MPK-1 ERK signaling is important for several aspects of germline development such as pachytene progression, oocyte growth and differentiation, oocyte meiotic maturation and sex determination. While core components of the RAS/MAP kinase pathway function in these processes, downstream targets as well as upstream signals are not known. One possible downstream target of MPK-1 ERK signaling is RSK (
p90 ribosomal S6 kinases), which was among the first substrates of ERK to be discovered in vertebrate systems and has been proposed to be a widespread mediator of ERK signaling. Database analysis identifies two C.elegans paralogous genes, T01H8.1 and C54G4.1, as being RSK homolog. We named these genes
rskn-1 and
rskn-2 respectively. Here we describe
rskn-1, which is the closest homolog of human RSK1. RSK proteins have N-terminal and C-terminal kinase domains and the allele
rskn-1(
ok159) deletes both and thus is likely a null mutation. The germline of
rskn-1(
ok159) is morphologically normal at all temperatures, although there is a low frequency Him phenotype (1.3%).
mpk-1(
ga111) is a temperature sensitive loss-of-function mutant that is essentially normal at 20C. The
rskn-1(
ok159);
mpk-1(
ga111) mutant is sterile at 20C, with small oocytes that are abnormally arranged in the proximal germline. RSKN-1 is efficiently phosphorylated by mammalian activated ERK2 in vitro consistent with results in vertebrate systems. Together, these results support the conclusion that RSKN-1 is positively regulated by MPK-1 ERK phosphorylation. In wild-type hermaphrodite germlines activated, di-phosphorylated, MPK-1 ERK is found in the last half of pachytene and in the most proximal 1 to 3 oocytes, with a low level in the intervening diplotene and diakinesis oocytes. In
rskn-1(
ok159) mutant hermaphrodites, high levels of activated MPK-1 ERK are found throughout diplotene and diakinesis indicating that RSKN-1 functions to down-regulate MPK-1 ERK activation. In wild-type females, activated MPK-1 ERK is not observed in the proximal gonad in the absence of the MSP sperm signal. In
rskn-1(
ok159) females, activated MPK-1 ERK is to a large extent absent, indicating that RSKN-1 mediated down-regulation of MPK-1 ERK activation is for the most part mediated by sperm signaling. The above results suggest that RSKN-1 functions in a sperm dependent negative feedback mechanism to down-regulate MPK-1 ERK activation in the proximal germline. Interestingly, in
rskn-1(
ok159) females a single late diplotene stage growing oocyte stains strongly for activated MPK-1 ERK. In this case, RSKN-1 may be acting in a sperm-independent manner to down-regulate MPK-1 ERK for oocyte growth control.