Genome-wide exonic small interference RNA-mediated gene silencing regulates sexual reproduction in the homothallic fungus <i>Fusarium graminearum</i>

다국어 초록 (Multilingual Abstract)

<▼1><P>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 <I>Fusarium graminearum</I>. 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 <I>Fg</I>Dicer1 and <I>Fg</I>Ago2, while the constitutively expressed RNAi components <I>Fg</I>Dicer2 and <I>Fg</I>Ago1 are responsible for hairpin-induced RNAi. Based on our results, we concluded that <I>F</I>. <I>graminearum</I> 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.</P></▼1><▼2><P><B>Author summary</B></P><P>Control of gene expression by small noncoding RNA (sRNA) has recently been highlighted as a significant post-transcriptional regulatory mechanism. To date, researchers have predominantly focused on the identification of microRNA-like RNAs (milRNAs) in fungi because microRNAs (miRNAs) are key regulators in animals and plants. In this study, we discovered that the sex-induced RNA interference (RNAi) mechanism had important roles in sexual reproduction in the head blight fungus <I>Fusarium graminearum</I>. In the late stages of sexual reproduction, small interference RNAs that were produced from gene regions (ex-siRNAs) were involved in post-transcriptional gene regulation at a genome-wide level. Based on our results, we concluded that <I>F</I>. <I>graminearum</I> specifically utilizes ex-siRNA-mediated RNAi for sexual development but not for other biological processes. This is the first genome-wide characterization of the sRNAs involved in fungal development.</P></▼2>