Abstract
Various ascomycete fungi possess sex-specific molecular mechanisms, such as repeat-induced point mutations, meiotic silencing by unpaired DNA, and unusual adenosine-to-inosine RNA editing, for genome defense or gene regulation. Using a combined analysis of functional genetics and deep sequencing of small noncoding RNA (sRNA), mRNA, and the degradome, we found that the sex-specifically induced exonic small interference RNA (ex-siRNA)-mediated RNA interference (RNAi) mechanism has an important role in fine-tuning the transcriptome during ascospore formation in the head blight fungus Fusarium graminearum. Approximately one-third of the total sRNAs were produced from the gene region, and sRNAs with an antisense direction or 5′-U were involved in post-transcriptional gene regulation by reducing the stability of the corresponding gene transcripts. Although both Dicers and Argonautes partially share their functions, the sex-specific RNAi pathway is primarily mediated by FgDicer1 and FgAgo2, while the constitutively expressed RNAi components FgDicer2 and FgAgo1 are responsible for hairpin-induced RNAi. Based on our results, we concluded that F. graminearum primarily utilizes ex-siRNA-mediated RNAi for ascosporogenesis but not for genome defenses and other developmental stages. Each fungal species appears to have evolved RNAi-based gene regulation for specific developmental stages or stress responses. This study provides new insights into the regulatory role of sRNAs in fungi and other lower eukaryotes.
Highlights
The ascomycete fungus Fusarium graminearum is a major causative agent of Fusarium head blight (FHB) in small-grain cereals worldwide [1]
Researchers have predominantly focused on the identification of microRNA-like RNAs in fungi because microRNAs are key regulators in animals and plants
Whereas both sense and antisense small noncoding RNA (sRNA) produced below 100 counts per kilobase did not show substantial changes in transcript levels of the corresponding genes, most genes producing antisense sRNAs at more than 1000 counts per kilobase were positively regulated in Fgdicer1 Fgdicer2 and Fgago1 Fgago2 compared to those in the wild type (Fig 5D). Both sense and antisense 50 end with U (50-U) sRNA (22–25 nt)-producing genes showed similar results to those obtained from antisense sRNAs (S4 Fig). These findings show that a sRNA-mediated gene regulatory mechanism is not a critical factor that determines final transcript levels of most genes, but highly expressed sRNAs with antisense orientations participate in the negative transcriptional gene regulation of corresponding genes at a genome-wide level
Summary
The ascomycete fungus Fusarium graminearum is a major causative agent of Fusarium head blight (FHB) in small-grain cereals worldwide [1]. The fungus reproduces using sexual spores (ascospores) and asexual spores (conidia). Both spore types contribute to disease initiation and propagation, ascospores serve as the primary inocula for FHB outbreaks because these spores are forcibly discharged into the air and can move long distances [2]. The sexual development process ensures the production of survival structures required for overwintering [3] and the genetic diversity of the population [4]; understanding the molecular mechanisms underlying F. graminearum sexual reproduction is important for developing novel FHB disease-control strategies. Perithecia (fruiting bodies) produced via sexual reproduction have complex multicellular structures with three distinguishable layers [5]. Many upstream signal transduction pathways and hundreds of signaling mediators, such as transcription factors and kinases, orchestrate sexual reproduction in F. graminearum [9,10,11]
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