Department of Plant Biology, Michigan State University, East Lansing, Michigan, USA.
Department of Biostatistics, Yale University, New Haven, Connecticut, USA.
mBio. 2018 Aug 14;9(4):e01292-18. doi: 10.1128/mBio.01292-18.
Long 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 , 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. is the causal agent of the head blight on our major staple crops, wheat and corn. The fruiting body formation on the host plants is indispensable for the disease cycle and epidemics. Long noncoding RNA (lncRNA) molecules are emerging as key regulatory components for sexual development in animals and plants. To date, however, there is a paucity of information on the roles of lncRNAs in fungal fruiting body formation. Here we characterized hundreds of lncRNAs that exhibited developmental stage-specific expression patterns during fruiting body formation. Also, we discovered that many lncRNAs were induced in parallel with their overlapping transcripts on the opposite DNA strand during sexual development. Finally, we found a subset of lncRNAs that were regulated by an RNA surveillance system during vegetative growth. This research provides fundamental genomic resources that will spur further investigations on lncRNAs that may play important roles in shaping fungal fruiting bodies.
长非编码 RNA（lncRNA）在真核生物的性发育中发挥重要作用。然而，在丝状真菌中，关于 lncRNA 在子实体形成过程中的表达和作用知之甚少。通过对植物病原真菌生命周期中发育转录组进行分析，我们鉴定出 547 个 lncRNA，其表达高度动态，约 40%在减数分裂阶段达到峰值。许多 lncRNA 与 mRNA 反义，形成 300 个正义-反义对。尽管这些重叠基因座上产生了小 RNA，但反义 lncRNA 似乎不参与基因沉默途径。全基因组小 RNA 簇分析鉴定出许多减数分裂阶段沉默的基因座。然而，我们发现转录活跃的小 RNA 簇，其中许多与 lncRNA 相关。此外，我们观察到许多反义 lncRNA 及其相应的有义转录物在子实体成熟时平行诱导。无意义介导的衰变（NMD）途径决定 lncRNA 以及 mRNA 的命运。因此，我们分析了 NMD 缺陷突变体，并鉴定出一小部分 lncRNA 在有性发育过程中被诱导，但在营养生长过程中被 NMD 抑制。这些结果突出了 lncRNA 表达在塑造真菌子实体方面的发育阶段特异性和功能潜力，并为研究有性阶段诱导的 lncRNA 提供了基础资源。是我们主要主食作物小麦和玉米上的赤霉病的病原体。在宿主植物上形成子实体对于疾病周期和流行至关重要。长非编码 RNA（lncRNA）分子作为动植物有性发育的关键调节成分而出现。然而，迄今为止，关于 lncRNA 在真菌子实体形成中的作用的信息很少。在这里，我们描述了数百个在子实体形成过程中表现出发育阶段特异性表达模式的 lncRNA。此外，我们发现许多 lncRNA 在有性发育过程中与其在相反 DNA 链上的重叠转录物平行诱导。最后，我们发现一小部分 lncRNA 受营养生长过程中 RNA 监测系统的调节。这项研究提供了基础基因组资源，将进一步推动对可能在塑造真菌子实体中发挥重要作用的 lncRNA 的研究。
