S. pombe wtf drivers use dual transcriptional regulation and selective protein exclusion from spores to cause meiotic drive

• Published in: PLoS genetics Vol. 18; no. 12; p. e1009847
• Main Authors: Nuckolls, Nicole L, Nidamangala Srinivasa, Ananya, Mok, Anthony C, Helston, Rachel M, Bravo Núñez, María Angélica, Lange, Jeffrey J, Gallagher, Todd J, Seidel, Chris W, Zanders, Sarah E
• Format: Journal Article
• Language: English
• Published: United States Public Library of Science 07.12.2022; Public Library of Science (PLoS)
• Subjects: Automobile drivers; Biology and Life Sciences; Fertility; Gametogenesis; Gene expression; Gene regulation; Genes; Genetic aspects; Genetic regulation; Genetic research; Genetic transcription; Heterozygotes; Infertility; Localization; Medicine and Health Sciences; Meiosis; Meiotic drive; Microscopy; Proteins; Research and Analysis Methods; Schizosaccharomyces - genetics; Schizosaccharomyces pombe Proteins - genetics; Sperm; Spores; Spores, Fungal - genetics; Transcription Factors - genetics; Yeast; United States
• ISSN: 1553-7404; 1553-7390; 1553-7404
• DOI: 10.1371/journal.pgen.1009847

Meiotic drivers bias gametogenesis to ensure their transmission into more than half the offspring of a heterozygote. In Schizosaccharomyces pombe, wtf meiotic drivers destroy the meiotic products (spores) that do not inherit the driver from a heterozygote, thereby reducing fertility. wtf drivers encode both a Wtfpoison protein and a Wtfantidote protein using alternative transcriptional start sites. Here, we analyze how the expression and localization of the Wtf proteins are regulated to achieve drive. We show that transcriptional timing and selective protein exclusion from developing spores ensure that all spores are exposed to Wtf4poison, but only the spores that inherit wtf4 receive a dose of Wtf4antidote sufficient for survival. In addition, we show that the Mei4 transcription factor, a master regulator of meiosis, controls the expression of the wtf4poison transcript. This transcriptional regulation, which includes the use of a critical meiotic transcription factor, likely complicates the universal suppression of wtf genes without concomitantly disrupting spore viability. We propose that these features contribute to the evolutionary success of the wtf drivers.