A downy mildew effector attenuates salicylic acid-triggered immunity in Arabidopsis by interacting with the host mediator complex.
A downy mildew effector attenuates salicylic acid-triggered immunity in Arabidopsis by interacting with the host mediator complex.
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DOI：
10.1371/journal.pbio.1001732
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发表时间：
2013-12
期刊：
影响因子：
9.8
通讯作者：
Jones JD
中科院分区：
文献类型：
--
作者：
Caillaud MC;Asai S;Rallapalli G;Piquerez S;Fabro G;Jones JD
HaRxL 44是拟南芥霜霉病病原体阿拉伯透明霜霉（Hyaloperonospora arabidopsidis）分泌的效应子，其通过与介体亚基MED 19 a相互作用并降解介体亚基MED 19 a来增强疾病易感性，从而扰乱植物防御基因转录。植物持续暴露于病原体攻击，但通常保持健康，因为它们可以在感知微生物时激活防御。然而，病原体已经进化到通过将效应物递送到植物细胞中以减弱防御来克服植物免疫，从而导致疾病。最近的研究表明，一些效应可能操纵宿主的转录，但这些效应促进易感性的具体机制仍不清楚。我们研究了卵菌霜霉病病原体拟南芥，透明operonospora arabidopsidis（Hpa），并在这里显示，核定位效应HaRxL 44与介体亚基19 a（MED 19 a）相互作用，导致MED 19 a的降解在蛋白酶体依赖的方式。在真核生物中，介导转录调节因子和RNA聚合酶II之间相互作用的介导因子复合物是广泛保守的。我们发现MED 19 a是抗Hpa免疫的正调节剂。表达谱分析实验揭示了类似于茉莉酸/乙烯（JA/ET）信号在HaRxL 44的存在下，也与Hpa感染后3天的转录变化。JA/ET信号升高与表达HaRxL 44的拟南芥植物和med 19 a功能丧失突变体中水杨酸（SA）触发的免疫（SATI）减少相关，而SATI在过表达MED 19 a的植物中升高。使用PR 1：：GUS报告，我们发现，Hpa抑制PR 1的表达，特别是在含有吸器的细胞，其中RxLR效应子交付，但不是在nonhistoriated相邻的细胞，显示高PR 1：：GUS表达水平。因此，HaRxL 44通过降解MED 19干扰介体功能，将防御转录的平衡从SA响应性防御转移到JA/ET信号传导，并通过减弱SA依赖性基因表达来增强对生物营养型的易感性。高度保守的介体复合物通过在转录因子和RNA聚合酶II之间提供分子桥梁而在转录调控中起重要作用。最近在拟南芥中的研究表明，它在植物防御中也起着重要作用。然而，病原体如何操纵介体功能以增加植物对感染的易感性仍然是未知的。在这篇文章中，我们表明，分泌的效应，HaRxL 44，从拟南芥霜霉病病原体阿拉伯透明霜霉（Hpa），相互作用，并降解介体亚基MED 19 a，导致植物防御基因转录的改变。这种效应子介导的干扰宿主转录调节扰乱茉莉酸/乙烯（JA/ET）和水杨酸（SA）依赖的防御之间的平衡。HaRxL 44与MED 19 a的相互作用导致SA调节的基因表达减少，表明该病原体效应子调节宿主转录以促进毒力。由此产生的防御转录模式的改变损害了植物防御病原体的能力，例如Hpa，其通过吸器（一种病原体结构，其产生扩展的宿主/寄生虫界面以提取营养物）与活宿主细胞建立长期寄生相互作用，但不抵抗杀死宿主细胞的坏死型病原体。HaRxL 44不太可能是实现激素平衡的这种转变的唯一效应子，其他研究人员报道了其他核HaRxL蛋白与中介体组分以及JA/ET信号通路的其他调节剂相互作用。对这些效应子的功能分析有助于发现植物免疫系统的新成分。这些数据表明，病原体可以针对宿主调节的基本机制，以打破信号通路的平衡，抑制防御和有利于寄生。
HaRxL44, a secreted effector from the Arabidopsis downy mildew pathogen Hyaloperonospora arabidopsidis, enhances disease susceptibility by interacting with and degrading Mediator subunit MED19a, thereby perturbing plant defense gene transcription. Plants are continually exposed to pathogen attack but usually remain healthy because they can activate defences upon perception of microbes. However, pathogens have evolved to overcome plant immunity by delivering effectors into the plant cell to attenuate defence, resulting in disease. Recent studies suggest that some effectors may manipulate host transcription, but the specific mechanisms by which such effectors promote susceptibility remain unclear. We study the oomycete downy mildew pathogen of Arabidopsis, Hyaloperonospora arabidopsidis (Hpa), and show here that the nuclear-localized effector HaRxL44 interacts with Mediator subunit 19a (MED19a), resulting in the degradation of MED19a in a proteasome-dependent manner. The Mediator complex of ∼25 proteins is broadly conserved in eukaryotes and mediates the interaction between transcriptional regulators and RNA polymerase II. We found MED19a to be a positive regulator of immunity against Hpa. Expression profiling experiments reveal transcriptional changes resembling jasmonic acid/ethylene (JA/ET) signalling in the presence of HaRxL44, and also 3 d after infection with Hpa. Elevated JA/ET signalling is associated with a decrease in salicylic acid (SA)–triggered immunity (SATI) in Arabidopsis plants expressing HaRxL44 and in med19a loss-of-function mutants, whereas SATI is elevated in plants overexpressing MED19a. Using a PR1::GUS reporter, we discovered that Hpa suppresses PR1 expression specifically in cells containing haustoria, into which RxLR effectors are delivered, but not in nonhaustoriated adjacent cells, which show high PR1::GUS expression levels. Thus, HaRxL44 interferes with Mediator function by degrading MED19, shifting the balance of defence transcription from SA-responsive defence to JA/ET-signalling, and enhancing susceptibility to biotrophs by attenuating SA-dependent gene expression. The highly conserved Mediator complex plays an essential role in transcriptional regulation by providing a molecular bridge between transcription factors and RNA polymerase II. Recent studies in Arabidopsis have revealed that it also performs an essential role in plant defence. However, it remains unknown how pathogens manipulate Mediator function in order to increase a plant's susceptibility to infection. In this article, we show that a secreted effector, HaRxL44, from the Arabidopsis downy mildew pathogen Hyaloperonospora arabidopsidis (Hpa), interacts with and degrades the Mediator subunit MED19a, resulting in the alteration of plant defence gene transcription. This effector-mediated interference with host transcriptional regulation perturbs the balance between jasmonic acid/ethylene (JA/ET) and salicylic acid (SA)–dependent defence. HaRxL44 interaction with MED19a results in reduced SA-regulated gene expression, indicating that this pathogen effector modulates host transcription to promote virulence. The resulting alteration in defence transcription patterns compromises the plant's ability to defend itself against pathogens, such as Hpa, that establish long-term parasitic interactions with living host cells via haustoria (a pathogen structure that creates an expanded host/parasite interface to extract nutrients) but not against necrotrophic pathogens that kill host cells. HaRxL44 is unlikely to be the sole effector that accomplishes this shift in hormonal balance, and other nuclear HaRxL proteins were reported by other researchers to interact with Mediator components, as well as with other regulators of the JA/ET signalling pathway. Functional analyses of these effectors should facilitate the discovery of new components of the plant immune system. These data show that pathogens can target fundamental mechanisms of host regulation in order to tip the balance of signalling pathways to suppress defence and favour parasitism.
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