now describe telomere-led rapid prophase movements (RPMs) that frequently exceed 1 microm/s and persist throughout meiotic prophase. Bouquet formation and RPMs depend on NDJ1, MPS3, and a new member of this pathway, CSM4, which encodes a meiosis-specific nuclear envelope protein required specifically for telomere mobility. RPMs initiate independently of recombination but differ quantitatively in mutants that fail to complete recombination, suggesting that RPMs respond to recombination status. Together with recombination defects described for ndj1, our observations suggest that RPMs and SCs balance the disruption and stabilization of recombinational interactions, respectively, to regulate crossing over.

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

“…Our analyses showed that chromosomes in live meiocytes in zygonema and pachynema exhibited very dynamic and complex patterns of motility. In zygonema, we registered chromosome velocities averaging 400 nm s Ϫ1 , which is within the same order of magnitude as the speed of the RPMs in budding yeast (10). In pachynema, chromosome movements were slower, reaching an average maximum velocity of 148 nm s Ϫ1 .…”

“…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).…”

“…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).…”

Opening the DNA repair toolbox: Localization of DNA double strand breaks to the nuclear periphery

“…28 Likewise, in meiotic cells Mps3 is required for formation of well-defined chromosomal bouquets where telomeres transiently localize into a single focus, 32,33 and Mps3 is required for rapid telomereled chromosome movements during meiotic prophase. 34 Likewise, meiotic bouquet formation also requires Sun1 and Sun2 in mammalian cells. 35,36 The interactions between yeast Mps3 and telomeres is likely to be mediated by a direct interaction with the Est1 component of the telomerase machinery.…”