A rust fungus effector directly binds plant pre-mRNA splice site to reprogram alternative splicing and suppress host immunity.
A rust fungus effector directly binds plant pre-mRNA splice site to reprogram alternative splicing and suppress host immunity.
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生锈真菌效应器直接结合植物前MRNA剪接位点，以重新编程替代剪接并抑制宿主免疫。
DOI：
10.1111/pbi.13800
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发表时间：
2022-06
影响因子：
13.8
通讯作者：
Wang, Xiaojie
中科院分区：
文献类型：
--
作者：
Tang, Chunlei;Xu, Qiang;Zhao, Jinren;Yue, Mingxing;Wang, Jianfeng;Wang, Xiaodong;Kang, Zhensheng;Wang, Xiaojie
选择性剪接（AS）是植物抗病性的一种重要转录后调控机制。然而，植物病原体是否以及如何靶向其宿主中的剪接仍然是未知的。例如，虽然小麦条锈菌（Puccinia striiformis f.小麦黑胫病（Pst）是一种严重影响世界范围内小麦产量的病原真菌，已被证明显著影响宿主中可变剪接转录物的水平，控制这一过程的机制及其功能后果尚未被研究。在这里，我们将Pst_A23鉴定为一种新的富含Pst精氨酸的效应物，其定位于宿主核斑点，即富含剪接因子的核区域。我们证明，瞬时表达的Pst_A23抑制植物的基础防御依赖于Pst_A23核斑点定位，这种蛋白质起着重要作用的毒力，稳定沉默，提高小麦条锈病抗性。值得注意的是，RNA-Seq数据显示，与对照植物相比，588个小麦基因的AS模式在Pst_A23过表达系中发生了改变。为了进一步研究Pst_A23和AS之间的直接关系，我们证实了从这些改变的剪接位点预测的两个RNA基序与Pst_A23在体外的直接结合。我们选择的两个RNA基序出现在TaXa 21-H和TaWRKY 53的顺式元件中，并且我们验证了Pst_A23过表达导致TaXa 21-H和TaWRKY 53的功能转录物减少，而TaXa 21-H和TaWRKY 53的沉默损害小麦对Pst的抗性。总的来说，这代表了植物病原体产生“剪接”效应物的正式证据，该效应物通过直接接合剪接位点来调节宿主前mRNA剪接，从而干扰宿主免疫力。
Alternative splicing (AS) is a crucial post‐transcriptional regulatory mechanism in plant resistance. However, whether and how plant pathogens target splicing in their host remains mostly unknown. For example, although infection by Puccinia striiformis f. sp. tritici (Pst), a pathogenic fungus that severely affects the yield of wheat worldwide, has been shown to significantly influence the levels of alternatively spliced transcripts in the host, the mechanisms that govern this process, and its functional consequence have not been examined. Here, we identified Pst_A23 as a new Pst arginine‐rich effector that localizes to host nuclear speckles, nuclear regions enriched in splicing factors. We demonstrated that transient expression of Pst_A23 suppresses plant basal defence dependent on the Pst_A23 nuclear speckle localization and that this protein plays an important role in virulence, stable silencing of which improves wheat stripe rust resistance. Remarkably, RNA‐Seq data revealed that AS patterns of 588 wheat genes are altered in Pst_A23‐overexpressing lines compared to control plants. To further examine the direct relationship between Pst_A23 and AS, we confirmed direct binding between two RNA motifs predicted from these altered splicing sites and Pst_A23 in vitro. The two RNA motifs we chose occur in the cis‐element of TaXa21‐H and TaWRKY53, and we validated that Pst_A23 overexpression results in decreased functional transcripts of TaXa21‐H and TaWRKY53 while silencing of TaXa21‐H and TaWRKY53 impairs wheat resistance to Pst. Overall, this represents formal evidence that plant pathogens produce ‘splicing’ effectors, which regulate host pre‐mRNA splicing by direct engagement of the splicing sites, thereby interfering with host immunity.
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