In most sexually reproducing animals, oocytes arrest in meiotic prophase and resume meiosis (meiotic maturation) in response to intercellular signals. In C. elegans, fully-grown oocytes arrest at diakinesis of meiotic prophase I in the absence of sperm. Sperm trigger release from meiotic arrest using the major sperm protein (MSP) as a signal. MSP signaling activates the conserved mitogen-activated protein kinase (MAPK) pathway in oocytes and promotes diverse meiotic responses, including M-phase entry, cortical cytoskeletal rearrangement, and gonadal sheath cell contraction. We took a genetic approach to define new regulators of the MSP signaling pathway and isolated a strong dominant mutant in the
std-1 (stuck in diakinesis) locus.
std-1(
tn691d,ts) animals exhibit maternal- and paternal-effect embryonic lethality and sterility and have a Him phenotype at permissive temperatures. The mechanisms that maintain the spatial and temporal organization of meiotic maturation are unknown, but may involve
std-1 function. In
std-1(
tn691d,ts) animals, oocytes accumulate distal to the loop region. We observe evidence of ectopic meiotic maturation, with distal oocytes undergoing apparent cortical rearrangement at high peneterance and nuclear envelope breakdown at low penetrance. Ovulation occurs with reduced rates in
std-1(
tn691d,ts) mutants, whereas basal sheath cell contraction rates are significantly elevated.
std-1(
tn691d,ts) affects the signal dependence and responsiveness of MAPK activation. In the wild type, MSP signaling activates MAPK in the most proximal one to three oocytes. In
std-1(
tn691d,ts), not only the most proximal three but also distal oocytes display MAPK activation. Moreover, in
std-1(
tn691d,ts);
fog-2(
q71) females, MAPK activation is frequently observed in oocytes, and is thus independent from the MSP signal. Similarly, localization of Aurora B family kinase AIR-2 to condensed chromosomes in the most proximal oocyte is sperm dependent (Schumacher et al., 1998). This localization extends to two to three proximal oocytes in
std-1(
tn691d,ts) animals, and is also observed in the most proximal oocyte in
std-1(
tn691d,ts);
fog-2(
q71) females. The positional cloning of
std-1(
tn691d,ts) indicates that it corresponds to
cgh-1 (C07H6.5), which belongs to a highly conserved small subfamily of DEAD-box RNA helicases associated with germline development in diverse organisms (Navarro et al., 2001). Analysis of a recessive sterile deletion allele,
cgh-1/std-1
(ok492) (a deletion including the DEAD-box), suggests that cgh/std-1
(tn691d,ts) has dominant-negative character.