Exogenous melatonin enhances Lr10-mediated resistance to Puccinia triticina by upregulating TaRAR1 and potentiating salicylic acid pathway and antioxidant defense system

IF 6.8 Q1 PLANT SCIENCES

Plant Stress Pub Date : 2025-07-28 DOI:10.1016/j.stress.2025.100974

Johannes Mapuranga, Lulu Song, Ruolin Li, Hao Li, Jiaying Chang, Jiaojie Zhao, Yingdan Zhang, Na Zhang, Wenxiang Yang

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引用次数: 0

Abstract

Wheat leaf rust, caused by the biotrophic fungal pathogen Puccinia triticina (Pt), continuously threatens global wheat production, causing considerable yield losses necessitating the implementation of effective management approaches. While conventional breeding and chemical control strategies have been used, priming agents and genetic regulators offer sustainable strategies for wheat leaf rust management. Melatonin (N-acetyl-5-methoxytryptamine), a pleiotropic signaling molecule, induces plant innate immunity against abiotic and biotic stresses. This study demonstrates that exogenous melatonin (100 µM) enhances Lr10-mediated resistance to wheat leaf rust by upregulating TaRAR1, salicylic acid downstream genes, antioxidant enzyme genes, MAPK cascade genes, and WRKY transcription factors during Pt infection. RAR1 serves as an initial convergence point in signaling pathways activated by several R genes. Herein, TaRAR1 was strongly upregulated during early stages of infection in incompatible interactions, and this was associated with increased endogenous SA and melatonin levels, correlating with enhanced defense responses. TaRAR1 silencing compromised TcLr10 resistance, reducing SA and melatonin levels, downregulating defense-related genes, and altering reactive oxygen species dynamics by increasing TaCAT expression and reducing hydrogen peroxide accumulation. TaRAR1 silencing also downregulated TaSGT1, and TaHSP90, suggesting its role in stabilizing NLR proteins. In conclusion, melatonin augments wheat resistance to leaf rust by upregulating TaRAR1, SA signaling, and antioxidant defenses, with MAPK cascades and WRKY transcription factors amplifying downstream responses. This study provides novel insights into the integration of phytohormonal and genetic approaches for enhancing wheat resistance to leaf rust, offering strategies for sustainable disease management.

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外源性褪黑素通过上调TaRAR1，增强水杨酸途径和抗氧化防御系统，增强lr10介导的小麦锈菌抗性

小麦叶锈病是由生物营养真菌病原菌小麦锈病（Puccinia triticina, Pt）引起的，持续威胁着全球小麦生产，造成了相当大的产量损失，需要采取有效的管理措施。在传统育种和化学防治策略被采用的同时，引物剂和遗传调节剂为小麦叶锈病的管理提供了可持续的策略。褪黑素（n -乙酰-5-甲氧基色胺）是一种多效性信号分子，可诱导植物对非生物和生物胁迫产生先天免疫。本研究表明，外源褪黑激素（100µM）在Pt侵染过程中通过上调TaRAR1、水杨酸下游基因、抗氧化酶基因、MAPK级联基因和WRKY转录因子，增强lr10介导的小麦对叶锈病的抗性。RAR1在多个R基因激活的信号通路中起着初始收敛点的作用。在此，TaRAR1在不相容相互作用感染的早期阶段被强烈上调，这与内源性SA和褪黑激素水平的增加有关，与增强的防御反应相关。TaRAR1沉默会损害TcLr10抗性，降低SA和褪黑素水平，下调防御相关基因，并通过增加TaCAT表达和减少过氧化氢积累来改变活性氧的动态。TaRAR1的沉默也下调了TaSGT1和TaHSP90，提示其在稳定NLR蛋白中的作用。综上所述，褪黑素通过上调TaRAR1、SA信号和抗氧化防御，通过MAPK级联反应和WRKY转录因子放大下游反应，增强小麦对叶锈病的抗性。本研究为整合植物激素和遗传方法增强小麦对叶锈病的抗性提供了新的见解，为病害的可持续管理提供了策略。

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来源期刊

Plant Stress PLANT SCIENCES-

CiteScore

5.20

自引率

8.00%

发文量

审稿时长

63 days

期刊介绍： The journal Plant Stress deals with plant (or other photoautotrophs, such as algae, cyanobacteria and lichens) responses to abiotic and biotic stress factors that can result in limited growth and productivity. Such responses can be analyzed and described at a physiological, biochemical and molecular level. Experimental approaches/technologies aiming to improve growth and productivity with a potential for downstream validation under stress conditions will also be considered. Both fundamental and applied research manuscripts are welcome, provided that clear mechanistic hypotheses are made and descriptive approaches are avoided. In addition, high-quality review articles will also be considered, provided they follow a critical approach and stimulate thought for future research avenues. Plant Stress welcomes high-quality manuscripts related (but not limited) to interactions between plants and: Lack of water (drought) and excess (flooding), Salinity stress, Elevated temperature and/or low temperature (chilling and freezing), Hypoxia and/or anoxia, Mineral nutrient excess and/or deficiency, Heavy metals and/or metalloids, Plant priming (chemical, biological, physiological, nanomaterial, biostimulant) approaches for improved stress protection, Viral, phytoplasma, bacterial and fungal plant-pathogen interactions. The journal welcomes basic and applied research articles, as well as review articles and short communications. All submitted manuscripts will be subject to a thorough peer-reviewing process.