A-to-I mRNA editing controls spore death induced by a fungal meiotic drive gene in homologous and heterologous expression systems

J. M. Lohmar, N. A. Rhoades, T. N. Patel, R. H. Proctor, T. M. Hammond and D. W. Brown,  Genetics,  2022.

Spore killers are meiotic drive elements that can block development of sexual spores in fungi. In the maize ear rot and mycotoxin-producing fungus Fusarium verticillioides, a spore killer called SkK has been mapped to a 102-kb interval of chromosome V. Here, we show that a gene within this interval, SKC1, is required for SkK-mediated spore killing and meiotic drive. We also demonstrate that SKC1 is associated with at least four transcripts, two sense (sense-SKC1a and sense-SKC1b) and two antisense (antisense-SKC1a and antisense-SKC1b). Both antisense SKC1 transcripts lack obvious protein-coding sequences and thus appear to be non-coding RNAs. In contrast, sense-SKC1a is a protein-coding transcript that undergoes A-to-I editing to sense-SKC1b in sexual tissue. Translation of sense-SKC1a produces a 70 amino acid protein (Skc1a), whereas translation of sense-SKC1b produces an 84 amino acid protein (Skc1b). Heterologous expression analysis of SKC1 transcripts shows that sense-SKC1a also undergoes A-to-I editing to sense-SKC1b during the Neurospora crassa sexual cycle. Site directed mutagenesis studies indicate that Skc1b is responsible for spore killing in F. verticillioides and that it induces most meiotic cells to die in N. crassa. Finally, we report that SKC1 homologs are present in over 20 Fusarium species. Overall, our results demonstrate that fungal meiotic drive elements like SKC1 can influence the outcome of meiosis by hijacking a cell’s A-to-I editing machinery and that the involvement of A-to-I editing in a fungal meiotic drive system does not preclude its horizontal transfer to a distantly related species.

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