Long noncoding RNAs emerge from transposon-derived antisense sequences and may contribute to infection stage-specific transposon regulation in a fungal phytopathogen.

IF 4.7 2区 生物学 Q1 GENETICS & HEREDITY Mobile DNA Pub Date : 2023-11-15 DOI:10.1186/s13100-023-00305-6
Jiangzhao Qian, Heba M M Ibrahim, Myriam Erz, Florian Kümmel, Ralph Panstruga, Stefan Kusch
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Abstract

Background: The genome of the obligate biotrophic phytopathogenic barley powdery mildew fungus Blumeria hordei is inflated due to highly abundant and possibly active transposable elements (TEs). In the absence of the otherwise common repeat-induced point mutation transposon defense mechanism, noncoding RNAs could be key for regulating the activity of TEs and coding genes during the pathogenic life cycle.

Results: We performed time-course whole-transcriptome shotgun sequencing (RNA-seq) of total RNA derived from infected barley leaf epidermis at various stages of fungal pathogenesis and observed significant transcript accumulation and time point-dependent regulation of TEs in B. hordei. Using a manually curated consensus database of 344 TEs, we discovered phased small RNAs mapping to 104 consensus transposons, suggesting that RNA interference contributes significantly to their regulation. Further, we identified 5,127 long noncoding RNAs (lncRNAs) genome-wide in B. hordei, of which 823 originated from the antisense strand of a TE. Co-expression network analysis of lncRNAs, TEs, and coding genes throughout the asexual life cycle of B. hordei points at extensive positive and negative co-regulation of lncRNAs, subsets of TEs and coding genes.

Conclusions: Our work suggests that similar to mammals and plants, fungal lncRNAs support the dynamic modulation of transcript levels, including TEs, during pivotal stages of host infection. The lncRNAs may support transcriptional diversity and plasticity amid loss of coding genes in powdery mildew fungi and may give rise to novel regulatory elements and virulence peptides, thus representing key drivers of rapid evolutionary adaptation to promote pathogenicity and overcome host defense.

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长非编码rna来自转座子衍生的反义序列,可能有助于真菌植物病原体感染阶段特异性转座子调控。
背景:专性生物营养性植物致病性大麦白粉病真菌Blumeria hordei的基因组由于高度丰富且可能活跃的转座因子(te)而膨胀。在缺乏其他常见的重复诱导点突变转座子防御机制的情况下,非编码rna可能是在致病性生命周期中调节TEs和编码基因活性的关键。结果:我们对真菌发病各阶段感染大麦叶表皮的总RNA进行了全转录组鸟枪测序(RNA-seq),观察到显著的转录积累和时间点依赖性的te调控。利用人工整理的344个te的共识数据库,我们发现了定位于104个共识转座子的阶段性小RNA,这表明RNA干扰对它们的调控起着重要作用。此外,我们鉴定出了5127个长链非编码rna (lncRNAs),其中823个来自TE的反义链。对白背蜂无性生命周期中lncRNAs、TEs和编码基因的共表达网络分析表明,lncRNAs、TEs亚群和编码基因存在广泛的正、负共调控。结论:我们的研究表明,与哺乳动物和植物类似,真菌lncRNAs在宿主感染的关键阶段支持转录物水平的动态调节,包括TEs。在白粉病真菌编码基因缺失的情况下,lncrna可能支持转录多样性和可塑性,并可能产生新的调控元件和毒力肽,因此代表了快速进化适应以促进致病性和克服宿主防御的关键驱动因素。
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来源期刊
Mobile DNA
Mobile DNA GENETICS & HEREDITY-
CiteScore
8.20
自引率
6.10%
发文量
26
审稿时长
11 weeks
期刊介绍: Mobile DNA is an online, peer-reviewed, open access journal that publishes articles providing novel insights into DNA rearrangements in all organisms, ranging from transposition and other types of recombination mechanisms to patterns and processes of mobile element and host genome evolution. In addition, the journal will consider articles on the utility of mobile genetic elements in biotechnological methods and protocols.
期刊最新文献
International congress on transposable elements (ICTE 2024) in Saint Malo: breaking down transposon waves and their impact. Accelerating de novo SINE annotation in plant and animal genomes. Association of hyperactivated transposon expression with exacerbated immune activation in systemic lupus erythematosus. Widespread HCD-tRNA derived SINEs in bivalves rely on multiple LINE partners and accumulate in genic regions. Correction: Transposon-derived introns as an element shaping the structure of eukaryotic genomes.
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