Poly(U) polymerase activity promotes establishment of primordial germ cells and limits somatic PGL granules in the Caenorhabditis elegans embryo.

Terminal uridylyl transferases/poly(U) polymerases (PUPs) promote animal development. Under conditions of temperature stress, Caenorhabditis elegans PUP-1 and the partially redundant PUP-2 ensure development of the larva/adult germline and embryonic viability. Using high-throughput RNA sequencing, we characterized the transcriptomes of adult hermaphrodites and early embryos lacking PUP-1, PUP-2, or both. Transcripts with altered abundance included those expressed in various somatic tissues or the germline, including neuronal and spermatogenic mRNAs. For some transcripts, abundance was altered only in the absence of both PUP-1 and PUP-2, indicating redundancy. In embryos, some maternally provided and zygotically synthesized mRNAs are elevated, especially in the absence of PUP-2. In the early embryo, PUP-1 promotes division of the germline founder cell (P4), and division failure correlates with adult sterility. PUP-1 promotes the accumulation of PGL-1 in P granules and limits accumulation of somatic PGL-1 foci. Somatic PGL granules are normally cleared by autophagy; loss of PUP-1 does not appear to impair autophagy and instead PGL-1 foci may be more stable due to a change in RNA stability. This work establishes roles for PUPs in early embryonic development that carry forward to adulthood.