A Ralstonia effector RipAU impairs peanut AhSBT1.7 immunity for pathogenicity via AhPME-mediated cell wall degradation

IF 6.2 1区生物学 Q1 PLANT SCIENCES

The Plant Journal Pub Date : 2025-01-27 DOI:10.1111/tpj.17210

Kun Chen, Yuhui Zhuang, Hua Chen, Taijie Lei, Mengke Li, Shanshan Wang, Lihui Wang, Huiwen Fu, Wenzhi Lu, Abhishek Bohra, Qiaoqiao Lai, Xiaolin Xu, Vanika Garg, Rutwik Barmukh, Biaojun Ji, Chong Zhang, Manish K. Pandey, Ronghua Tang, Rajeev K. Varshney, Weijian Zhuang

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Abstract

Bacterial wilt caused by Ralstonia solanacearum is a devastating disease affecting a great many crops including peanut. The pathogen damages plants via secreting type Ш effector proteins (T3Es) into hosts for pathogenicity. Here, we characterized RipAU was among the most toxic effectors as ΔRipAU completely lost its pathogenicity to peanuts. A serine residue of RipAU is the critical site for cell death. The RipAU targeted a subtilisin-like protease (AhSBT1.7) in peanut and both protein moved into nucleus. Heterotic expression of AhSBT1.7 in transgenic tobacco and Arabidopsis thaliana significantly improved the resistance to R. solanacearum. The enhanced resistance was linked with the upregulating ERF1 defense marker genes and decreasing pectin methylesterase (PME) activity like PME2&4 in cell wall pathways. The RipAU played toxic effect by repressing R-gene, defense hormone signaling, and AhSBTs metabolic pathways but increasing PMEs expressions. Furthermore, we discovered AhSBT1.7 interacted with AhPME4 and was colocalized at nucleus. The AhPME speeded plants susceptibility to pathogen via mediated cell wall degradation, which inhibited by AhSBT1.7 but upregulated by RipAU. Collectively, RipAU impaired AhSBT1.7 defense for pathogenicity by using PME-mediated cell wall degradation. This study reveals the mechanism of RipAU pathogenicity and AhSBT1.7 resistance, highlighting peanut immunity to bacterial wilt for future improvement.

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由 Ralstonia solanacearum 引起的细菌枯萎病是一种毁灭性病害，影响包括花生在内的许多作物。病原体通过向宿主分泌Ш型效应蛋白（T3Es）来损害植物，从而产生致病性。在这里，我们发现 RipAU 是毒性最强的效应蛋白之一，因为 ΔRipAU 完全丧失了对花生的致病性。RipAU 的一个丝氨酸残基是细胞死亡的关键部位。RipAU 以花生中的一种类似枯草蛋白的蛋白酶（AhSBT1.7）为靶标，这两种蛋白都进入了细胞核。在转基因烟草和拟南芥中异源表达 AhSBT1.7 能显著提高对茄科细菌的抗性。抗性的增强与ERF1防御标记基因的上调和细胞壁通路中果胶甲基酯酶（PME）（如PME2和PME4）活性的降低有关。RipAU 通过抑制 R 基因、防御激素信号转导和 AhSBTs 代谢途径，但增加了 PMEs 的表达，从而发挥毒性作用。此外，我们还发现AhSBT1.7与AhPME4相互作用，并在细胞核内共定位。AhPME 通过介导细胞壁降解加速植物对病原体的易感性，AhSBT1.7 可抑制细胞壁降解，但 RipAU 可上调细胞壁降解。总之，RipAU 通过利用 PME 介导的细胞壁降解，削弱了 AhSBT1.7 的致病性防御能力。这项研究揭示了 RipAU 的致病性和 AhSBT1.7 的抗性机理，突出了花生对细菌性枯萎病的免疫力，为今后的改良提供了依据。

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来源期刊

The Plant Journal 生物-植物科学

CiteScore

13.10

自引率

4.20%

发文量

415

审稿时长

2.3 months

期刊介绍： Publishing the best original research papers in all key areas of modern plant biology from the world"s leading laboratories, The Plant Journal provides a dynamic forum for this ever growing international research community. Plant science research is now at the forefront of research in the biological sciences, with breakthroughs in our understanding of fundamental processes in plants matching those in other organisms. The impact of molecular genetics and the availability of model and crop species can be seen in all aspects of plant biology. For publication in The Plant Journal the research must provide a highly significant new contribution to our understanding of plants and be of general interest to the plant science community.