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

Abstract

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 <i>Fusarium graminearum</i>, 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.