Hyphal editing of the conserved premature stop codon in CHE1 is stimulated by oxidative stress in Fusarium graminearum

Abstract

Although genome-wide A-to-I editing mediated by adenosine-deaminase-acting-on-tRNA (ADAT) occurs during sexual reproduction in the presence of stage-specific cofactors, RNA editing is not known to occur during vegetative growth in filamentous fungi. Here we identified 33 A-to-I RNA editing events in vegetative hyphae of Fusarium graminearum and functionally characterized one conserved hyphal-editing site. Similar to ADAT-mediated editing during sexual reproduction, majority of hyphal-editing sites are in coding sequences and nonsynonymous, and have strong preference for U at -1 position and hairpin loops. Editing at TA⁴³⁷G, one of the hyphal-specific editing sites, is a premature stop codon correction (PSC) event that enables CHE1 gene to encode a full-length zinc fingertranscription factor. Manual annotations showed that this PSC site is conserved in CHE1 orthologs from closely-related Fusarium species. Whereas the che1 deletion and CHE1^TAA (G⁴³⁸ to A) mutants had no detectable phenotype, the CHE1^TGG (A⁴³⁷ to G) mutant was defective in hyphal growth, conidiation, sexual reproduction, and plant infection. However, the CHE1^TGG mutant was increased in tolerance against oxidative stress and editing of TA⁴³⁷G in CHE1 was stimulated by H₂O₂ treatment in F. graminearum. These results indicate that fixation of the premature stop codon in CHE1 has a fitness cost on normal hyphal growth and reproduction but provides a benefit to tolerance against oxidative stress. Taken together, A-to-I editing events, although rare (not genome-wide), occur during vegetative growth and editing in CHE1 plays a role in response to oxidative stress in F. graminearum and likely in other fungal pathogens.

Keywords: CHE1; ADAT-mediated mRNA editing; Editing during asexual reproduction; Hyphal editing; Tad2 and Tad3; mRNA editing.