Adaptive Spo11 RNA editing gate optimizes meiosis I pace and mitotic proliferation while preserving ascospore formation.

Spo11-mediated DNA double-strand breaks (DSBs) are essential for meiotic recombination, yet how Spo11 activity is temporally regulated during mitosis and fungal development remains unclear. In the fungal plant pathogen Fusarium graminearum, we found that FgSpo11 has a DSB-independent role delaying meiosis I and a DSB-dependent role critical for postmeiotic mitoses during ascosporogenesis. Loss of FgSpo11 accelerates meiosis I and causes excessive postmeiotic divisions, ultimately causing aborted ascospores. A premature stop codon (TAG) is corrected to tryptophan (TGG) by adenosine-to-inosine RNA editing exclusively during sexual reproduction, enabling full-length protein synthesis. A genomically "corrected" allele bypassing this editing preserves ascospore formation but causes meiotic and vegetative mitotic defects. Beyond its on-switch function, this editing acts as a tunable rheostat fine-tuning FgSpo11 dosage during meiosis. Evolutionary analyses reveal recurrent gain and loss of this editing, highlighting adaptive modulation of Spo11 deployment. This study uncovers a single-site RNA editing gate controlling a key meiotic regulator and illustrates transcriptome plasticity in reconciling life cycle demands in eukaryotic pathogens.