The Puf RNA-binding proteins FBF-1 and FBF-2 inhibit the expression of synaptonemal complex proteins in germline stem cells

Abstract

FBF-1 and FBF-2 (collectively FBF) are two nearly identical Puf-domain RNA-binding proteins that regulate the switch from mitosis to meiosis in the C. elegans germline. In germline stem cells, FBF prevents premature meiotic entry by inhibiting the expression of meiotic regulators, such as the RNA-binding protein GLD-1. Here, we demonstrate that FBF also directly inhibits the expression of structural components of meiotic chromosomes. HIM-3, HTP-1, HTP-2, SYP-2 and SYP-3 are components of the synaptonemal complex (SC) that forms between homologous chromosomes during meiotic prophase. In wild-type germlines, the five SC proteins are expressed shortly before meiotic entry. This pattern depends on FBF binding sites in the 3′ UTRs of the SC mRNAs. In the absence of FBF or the FBF binding sites, SC proteins are expressed precociously in germline stem cells and their precursors. SC proteins aggregate and SC formation fails at meiotic entry. Precocious SC protein expression is observed even when meiotic entry is delayed in fbf mutants by reducing GLD-1. We propose that parallel regulation by FBF ensures that in wild-type gonads, meiotic entry is coordinated with just-in-time synthesis of synaptonemal proteins.