Cytoskeletal forces span the nuclear envelope to coordinate meiotic chromosome pairing and synapsis.
During meiosis, each chromosome must pair with its unique homologous partner, a process that usually culminates with the formation of the synaptonemal complex (SC). In the nematode Caenorhabditis elegans, special regions on each chromosome known as pairing centers are essential for both homologous pairing and synapsis. We report that during early meiosis, pairing centers establish transient connections to the cytoplasmic microtubule network. These connections through the intact nuclear envelope require the SUN/KASH domain protein pair SUN-1 and ZYG-12. Disruption of microtubules inhibits chromosome pairing, indicating that these connections promote interhomolog interactions. Dynein activity is essential to license formation of the SC once pairing has been accomplished, most likely by overcoming a barrier imposed by the chromosome-nuclear envelope connection. Our findings thus provide insight into how homolog pairing is accomplished in meiosis and into the mechanisms regulating synapsis so that it occurs selectively between homologs. For a video summary of this article, see the PaperFlick file with the Supplemental Data available online.
Sato
Aya
A
Howard Hughes Medical Institute, Chevy Chase, MD 20815 USA.
Isaac
Berith
B
Phillips
Carolyn M
CM
Rillo
Regina
R
Carlton
Peter M
PM
Wynne
David J
DJ
Kasad
Roshni A
RA
Dernburg
Abby F
AF
D000818:Animals; D017173:Caenorhabditis elegans / Q000166:cytology* / Q000378:metabolism; D029742:Caenorhabditis elegans Proteins / Q000378:metabolism; D018797:Cell Cycle Proteins / Q000378:metabolism; D023902:Chromosome Pairing; D002875:Chromosomes; D004398:Dyneins / Q000378:metabolism; D008540:Meiosis; D049469:Meiotic Prophase I; D008870:Microtubules / Q000378:metabolism*; D009685:Nuclear Envelope / Q000378:metabolism*; D018160:Receptors, Cytoplasmic and Nuclear / Q000378:metabolism
D029742:Caenorhabditis elegans Proteins; D018797:Cell Cycle Proteins; D018160:Receptors, Cytoplasmic and Nuclear; C514114:sun-1 protein, C elegans; C480800:zyg-12 protein, C elegans; D004398:Dyneins