Centralspindlin promotesC. elegansanchor cell specification, vulva induction and morphogenesis

ABSTRACT Caenorhabditis elegans vulval development is a relatively simple model of organ development whereby a signal from the overlying gonad induces three epithelial cells to undergo three rounds of cell division to generate 22 cells that make up the vulva. Specification of the vulva cell fates requires coordination between cell division and cell signaling via LIN-12/Notch and LET-23/EGFR pathways in the somatic gonad and the underlying epithelium. Here we characterize the positive regulation of vulval development by the centralspindlin complex, a conserved cytokinesis regulator. Centralspindlin, a heterotetramer of ZEN-4/KIF23 and CYK-4/RacGAP1, is essential for completion of cytokinesis during early embryonic cell divisions. We found that centralspindlin is required in the somatic gonad for division of somatic gonad precursor cells and hence specification of the LIN-3/EGF-secreting anchor cell critical for LET-23/EGFR-mediated vulval induction. However, the requirements for centralspindlin for cytokinesis during postembryonic development are incomplete as a binucleate anchor cell is frequently specified. The presence of the binucleate anchor cell correlates with vulva induction and demonstrates that LIN-12/Notch signaling, required for anchor cell specification, and LET-23/EGFR signaling, required for vulva induction, is largely functional in these cells. Centralspindlin is also partially required for cytokinesis of the vulval cells where it regulates vulva morphogenesis rather than induction. We also found that the GAP domain of CYK-4/RacGAP1 required for contractile ring assembly during embryonic division is not essential for vulval development. Thus, there appears to be different requirements for centralspindlin during postembryonic development of the somatic gonad and vulva as compared to early embryogenesis.