Rice stripe virus NS3 protein regulates primary miRNA processing through association with the miRNA biogenesis factor OsDRB1 and facilitates virus infection in rice.
Rice stripe virus NS3 protein regulates primary miRNA processing through association with the miRNA biogenesis factor OsDRB1 and facilitates virus infection in rice.
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水稻条纹病毒 NS3 蛋白通过与 miRNA 生物发生因子 OsDRB1 关联来调节初级 miRNA 加工，并促进水稻中的病毒感染
DOI：
10.1371/journal.ppat.1006662
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发表时间：
2017-10
期刊：
影响因子：
6.7
通讯作者：
Li Y
中科院分区：
文献类型：
--
作者：
Zheng L;Zhang C;Shi C;Yang Z;Wang Y;Zhou T;Sun F;Wang H;Zhao S;Qin Q;Qiao R;Ding Z;Wei C;Xie L;Wu J;Li Y
microRNAs（miRNAs）是由miRNAs转录产物加工而成的小分子调控RNA，在植物的生长发育和对微生物侵染的应答中起着重要作用。微生物感染广泛地改变了miRNA的生物合成，但其潜在机制仍然知之甚少。在这项研究中，我们报告了水稻条纹病毒（RSV）编码的非结构蛋白3（NS 3）与OsDRB 1相互作用，OsDRB 1是水稻（Oryza sativa）miRNA加工复合体的一个不可或缺的组成部分。此外，NS 3-OsDRB 1相互作用发生在OsDRB 1自身相互作用所需的位点，这对miRNA的生物合成至关重要。进一步的分析表明，NS 3作为OsDRB 1和pri-miRNAs之间的支架，调节它们的关联，并帮助pri-miRNAs在体内加工。拟南芥中的遗传证据表明，NS 3在miRNA生物合成过程中可以部分替代AtDRB 1/AtHYL 1的双链RNA结合域（dsRBD）的功能。因此，NS 3诱导了几种miRNA的积累，其中大多数靶向与发育或病原体抗性相关的关键基因。相比之下，NS 3的突变体版本（mNS 3），它仍然与OsDRB 1相关，但在pri-miRNA结合中有缺陷，减少了这些miRNA的积累。与非转基因野生型植物相比，表达NS 3的转基因水稻品系对RSV感染表现出显著更高的易感性，而表达mNS 3的转基因品系表现出较低的敏感性反应。我们的研究结果揭示了一个以前未知的机制，其中病毒蛋白质劫持OsDRB 1，加工复合物的关键组成部分，用于miRNA生物合成，并增强了水稻中的病毒感染和致病性。microRNA（miRNAs）在转录或转录后水平调控基因表达，在植物生长发育和生物及非生物胁迫应答中发挥重要作用。越来越多的证据表明，miRNA是宿主-病毒相互作用的关键调节剂，但病毒如何调节miRNA积累仍然知之甚少。本文报道水稻条纹病毒（Rice stripe virus，RSV）编码的NS 3蛋白通过调节pri-miRNA与OsDRB 1的结合来调节pri-miRNA转录物（pri-miRNAs）的加工，OsDRB 1是pri-miRNAs加工复合体的关键因子。NS 3通过与OsDRB 1在OsDRB 1二聚体形成所需的位点结合，增加pri-miRNA向加工复合体的募集，并诱导几种miRNA的积累以及靶基因的阻遏，从而提高水稻对RSV感染的敏感性。这些发现共同揭示了RSV调节pri-miRNA加工的新机制，导致增强的病毒感染。
MicroRNAs (miRNAs) are small regulatory RNAs processed from primary miRNA transcripts, and plant miRNAs play important roles in plant growth, development, and response to infection by microbes. Microbial infections broadly alter miRNA biogenesis, but the underlying mechanisms remain poorly understood. In this study, we report that the Rice stripe virus (RSV)-encoded nonstructural protein 3 (NS3) interacts with OsDRB1, an indispensable component of the rice (Oryza sativa) miRNA-processing complex. Moreover, the NS3-OsDRB1 interaction occurs at the sites required for OsDRB1 self-interaction, which is essential for miRNA biogenesis. Further analysis revealed that NS3 acts as a scaffold between OsDRB1 and pri-miRNAs to regulate their association and aids in vivo processing of pri-miRNAs. Genetic evidence in Arabidopsis showed that NS3 can partially substitute for the function of double-stranded RNA binding domain (dsRBD) of AtDRB1/AtHYL1 during miRNA biogenesis. As a result, NS3 induces the accumulation of several miRNAs, most of which target pivotal genes associated with development or pathogen resistance. In contrast, a mutant version of NS3 (mNS3), which still associated with OsDRB1 but has defects in pri-miRNA binding, reduces accumulation of these miRNAs. Transgenic rice lines expressing NS3 exhibited significantly higher susceptibility to RSV infection compared with non-transgenic wild-type plants, whereas the transgenic lines expressing mNS3 showed a less-sensitive response. Our findings revealed a previously unknown mechanism in which a viral protein hijacks OsDRB1, a key component of the processing complex, for miRNA biogenesis and enhances viral infection and pathogenesis in rice. MicroRNAs (miRNAs) regulate gene expression at the transcriptional or post-transcriptional level and have emerged as key players in regulating plant growth, development and response to biotic and abiotic stresses. Accumulating evidences suggest that miRNAs are pivotal modulators of host–virus interactions, but how virus regulates miRNA accumulation remains poorly understood. Here, we report that NS3 protein encoded by Rice stripe virus (RSV) regulates the processing of several primary miRNA transcripts (pri-miRNAs) by acting as an intermediary to modulate the association of pri-miRNAs and OsDRB1, a key factor of the pri-miRNA processing complex. NS3 increases recruitment of pri-miRNA to the processing complex by its association with OsDRB1 at the sites required for OsDRB1 dimer formation and induces several miRNAs accumulations as well as target genes repression, promoting the sensitivity of rice to RSV infection. Together these findings reveal a novel mechanism by which RSV regulates pri-miRNA processing, leading to enhanced viral infection.
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作者：
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