A non-pheromone GPCR is essential for meiosis and ascosporogenesis in the wheat scab fungus.

Abstract

Meiosis is essential for generating genetic diversity and sexual spores, but the regulation of meiosis and ascosporogenesis is not clear in filamentous fungi, in which dikaryotic and diploid cells formed inside fruiting bodies are not free living and independent of pheromones or pheromone receptors. In this study, Gia1, a non-pheromone GPCR (G protein-coupled receptor) with sexual-specific expression in <i>Fusarium graminearum</i>, is found to be essential for ascosporogenesis. The <i>gia1</i> mutant was normal in perithecium development, crozier formation, and karyogamy but failed to undergo meiosis, which could be partially rescued by a dominant active mutation in <i>GPA1</i> and activation of the Gpmk1 pathway. <i>GIA1</i> orthologs have conserved functions in regulating meiosis and ascosporogenesis in Sordariomycetes. <i>GIA1</i> has a paralog, <i>GIP1</i>, in <i>F. graminearum</i> and other Hypocreales species which is essential for perithecium formation. <i>GIP1</i> differed from <i>GIA1</i> in expression profiles and downstream signaling during sexual reproduction. Whereas the C-terminal tail and IR3 were important for intracellular signaling, the N-terminal region and EL3 of Gia1 were responsible for recognizing its ligand, which is likely a protein enriched in developing perithecia, particularly in the <i>gia1</i> mutant. Taken together, these results showed that <i>GIA1</i> encodes a non-pheromone GPCR that regulates the entry into meiosis and ascosporogenesis via the downstream Gpmk1 MAP kinase pathway in <i>F. graminearum</i> and other filamentous ascomycetes.