Next-generation mapping of the salicylic acid signaling hub and transcriptional cascade.

IF 17.1 1区 生物学 Q1 BIOCHEMISTRY & MOLECULAR BIOLOGY Molecular Plant Pub Date : 2024-10-07 Epub Date: 2024-08-22 DOI:10.1016/j.molp.2024.08.008
Jordan Powers, Xing Zhang, Andres V Reyes, Raul Zavaliev, Roni Ochakovski, Shou-Ling Xu, Xinnian Dong
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Abstract

For over 60 years, salicylic acid (SA) has been known as a plant immune signal required for basal and systemic acquired resistance. SA activates these immune responses by reprogramming ∼20% of the transcriptome through NPR1. However, components in the NPR1 signaling hub, which appears as nuclear condensates, and the NPR1 signaling cascade have remained elusive due to difficulties in studying this transcriptional cofactor, whose chromatin association is indirect and likely transient. To overcome this challenge, we applied TurboID to divulge the NPR1 proxiome, which detected almost all known NPR1 interactors as well as new components of transcription-related complexes. Testing of new components showed that chromatin remodeling and histone demethylation contribute to SA-induced resistance. Globally, the NPR1 proxiome has a striking similarity to the proxiome of GBPL3 that is involved in SA synthesis, except for associated transcription factors (TFs), suggesting that common regulatory modules are recruited to reprogram specific transcriptomes by transcriptional cofactors, like NPR1, through binding to unique TFs. Stepwise green fluorescent protein-tagged factor cleavage under target and release using nuclease (greenCUT&RUN) analyses showed that, upon SA induction, NPR1 initiates the transcriptional cascade primarily through association with TGACG-binding TFs to induce expression of secondary TFs, predominantly WRKYs. Further, WRKY54 and WRKY70 were identified to play a major role in inducing immune-output genes without interacting with NPR1 at the chromatin. Moreover, loss of condensate formation function of NPR1 decreases its chromatin association and transcriptional activity, indicating the importance of condensates in organizing the NPR1 signaling hub and initiating the transcriptional cascade. Collectively, this study demonstrates how combinatorial applications of TurboID and stepwise greenCUT&RUN transcend traditional genetic methods to globally map signaling hubs and transcriptional cascades for in-depth explorations.

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水杨酸信号枢纽和转录级联的下一代图谱。
60 多年来,水杨酸(SA)一直是基础和系统获得性抗性(SAR)所需的植物免疫信号。水杨酸通过 NPR1 的功能对 20% 的转录组进行重编程,从而激活这些免疫反应。然而,由于研究这种转录辅助因子的困难,NPR1-信号中枢(以核凝聚物的形式出现)和 NPR1-信号级联中的成分仍然难以捉摸,因为这种转录辅助因子的染色质关联是间接的,而且很可能是瞬时的。为了克服这一难题,我们应用 TurboID 揭示了 NPR1-proxiome,它检测到了几乎所有已知的 NPR1-interactors,以及转录相关复合物的新成分。对新成分的测试表明,染色质重塑和组蛋白去甲基化有助于提高 SA 诱导的抗性。从全球来看,除了相关的转录因子(TFs)外,NPR1-proxiome与参与SA合成的GBPL3-proxiome有着惊人的相似性,这表明NPR1等转录辅助因子通过与独特的TFs结合,招募了共同的调控模块来重编特定的转录组。逐步绿色 CUT&RUN 分析表明,在 SA 诱导下,NPR1 主要通过与 TGA TFs 结合启动转录级联,诱导次级 TFs(主要是 WRKYs)的表达。然后,WRKY54 和 WRKY70 在诱导免疫输出基因方面发挥主要作用,而不与 NPR1 在染色质上相互作用。此外,失去 NPR1 凝聚物的形成会降低该蛋白的染色质结合和转录活性,这表明凝聚物在组织 NPR1 信号中枢和启动转录级联方面的重要性。这项研究展示了 TurboID 和 stepwise greenCUT&RUN 的组合应用如何超越传统的遗传学方法,在全球范围内绘制信号枢纽和转录级联图,进行深入探索。
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来源期刊
Molecular Plant
Molecular Plant 植物科学-生化与分子生物学
CiteScore
37.60
自引率
2.20%
发文量
1784
审稿时长
1 months
期刊介绍: Molecular Plant is dedicated to serving the plant science community by publishing novel and exciting findings with high significance in plant biology. The journal focuses broadly on cellular biology, physiology, biochemistry, molecular biology, genetics, development, plant-microbe interaction, genomics, bioinformatics, and molecular evolution. Molecular Plant publishes original research articles, reviews, Correspondence, and Spotlights on the most important developments in plant biology.
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