Identification of <i>rfk-1</i> , a Meiotic Driver Undergoing RNA Editing in <i>Neurospora</i>

Abstract

<i>Sk-2</i> is a meiotic drive element that was discovered in wild populations of <i>Neurospora</i> fungi over 40 years ago. While early studies quickly determined that <i>Sk-2</i> transmits itself through sexual reproduction in a biased manner via spore killing, the genetic factors responsible for this phenomenon have remained mostly unknown. Here, we identify and characterize <i>rfk-1</i>, a gene required for <i>Sk-2</i>-based spore killing. The <i>rfk-1</i> gene contains four exons, three introns, and two stop codons, the first of which undergoes RNA editing to a tryptophan codon during sexual development. Translation of an unedited <i>rfk-1</i> transcript in vegetative tissue is expected to produce a 102-amino acid protein, whereas translation of an edited <i>rfk-1</i> transcript in sexual tissue is expected to produce a protein with 130 amino acids. These findings indicate that unedited and edited <i>rfk-1</i> transcripts exist and that these transcripts could have different roles with respect to the mechanism of meiotic drive by spore killing. Regardless of RNA editing, spore killing only succeeds if <i>rfk-1</i> transcripts avoid silencing caused by a genome defense process called meiotic silencing by unpaired DNA (MSUD). We show that <i>rfk-1</i>'s MSUD avoidance mechanism is linked to the genomic landscape surrounding the <i>rfk-1</i> gene, which is located near the <i>Sk-2</i> border on the right arm of chromosome III. In addition to demonstrating that the location of <i>rfk-1</i> is critical to spore-killing success, our results add to accumulating evidence that MSUD helps protect <i>Neurospora</i> genomes from complex meiotic drive elements.