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

Authors: Lohmar, Jessica; RHOADES, NICHOLAS - Illinois State University; PATEL, TEJAS - Illinois State University; Proctor, Robert; HAMMOND, THOMAS - Illinois State University; Brown, Daren

Submitted to: Genetics
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 2/6/2022
Publication Date: 2/15/2022
Citation: Lohmar, J.M., Rhoades, N.A., Patel, T.N., Proctor, R., Hammond, T.M., Brown, D.W. 2022. A-to-I mRNA editing controls spore death induced by a fungal meiotic drive gene in homologous and heterologous expression systems. Genetics. 221(1). Article iyac029. https://doi.org/10.1093/genetics/iyac029.
DOI: https://doi.org/10.1093/genetics/iyac029

Interpretive Summary: The fungal toxins fumonisins pose health hazards to humans and livestock because they frequently contaminate corn. The toxins can also negatively impact farmers because the contamination, which is caused primarily by the fumonisin-producing fungus Fusarium verticillioides, can markedly reduce the value of corn. ARS researchers in Peoria, Illinois, and their collaborators at Illinois State University have identified a naturally occurring F. verticillioides gene, called Spore Killer, that kills spores of the fungus that lack the gene. The researchers also found evidence that the gene has the same spore-killing effect when transferred to other fungi. Together, the results point to a novel method to reduce fumonisin contamination in corn using strains of F. verticillioides that have Spore Killer fused to a gene that blocks fumonisin production. Further, because the effect of Spore Killer is not limited to F. verticillioides, it has potential to control toxin contamination problems caused by other fungi. Thus, the results of this ARS research have potential to improve the safety of crops used for food and feed, and to reduce the negative financial impacts caused by toxin contamination.

Technical Abstract: Spore killers are meiotic drive elements that can block the 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 4 transcripts, 2 sense (sense-SKC1a and sense-SKC1b) and 2 antisense (antisense-SKC1a and antisense-SKC1b). Both antisense SKC1 transcripts lack obvious protein-coding sequences and thus appear to be noncoding 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 the 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 Fusarium verticillioides and that it induces most meiotic cells to die in Neurospora 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.