CPEB proteins control two key steps in spermatogenesis in C-elegans

Cytoplasmic polyadenylation element binding (CPEB) proteins bind to and reg ulate the translation of specific mRNAs. CPEBs from Xenopus, Drosophila, an d Spisula participate in oogenesis. In this report, we examine the biologic al roles of all identifiable CPEB homologs in a single organism, Caenorhabd itis elegans. We find four homologs in the C. elegans genome: cbp-1, cpb-2, cpb-3, and fog-1. Surprisingly, two homologs, CPB-1 and FOG-1, have key fu nctions in spermatogenesis and are dispensable for oogenesis. CPB-2 and CPB -3 also appear not to be required for oogenesis. CPB-1 is essential for pro gression through meiosis: cpb-1(RNAi) spermatocytes fail to undergo the mei otic cell divisions. CPB-1 protein is present in the germ line just prior t o overt spermatogenesis; once sperm differentiation begins, CPB-1 disappear s. CPB-1 physically interacts with EBF, another RNA-binding protein and 3' UTR regulator. In addition to its role in controlling the sperm/oocyte swit ch, we find that EBF also appears to be required for spermatogenesis, consi stent with its interaction with CPEB. A second CPEB homolog, FOG-I, is requ ired for specification of the sperm fate. The fog-1 gene produces fog-1(L) and fog-1(S) transcripts. The fog-1(L) RNA is enriched in animals making sp erm and is predicted to encode a larger protein; fog-1(S) RNA is enriched i n animals making oocytes and is predicted to encode a smaller protein. The relative abundance of the two mRNAs is controlled temporally during germ-li ne development and by the sex determination pathway in a fashion that sugge sts that the fog-1(L) species encodes the active form. In sum, our results demonstrate that, in C. elegans, two CPEB proteins have distinct functions in the germ line, both in spermatogenesis: FOG-1 specifies the sperm cell f ate and CPB-1 executes that decision.