During oogenesis the germline nuclei synthesise at least two distinct mRNA populations; one required for immediate germ cell functions, and another for late oocyte and early zygote development. To study this division, we mapped the pathway of transcriptome separation through changes to mRNA poly(A)-tail length-distributions. By comparing the adenylation-state of adult
gld-2(
q497) and wild type transcriptomes, we identified more than 1000 targets of GLD-2 mediated cytoplasmic polyadenylation through statistically significant changes in their steady-state polyadenylation. Among the mRNA with the most significant change in poly(A) length-distributions were those encoding RNA binding proteins, such as
mex-5,
pos-1 and
oma-1, known to regulate spatial and temporal patterning of embryonic programs. The 3'UTR of mRNAs that depend on cytoplasmic polyadenylation were overall longer, showed enrichment of non-standard adenylation-sites (eg AAUGAA) and contained more cytosine residues. To identify the initiating deadenylase responsible for silencing mRNA, we depleted the five known deadenylases in the
gld-2 mutant by RNAi. Only, the loss of
ccf-1 suppressed the short-tailed phenotype of GLD-2 target mRNA, suggesting that in addition to its general role in RNA turnover, this is the major silencing deadenylase for the oocyte transcriptome. We present a model whereby the nuclei of the adult maternal germline are responsible for the transcription of at least two separate gene-expression programs: the 'ready-to-wear' transcriptome that sustains and builds the germ cells and oocytes and the 'couture' line, selected, silenced and partitioned, waiting for specific cues for reactivation during oocyte maturation and early embryo development.