Zheng Yi, Wang Ying, Ding Biao, Fei Zhangjun
Boyce Thompson Institute, Cornell University, Ithaca, New York, USA.
Department of Molecular Genetics, The Ohio State University, Columbus, Ohio, USA
J Virol. 2017 May 12;91(11). doi: 10.1128/JVI.00247-17. Print 2017 Jun 1.
Many pathogens express noncoding RNAs (ncRNAs) during infection processes. In the most extreme case, pathogenic ncRNAs alone (such as viroids) can infect eukaryotic organisms, leading to diseases. While a few pathogenic ncRNAs have been implicated in regulating gene expression, the functions of most pathogenic ncRNAs in host-pathogen interactions remain unclear. Here, we employ potato spindle tuber viroid (PSTVd) infecting tomato as a system to dissect host interactions with pathogenic ncRNAs, using comprehensive transcriptome analyses. We uncover various new activities in regulating gene expression during PSTVd infection, such as genome-wide alteration in alternative splicing of host protein-coding genes, enhanced guided-cleavage activities of a host microRNA, and induction of the -acting function of phased secondary small interfering RNAs. Furthermore, we reveal that PSTVd infection massively activates genes involved in plant immune responses, mainly those in the calcium-dependent protein kinase and mitogen-activated protein kinase cascades, as well as prominent genes involved in hypersensitive responses, cell wall fortification, and hormone signaling. Intriguingly, our data support a notion that plant immune systems can respond to pathogenic ncRNAs, which has broad implications for providing new opportunities for understanding the complexity of immune systems in differentiating "self" and "nonself," as well as lay the foundation for resolving the long-standing question regarding the pathogenesis mechanisms of viroids and perhaps other infectious RNAs. Numerous pathogens, including viruses, express pathogenic noncoding transcripts during infection. In the most extreme case, pathogenic noncoding RNAs alone (i.e., viroids) can cause disease in plants. While some work has demonstrated that pathogenic noncoding RNAs interact with host factors for function, the biological significance of pathogenic noncoding RNAs in host-pathogen interactions remains largely unclear. Here, we apply comprehensive genome-wide analyses of plant-viroid interactions and discover several novel molecular activities underlying nuclear-replicating viroid infection processes in plants, including effects on the expression and function of host noncoding transcripts, as well as the alternative splicing of host protein-coding genes. Importantly, we show that plant immunity is activated upon infection of a nuclear-replicating viroid, which is a new concept that helps to understand viroid-based pathogenesis. Our finding has broad implications for understanding the complexity of host immune systems and the diverse functions of noncoding RNAs.
许多病原体在感染过程中会表达非编码RNA（ncRNA）。在最极端的情况下，仅致病性ncRNA（如类病毒）就能感染真核生物并导致疾病。虽然少数致病性ncRNA已被证明参与调节基因表达，但大多数致病性ncRNA在宿主-病原体相互作用中的功能仍不清楚。在此，我们以感染番茄的马铃薯纺锤块茎类病毒（PSTVd）为系统，通过全面的转录组分析来剖析宿主与致病性ncRNA的相互作用。我们发现了PSTVd感染过程中调节基因表达的各种新活动，例如宿主蛋白质编码基因可变剪接的全基因组改变、宿主微小RNA引导切割活性的增强以及阶段性次级小干扰RNA顺式作用功能的诱导。此外，我们揭示PSTVd感染会大量激活参与植物免疫反应的基因，主要是钙依赖蛋白激酶和丝裂原活化蛋白激酶级联反应中的基因，以及参与过敏反应、细胞壁强化和激素信号传导的重要基因。有趣的是，我们的数据支持这样一种观点，即植物免疫系统能够对致病性ncRNA作出反应，这对于理解免疫系统区分“自我”和“非自我”的复杂性提供了新机会具有广泛意义，同时也为解决关于类病毒及可能其他感染性RNA致病机制的长期问题奠定了基础。许多病原体，包括病毒，在感染过程中都会表达致病性非编码转录本。在最极端的情况下，仅致病性非编码RNA（即类病毒）就能使植物患病。虽然一些研究表明致病性非编码RNA与宿主因子相互作用以发挥功能，但致病性非编码RNA在宿主-病原体相互作用中的生物学意义仍 largely不清楚。在此，我们对植物-类病毒相互作用进行全面的全基因组分析，并发现了植物中核复制类病毒感染过程背后的几种新分子活动，包括对宿主非编码转录本表达和功能的影响，以及宿主蛋白质编码基因的可变剪接。重要的是，我们表明核复制类病毒感染后植物免疫会被激活，这是一个有助于理解类病毒致病机制的新概念。我们的发现对于理解宿主免疫系统的复杂性和非编码RNA的多种功能具有广泛意义。
