Spindle assembly checkpoint proteins regulate and monitor meiotic synapsis in C. elegans.
Homologue synapsis is required for meiotic chromosome segregation, but how synapsis is initiated between chromosomes is poorly understood. In Caenorhabditis elegans, synapsis and a checkpoint that monitors synapsis depend on pairing centers (PCs), cis-acting loci that interact with nuclear envelope proteins, such as SUN-1, to access cytoplasmic microtubules. Here, we report that spindle assembly checkpoint (SAC) components MAD-1, MAD-2, and BUB-3 are required to negatively regulate synapsis and promote the synapsis checkpoint response. Both of these roles are independent of a conserved component of the anaphase-promoting complex, indicating a unique role for these proteins in meiotic prophase. MAD-1 and MAD-2 localize to the periphery of meiotic nuclei and interact with SUN-1, suggesting a role at PCs. Consistent with this idea, MAD-1 and BUB-3 require full PC function to inhibit synapsis. We propose that SAC proteins monitor the stability of pairing, or tension, between homologues to regulate synapsis and elicit a checkpoint response.
Department of Molecular, Cell, and Developmental Biology, University of California, Santa Cruz, Santa Cruz, CA 95064.
Tisha
T
Bohr
Department of Molecular, Cell, and Developmental Biology, University of California, Santa Cruz, Santa Cruz, CA 95064.
Christian R
CR
Nelson
Department of Molecular, Cell, and Developmental Biology, University of California, Santa Cruz, Santa Cruz, CA 95064.
Erin
E
Klee
Department of Molecular, Cell, and Developmental Biology, University of California, Santa Cruz, Santa Cruz, CA 95064 nbhalla@ucsc.edu.
Needhi
N
Bhalla
D000818:Animals; D017173:Caenorhabditis elegans / Q000235:genetics / Q000502:physiology*; D029742:Caenorhabditis elegans Proteins / Q000235:genetics / Q000378:metabolism*; D018797:Cell Cycle Proteins / Q000235:genetics / Q000378:metabolism*; D002467:Cell Nucleus / Q000378:metabolism; D023902:Chromosome Pairing; D020090:Chromosome Segregation; D002875:Chromosomes / Q000378:metabolism; D004398:Dyneins / Q000235:genetics / Q000378:metabolism; D064246:Mad2 Proteins / Q000235:genetics / Q000378:metabolism*; D008540:Meiosis; D009687:Nuclear Proteins / Q000235:genetics / Q000378:metabolism*; D034622:RNA Interference; D034741:RNA, Small Interfering; D018160:Receptors, Cytoplasmic and Nuclear / Q000378:metabolism; D008941:Spindle Apparatus / Q000378:metabolism*
C000599843:BUB-3 protein, C elegans; D029742:Caenorhabditis elegans Proteins; D018797:Cell Cycle Proteins; C412839:MDF-1 protein, C elegans; D064246:Mad2 Proteins; D009687:Nuclear Proteins; C000599595:PCH-2 protein, C elegans; D034741:RNA, Small Interfering; D018160:Receptors, Cytoplasmic and Nuclear; C514114:sun-1 protein, C elegans; C586892:DLC-1 protein, C elegans; D004398:Dyneins