Molecular mechanism through which the JrMAPK3-JrWRKY22 module mediates pathogenesis-related genes to increase walnut anthracnose resistance

doi:10.1016/j.jia.2026.04.018

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Haifeng Xu¹, Guifang Wang¹, Sumin Qi¹, Tiantian Ye¹, Kun Xiang¹, Meiyong Zhang¹, Rui Zhang², Guangning Shen¹, Xin Chen^1#

¹ Key Laboratory of Huanghuai Protected Horticulture Engineering, National Walnut and Chestnut Germplasm Resources Nursery, Shandong Institute of Pomology, Tai’an, Shandong 271000, China

² College of Horticulture and Forestry, Tarim University, Alar, Xinjiang 843300, China

Highlights:

1. The JrMAPK3-JrWRKY22 module associated with anthracnose is first identified in walnut.

2. It reveals the mechanism by which the JrMAPK3-JrWRKY22 module regulates the downstream disease-resistant genes JrPR1 and JrGLU.

3. It is the first time to identify disease-resistant phenotypes using virus vector-mediated transient overexpression and transient silencing in walnut fruits.

Abstract
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摘要

核桃是重要的木本油料经济树种，由胶孢炭疽菌引起的炭疽病是中国核桃生产中的灾难性病害。MAPK-WRKY信号途径在调控植物抗病方面具有重要作用，然而核桃中的MAPK-WRKY途径的鉴定及其介导的炭疽病抗性机制仍不清晰。我们以炭疽病抗性存在明显差异的‘Taile’和‘Xiangling’为试材，通过转录组学筛选到与炭疽病抗性相关的潜在JrMAPK3-JrWRKY22途径。进一步通过酵母双杂，Bifc，Pull-down和体外磷酸化分析表明JrWRKY22与JrMAPK3互作，并被JrMAPK3磷酸化。核桃果实瞬时注射结果表明，过表达JrWRKY22能抑制胶孢炭疽菌侵染，提高果实炭疽病抗性，同时显著促进病程相关基因JrPR1和PR-2家族的β-1,3-葡聚糖酶基因JrGLU表达，而沉默JrWRKY22后胶孢炭疽菌侵染病斑明显增大，相应基因表达水平降低。双荧光素酶实验也验证上述结果，JrWRKY22能激活JrPR1和JrGLU启动子活性，且被JrMAPK3磷酸化增强。进一步通过酵母单杂、Chip-PCR和EMSA分析表明JrWRKY22能结合JrPR1和JrGLU启动子中W-box元件。这些解析了JrMAPK3-JrWRKY22模块提高核桃炭疽病抗性的分子机制，拓宽了抗病理论，为核桃抗病分子设计育种提供科学依据。

Abstract

Walnut is an important economic woody oil tree species, and anthracnose caused by Colletotrichum gloeosporioides is a devastating disease affecting walnut production in China. The MAPK-WRKY signaling pathway plays an important role in regulating plant disease resistance. However, the MAPK-WRKY pathway in walnut and the mechanism involved in anthracnose resistance remain unclear. Using 'Taile' and 'Xiangling' with significant differences in anthracnose resistance as materials, we identified a potential JrMAPK3-JrWRKY22 pathway related to anthracnose resistance through transcriptomics. Further analysis using yeast two-hybrid, bimolecular fluorescence complementation, pull-down, and in vitro phosphorylation assays revealed that JrWRKY22 interacts with and is phosphorylated by JrMAPK3. Transient injection results in walnut fruit revealed that overexpression of JrWRKY22 can inhibit Colletotrichum gloeosporioides infection, increase fruit anthracnose resistance, and significantly promote the expression of the β-1,3-glucanase gene JrGLU of the PR-2 family and the pathogenesis-related gene JrPR1. In contrast, silencing JrWRKY22 resulted in a significant increase in lesion size caused by Colletotrichum gloeosporioides and a corresponding decrease in gene expression levels. A dual-luciferase assay confirmed that JrWRKY22 can activate the promoter activity of JrPR1 and JrGLU and that phosphorylation by JrMAPK3 increases this activation. Further analysis using yeast one-hybrid assays, ChIP-PCR, and EMSA demonstrated that JrWRKY22 can bind to W-box elements in the promoters of JrPR1 and JrGLU. These findings elucidate the molecular mechanism by which the JrMAPK3-JrWRKY22 module increases walnut anthracnose resistance, broaden the understanding of resistance mechanisms, and provide a scientific basis for molecular breeding in the context of walnut disease resistance.

Keywords: JrMAPK3 JrWRKY22 pathogenesis-related genes walnut anthracnose

Online: 15 April 2026

Fund:

This work was supported by the National Natural Science Foundation of China (32301628), the Natural Science Foundation of Shandong Province (ZR2024QC110), the Shandong Province Fruit Industry Technology System (SDAIT-06-1) and the Key Industry Innovation Development Support Plan for South Xin-jiang (2022DB022).

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Haifeng Xu, Guifang Wang, Sumin Qi, Tiantian Ye, Kun Xiang, Meiyong Zhang, Rui Zhang, Guangning Shen, Xin Chen. 2026. Molecular mechanism through which the JrMAPK3-JrWRKY22 module mediates pathogenesis-related genes to increase walnut anthracnose resistance. Journal of Integrative Agriculture, Doi:10.1016/j.jia.2026.04.018

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