RNA Pol I shapes meiotic chromatin, germline H3K4me3 dynamics, and oogenesis independent of ribosome assembly

Oogenesis requires extensive chromatin remodeling that primes promoters for embryonic transcription. We reveal a non-canonical role for RNA polymerase I (Pol I) in driving these transitions during Caenorhabditis elegans oogenesis. Using the auxin-inducible degron to deplete Pol I catalytic subunits or ribosome assembly factors, we separated nucleolar disruption from reduced ribosome assembly. Loss of ribosome assembly minimally affected oocyte number or morphology, whereas Pol I depletion led to broadly altered autosomal chromatin accessibility, reduced the distal-proximal H3K4me3 gradient, impaired synapsis, and increased ATM/ATR phosphorylation, yielding fewer but larger oocytes. Despite increased promoter accessibility, oogenesis genes changed little at steady-state mRNA, consistent with pre-fertilization transcription repression. Instead, Pol I depletion prematurely remodeled oogenic chromatin by misdirecting H3K4me3 to promoters normally primed for zygotic genome activation. These findings reveal an epigenetic gating function for nucleolar integrity: Pol I preserves chromatin organization and maintains proper histone-modification dynamics during oocyte maturation, independent of ribosome assembly.