A-to-I RNA editing during sexual reproduction in filamentous ascomycetes

Fungi, like plants, do not have ADAR orthologs and are believed to lack A-to-I RNA editing, which is the prevalent mRNA editing in animals. However, genome-wide A-to-I editing occurs specifically during sexual reproduction in the wheat scab fungus Fusarium graminearum. Unlike those in animals, majority of A-to-I editing sites in F. graminearum occur in coding regions and over two-thirds of them result in amino acid changes, including editing of 69 pseudogenes with the UAG stop codon in their ORFs. Furthermore, F. graminearum differs from animals in the sequence-preference and structure-selectivity of editing sites. Genome-wide A-to-I editing also specifically occurs during sexual reproduction in Neurospora crassa, N. tetrasperma, and F. verticillioides. Some of the editing sites are conserved in these fungi and they may be functionally related to their stage-specific functions during ascus or ascospore development. Unlike in humans, RNA editing in fungi preferentially targets As in hairpin loops, which is similar to the anticodon loop of tRNA targeted by ADATs, and nonsynonymous editing events in fungi are generally beneficial and favored by positive selection. RNA editing occurred before ascus development but became prevalent during ascosporogenesis. Overall, our results indicate that A-to-I editing in fungi occurs specifically during sexual reproduction with ADAR-independent mechanisms, is generally adaptive, and may be functionally related to other stage specific genetic phenomena.