Developmental Dynamics of Long Noncoding RNA Expression during Sexual Fruiting Body Formation in Fusarium graminearum.

Wonyong Kim,Jie Wang,Frances Trail,Cristina Miguel-Rojas,Jeffrey P Townsend,Antonio Di Pietro

doi:10.1128/mbio.01292-18

Abstract

ABSTRACTLong noncoding RNA (lncRNA) plays important roles in sexual development in eukaryotes. In filamentous fungi, however, little is known about the expression and roles of lncRNAs during fruiting body formation. By profiling developmental transcriptomes during the life cycle of the plant-pathogenic fungus Fusarium graminearum, we identified 547 lncRNAs whose expression was highly dynamic, with about 40% peaking at the meiotic stage. Many lncRNAs were found to be antisense to mRNAs, forming 300 sense-antisense pairs. Although small RNAs were produced from these overlapping loci, antisense lncRNAs appeared not to be involved in gene silencing pathways. Genome-wide analysis of small RNA clusters identified many silenced loci at the meiotic stage. However, we found transcriptionally active small RNA clusters, many of which were associated with lncRNAs. Also, we observed that many antisense lncRNAs and their respective sense transcripts were induced in parallel as the fruiting bodies matured. The nonsense-mediated decay (NMD) pathway is known to determine the fates of lncRNAs as well as mRNAs. Thus, we analyzed mutants defective in NMD and identified a subset of lncRNAs that were induced during sexual development but suppressed by NMD during vegetative growth. These results highlight the developmental stage-specific nature and functional potential of lncRNA expression in shaping the fungal fruiting bodies and provide fundamental resources for studying sexual stage-induced lncRNAs.

Highlights

Long noncoding RNA plays important roles in sexual development in eukaryotes
The nuclear exosome is engaged in RNA processing and degradation of transcripts, including Long noncoding RNA (lncRNA) that are expressed during sexual sporulation; the deletion of RRP6 encoding the exosome-associated exonuclease resulted in the accumulation of noncoding transcripts that otherwise remained silenced during vegetative growth [17,18,19]
This study has revealed global properties of lncRNAs during perithecial development, characterized by dynamic and developmental stage-specific expression

Summary

Introduction

Long noncoding RNA (lncRNA) plays important roles in sexual development in eukaryotes. A promoter-derived lncRNA suppresses the expression of IME1 (inducer of meiosis 1), the master regulator for the sexual sporulation, by inducing heterochromatin formation in the promoter region of IME1 during vegetative growth [10]. There is no such conserved or analogous regulatory mechanism in fission yeast, lncRNAs play diverse roles in sexual sporulation: for example, sequestering RNA elimination factors that repress meiotic gene expression [13,14,15] and contributing to homologous chromosome pairing [16]. The nuclear exosome is engaged in RNA processing and degradation of transcripts, including lncRNAs that are expressed during sexual sporulation; the deletion of RRP6 encoding the exosome-associated exonuclease resulted in the accumulation of noncoding transcripts that otherwise remained silenced during vegetative growth [17,18,19]. Subsets of lncRNAs found in budding yeast, the model plant Arabidopsis, and animals are subject to degradation through the NMD pathway [23,24,25]

Objectives

Methods

Results

Conclusion