Identification ofrfk-1, a Meiotic Driver Undergoing RNA Editing inNeurospora

Abstract

Sk-2 is a meiotic drive element that was discovered in wild populations of Neurospora fungi over 40 years ago. While early studies quickly determined that Sk-2 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 rfk-1, a gene required for Sk-2-based spore killing. The rfk-1 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 rfk-1 transcript in vegetative tissue is expected to produce a 102-amino acid protein, whereas translation of an edited rfk-1 transcript in sexual tissue is expected to produce a protein with 130 amino acids. These findings indicate that unedited and edited rfk-1 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 rfk-1 transcripts avoid silencing caused by a genome defense process called meiotic silencing by unpaired DNA (MSUD). We show that rfk-1's MSUD avoidance mechanism is linked to the genomic landscape surrounding the rfk-1 gene, which is located near the Sk-2 border on the right arm of chromosome III. In addition to demonstrating that the location of rfk-1 is critical to spore-killing success, our results add to accumulating evidence that MSUD helps protect Neurospora genomes from complex meiotic drive elements.

The wtf4 meiotic driver utilizes controlled protein aggregation to generate selective cell death

“…The Wtf4 poison forms distributed toxic aggregates and the Wtf4 antidote co-assembles with the Wtf4 poison and neutralizes the aggregate’s toxicity via trafficking to the vacuole ( Figure 6 ). This mechanism is unlike the mechanism of any other meiotic driver described to date ( Grognet et al, 2014 ; Didion et al, 2015 ; Long et al, 2008 ; Dawe et al, 2018 ; Rhoades et al, 2019 ; Dalstra et al, 2005 ; Hammond et al, 2012 ; Vogan et al, 2019 ; Chen et al, 2008 ; Akera et al, 2017 ; Bauer et al, 2012 ; Pieper et al, 2018 ; Herrmann et al, 1999 ; Shen et al, 2017 ; Yu et al, 2018 ; Bauer et al, 2007 ; Wu et al, 1988 ; Xie et al, 2019 ; Kruger et al, 2019 ; Lin et al, 2018 ; Svedberg et al, 2020 ), but there are very few mechanistically characterized killer meiotic drive systems (reviewed in Bravo Núñez et al, 2018b ).…”

Dramatically diverse Schizosaccharomyces pombe wtf meiotic drivers all display high gamete-killing efficiency

“…Our current work shows that many of these predicted drive genes are able to drive in the right genetic context. This work expands the rapidly growing number of bona fide drive genes identified in recent years [4,[16][17][18][33][34][35][36][37][38][39][40][41][42][43].…”

Atypical meiosis can be adaptive in outcrossedS. pombedue towtfmeiotic drivers

“…A growing body of evidence indicates that meiotic drive is pervasive in eukaryotes, and more drivers are identified each year. This includes the gamete-killing type of meiotic drivers described in this work (Bauer et al, 2012; Bravo Núñez et al, 2018; Bravo Núñez et al, 2020; Burt and Trivers 2006; Didion et al, 2015; Grognet et al, 2014; Hammond et al, 2012; Hu et al, 2017; Larracuente and Presgraves 2012; Long et al, 2008; Nuckolls et al, 2017; Pieper et al, 2018; Rhoades et al, 2019; Vogan et al, 2019; Xie et al, 2019; Yang et al, 2012; Yu et al, 2018), but also extends to other drivers that use completely different methods to gain a transmission advantage. For example, biased gene conversion favoring unbroken DNA during meiotic recombination is a form of meiotic drive tied to the mechanisms of double-strand break repair (Marais 2003).…”