Turnip mosaic virus P1 suppresses JA biosynthesis by degrading cpSRP54 that delivers AOCs onto the thylakoid membrane to facilitate viral infection.

Turnip mosaic virus P1 suppresses JA biosynthesis by degrading cpSRP54 that delivers AOCs onto the thylakoid membrane to facilitate viral infection.
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萝卜花叶病毒 P1 通过降解 cpSRP54 来抑制 JA 生物合成,cpSRP54 将 AOC 传递到类囊体膜上以促进病毒感染

DOI:
10.1371/journal.ppat.1010108
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发表时间:
2021-12
期刊:
影响因子:
6.7
通讯作者:
Yan F
Yan F
中科院分区:
医学1区
文献类型:
--
作者:
Ji M;Zhao J;Han K;Cui W;Wu X;Chen B;Lu Y;Peng J;Zheng H;Rao S;Wu G;Chen J;Yan F

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茉莉酸(JA)是植物抗病毒免疫中的重要激素。越来越多的证据表明,病毒通过干扰JA生物合成和信号传导来对抗这种宿主免疫应答。然而,病毒影响JA生物合成的机制在很大程度上仍未被探索。在这里,我们表明,一个高度保守的叶绿体蛋白cpSRP54被下调,在烟草本塞姆亚纳感染芜菁花叶病毒(TuMV)。其沉默促进TuMV感染。此外,cpSRP54与丙二烯氧化物环化酶(AOCs)(JA生物合成的关键酶)相互作用,并负责将AOCs递送到类囊体膜(TM)上。有趣的是,TuMV P1蛋白与cpSRP54相互作用,并通过26S蛋白体和自噬途径介导其降解。结果表明,TuMV已经进化出一种策略,通过抑制cpSRP54及其向TM递送AOC,来抑制JA生物合成并增强病毒感染。cpSRP54与AOCs之间的相互作用在拟南芥和水稻中是保守的,而cpSRP54也与辣椒轻斑驳病毒(PMMoV)126 kDa蛋白和马铃薯X病毒(PVX)p25蛋白相互作用并被其降解,表明cpSRP54的抑制可能是病毒对抗JA途径的共同机制。茉莉酸途径已成为植物与病毒之间的主要战场之一。一些研究表明,除了干扰JA信号传导,植物病毒也可以影响JA的生物合成,但它们之间的直接分子联系仍然难以捉摸。在这里,我们确定了一个高度保守的叶绿体蛋白cpSRP54作为一个关键的正调控JA生物合成和病毒属于不同属的共同目标。通过与cpSRP54结合并利用其编码的蛋白诱导其降解,病毒可以抑制cpSRP54促进的AOC向类囊体膜的递送和JA介导的防御的操纵。病毒的这种能力可能定义一种新的和有效的对抗抗病毒JA途径的策略。
Jasmonic acid (JA) is a crucial hormone in plant antiviral immunity. Increasing evidence shows that viruses counter this host immune response by interfering with JA biosynthesis and signaling. However, the mechanism by which viruses affect JA biosynthesis is still largely unexplored. Here, we show that a highly conserved chloroplast protein cpSRP54 was downregulated in Nicotiana benthamiana infected by turnip mosaic virus (TuMV). Its silencing facilitated TuMV infection. Furthermore, cpSRP54 interacted with allene oxide cyclases (AOCs), key JA biosynthesis enzymes, and was responsible for delivering AOCs onto the thylakoid membrane (TM). Interestingly, TuMV P1 protein interacted with cpSRP54 and mediated its degradation via the 26S proteosome and autophagy pathways. The results suggest that TuMV has evolved a strategy, through the inhibition of cpSRP54 and its delivery of AOCs to the TM, to suppress JA biosynthesis and enhance viral infection. Interaction between cpSRP54 and AOCs was shown to be conserved in Arabidopsis and rice, while cpSRP54 also interacted with, and was degraded by, pepper mild mottle virus (PMMoV) 126 kDa protein and potato virus X (PVX) p25 protein, indicating that suppression of cpSRP54 may be a common mechanism used by viruses to counter the antiviral JA pathway. Jasmonic acid pathway has emerged as one of the predominant battlefields between plants and viruses. Several studies have indicated that, in addition to interfering with JA signaling, plant viruses can also affect JA biosynthesis, but the direct molecular links between them remain elusive. Here, we identify a highly conserved chloroplast protein cpSRP54 as a key positive regulator in JA biosynthesis and a common target for viruses belong to different genera. Through associating with cpSRP54 and inducing its degradation using the protein they encoded, the viruses can inhibit the cpSRP54-facilitated delivery of AOCs to the thylakoid membrane and manipulation of JA-mediated defense. This capability of viruses might define a novel and effective strategy against the antiviral JA pathway.
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