A ZYG-12-dynein interaction at the nuclear envelope defines cytoskeletal architecture in the C. elegans gonad.
Changes in cellular microtubule organization often accompany developmental progression. In the Caenorhabditis elegans embryo, the centrosome, which is attached to the nucleus via ZYG-12, organizes the microtubule network. In this study, we investigate ZYG-12 function and microtubule organization before embryo formation in the gonad. Surprisingly, ZYG-12 is dispensable for centrosome attachment in the germline. However, ZYG-12-mediated recruitment of dynein to the nuclear envelope is required to maintain microtubule organization, membrane architecture, and nuclear positioning within the syncytial gonad. We examined gamma-tubulin localization and microtubule regrowth after depolymerization to identify sites of nucleation in germ cells. gamma-Tubulin localizes to the plasma membrane in addition to the centrosome, and regrowth initiates at both sites. Because we do not observe organized microtubules around zyg-12(ct350) mutant nuclei with attached centrosomes, we propose that gonad architecture, including membrane and nuclear positioning, is determined by microtubule nucleation at the plasma membrane combined with tension on the microtubules by dynein anchored at the nucleus by ZYG-12.
Zhou
Kang
K
Department of Biochemistry and Molecular Biology, The Pennsylvania State University, University Park, PA 16802, USA.
Rolls
Melissa M
MM
Hall
David H
DH
Malone
Christian J
CJ
Hanna-Rose
Wendy
W
D000818:Animals; D017173:Caenorhabditis elegans / Q000166:cytology / Q000196:embryology; D029742:Caenorhabditis elegans Proteins / Q000235:genetics / Q000378:metabolism*; D018797:Cell Cycle Proteins / Q000235:genetics / Q000378:metabolism*; D002462:Cell Membrane / Q000378:metabolism; D002467:Cell Nucleus / Q000378:metabolism / Q000648:ultrastructure; D018385:Centrosome / Q000378:metabolism; D003599:Cytoskeleton / Q000378:metabolism*; D004398:Dyneins / Q000235:genetics / Q000378:metabolism*; D005854:Germ Cells / Q000166:cytology / Q000502:physiology; D006066:Gonads / Q000166:cytology / Q000378:metabolism; D008870:Microtubules / Q000378:metabolism / Q000648:ultrastructure; D009685:Nuclear Envelope / Q000378:metabolism* / Q000648:ultrastructure; D009866:Oogenesis / Q000502:physiology; D011993:Recombinant Fusion Proteins / Q000235:genetics / Q000378:metabolism; D014404:Tubulin / Q000235:genetics / Q000378:metabolism; D020798:Two-Hybrid System Techniques
D029742:Caenorhabditis elegans Proteins; D018797:Cell Cycle Proteins; D011993:Recombinant Fusion Proteins; D014404:Tubulin; C480800:zyg-12 protein, C elegans; D004398:Dyneins