Adenosine Deaminase Acting on RNA (ADAR) enzymes mediated adenosine-to-inosine (A-to-I) editing is the most prevalent post-transcriptional modification of RNA in animals. Organisms outside animal kingdom do not have ADAR orthologs and are believed to lack A-to-I RNA editing. However, we demonstrates genome-wide A-to-I RNA editing occurs in fungi specifically during sexual reproduction, involving adenosine deamination mechanisms distinct from animal ADARs. Genome-wide analysis identified 26,056 perithecium-specific A-to-I editing sites in Fusarium graminearum. Unlike those in animals, 70.5% of A-to-I editing sites in F. graminearum occur in coding regions, and more than two-thirds of them result in amino acid changes, including editing of 70 pseudogenes with stop codons in ORFs. F. graminearum differs from animals in the sequence preference and structure selectivity of A-to-I editing sites. Whereas A’s embedded in RNA stems are targeted by ADARs, RNA editing in F. graminearum preferentially targets A’s in hairpin loops, which is similar to the anticodon loop of tRNA targeted by adenosine deaminases acting on tRNA (ADATs). In addition, we also identified A-to-I RNA editing events in Neurospora crassa and F. verticillioides.
Overall, our study showed that A-to-I RNA editing occurs specifically during sexual reproduction and mainly in the coding regions in filamentous ascomycetes, involving adenosine deamination mechanisms distinct from metazoan ADARs. Our work provides important new information about gene and protein regulation in fungi and makes an important contribution to our understanding of RNA editing in eukaryotes.