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

  1. Cameron Luitjens1,
  2. Maria Gallegos1,4,6,
  3. Brian Kraemer2,5,6,
  4. Judith Kimble2,3, and
  5. Marvin Wickens2,7
  1. 1Program in Cell and Molecular Biology, 2Department of Biochemistry, and 3Howard Hughes Medical Institute, University of Wisconsin, Madison, Wisconsin 53706, USA

Abstract

Cytoplasmic polyadenylation element binding (CPEB) proteins bind to and regulate the translation of specific mRNAs. CPEBs fromXenopus, Drosophila, and Spisula participate in oogenesis. In this report, we examine the biological roles of all identifiable CPEB homologs in a single organism, Caenorhabditis 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 functions 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 progression through meiosis: cpb-1(RNAi) spermatocytes fail to undergo the meiotic cell divisions. CPB-1 protein is present in the germ line just prior to overt spermatogenesis; once sperm differentiation begins, CPB-1 disappears. CPB-1 physically interacts with FBF, another RNA-binding protein and 3′ UTR regulator. In addition to its role in controlling the sperm/oocyte switch, we find that FBF also appears to be required for spermatogenesis, consistent with its interaction with CPEB. A second CPEB homolog, FOG-1, is required for specification of the sperm fate. The fog-1 gene produces fog-1(L) and fog-1(S) transcripts. Thefog-1(L) RNA is enriched in animals making sperm and is predicted to encode a larger protein; fog-1(S) RNA is enriched in animals making oocytes and is predicted to encode a smaller protein. The relative abundance of the two mRNAs is controlled temporally during germ-line development and by the sex determination pathway in a fashion that suggests 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 fate and CPB-1 executes that decision.

Keywords

Footnotes

  • Present addresses: 4University of California, Department of Anatomy, San Francisco, CA 94143–0452, USA

  • 5 Seattle VA Medical Center, University of Washington, Seattle, WA 98108, USA.

  • 6 These authors contributed equally to this work.

  • 7 Corresponding author.

  • E-MAIL wickens{at}biochem.wisc.edu; FAX (608) 262-9108.

  • Article and publication are at www.genesdev.org/cgi/doi/10.1101/gad.831700.

    • Received July 5, 2000.
    • Accepted August 18, 2000.
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