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

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 t...

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Bibliographic Details
Published in:Genetics (Austin) 2022-05, Vol.221 (1)
Main Authors: Lohmar, Jessica M, Rhoades, Nicholas A, Patel, Tejas N, Proctor, Robert H, Hammond, Thomas M, Brown, Daren W
Format: Article
Language:English
Subjects:
Amino acids
Chromosome 5
Ear rot
Editing
Fungi
Fusarium
Fusarium - genetics
Fusarium verticillioides
Genes, Fungal
Genetics
Homology
Horizontal transfer
Investigation
Meiosis
Meiosis - genetics
Meiotic drive
Mycotoxins
Neurospora
Neurospora crassa
Neurospora crassa - genetics
Non-coding RNA
Proteins
RNA editing
RNA, Messenger
Site-directed mutagenesis
Spores
Spores, Fungal - genetics
Translation
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Summary: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.
ISSN:1943-2631
0016-6731
1943-2631
DOI:10.1093/genetics/iyac029