Siyuan Xie , Lanning Wang , Jingkun Lv , Xiang Feng , Siyu Li , Haojie Tan , Chao Wang , Gang Wang , Hongjun Ge , Chun Xiao , Danyu Shen , Daolong Dou
{"title":"反式-2-癸烯醛通过诱导ROS积累和线粒体功能障碍抑制辣椒疫霉","authors":"Siyuan Xie , Lanning Wang , Jingkun Lv , Xiang Feng , Siyu Li , Haojie Tan , Chao Wang , Gang Wang , Hongjun Ge , Chun Xiao , Danyu Shen , Daolong Dou","doi":"10.1016/j.pestbp.2025.106673","DOIUrl":null,"url":null,"abstract":"<div><div><em>Phytophthora capsici</em> is a highly destructive plant-pathogenic oomycete that poses a severe threat to global agricultural production. <em>Trans</em>-2-decenal is a natural plant-derived unsaturated aliphatic aldehyde, whose antimicrobial properties against plant pathogens remain poorly understood. In this study, its inhibitory efficacy and underlying mechanisms against <em>P. capsici</em> were systematically investigated. <em>Trans</em>-2-decenal exhibited potent inhibitory activity against <em>P. capsici</em> via biofumigation, with an EC<sub>50</sub> value of 12.37 μg/mL. It not only impacted normal hyphal morphology and ultrastructure, but also inhibited sporangia formation, zoospore release, and germination in a dose-dependent manner. Calcofluor white staining showed that <em>trans</em>-2-decenal disrupted cell wall integrity. <em>Trans</em>-2-decenal treatment compromised cell membrane integrity and permeability, accompanied by DNA and soluble protein leakage. Additionally, <em>trans</em>-2-decenal triggered intracellular ROS accumulation, reduced glutathione levels, and disrupted mitochondrial membrane potential, ultimately leading to cellular dysfunction and death. <em>In planta</em> assays validated its robust control efficacy against <em>P. capsici</em> infection. Transcriptomic analysis further identified 2557 differentially expressed genes, with significant downregulation in critical metabolic pathways such as nitrogen metabolism, tyrosine metabolism and phenylalanine metabolism. Taken together, these results elucidate a multitarget inhibitory mechanism of <em>trans</em>-2-decenal against <em>P. capsici</em>, and highlight its potential as an eco-friendly agent for the sustainable management of <em>Phytophthora</em>-induced plant diseases.</div></div>","PeriodicalId":19828,"journal":{"name":"Pesticide Biochemistry and Physiology","volume":"215 ","pages":"Article 106673"},"PeriodicalIF":4.0000,"publicationDate":"2025-09-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":"0","resultStr":"{\"title\":\"Trans-2-decenal inhibits Phytophthora capsici by inducing ROS accumulation and mitochondrial dysfunction\",\"authors\":\"Siyuan Xie , Lanning Wang , Jingkun Lv , Xiang Feng , Siyu Li , Haojie Tan , Chao Wang , Gang Wang , Hongjun Ge , Chun Xiao , Danyu Shen , Daolong Dou\",\"doi\":\"10.1016/j.pestbp.2025.106673\",\"DOIUrl\":null,\"url\":null,\"abstract\":\"<div><div><em>Phytophthora capsici</em> is a highly destructive plant-pathogenic oomycete that poses a severe threat to global agricultural production. <em>Trans</em>-2-decenal is a natural plant-derived unsaturated aliphatic aldehyde, whose antimicrobial properties against plant pathogens remain poorly understood. In this study, its inhibitory efficacy and underlying mechanisms against <em>P. capsici</em> were systematically investigated. <em>Trans</em>-2-decenal exhibited potent inhibitory activity against <em>P. capsici</em> via biofumigation, with an EC<sub>50</sub> value of 12.37 μg/mL. It not only impacted normal hyphal morphology and ultrastructure, but also inhibited sporangia formation, zoospore release, and germination in a dose-dependent manner. Calcofluor white staining showed that <em>trans</em>-2-decenal disrupted cell wall integrity. <em>Trans</em>-2-decenal treatment compromised cell membrane integrity and permeability, accompanied by DNA and soluble protein leakage. Additionally, <em>trans</em>-2-decenal triggered intracellular ROS accumulation, reduced glutathione levels, and disrupted mitochondrial membrane potential, ultimately leading to cellular dysfunction and death. <em>In planta</em> assays validated its robust control efficacy against <em>P. capsici</em> infection. Transcriptomic analysis further identified 2557 differentially expressed genes, with significant downregulation in critical metabolic pathways such as nitrogen metabolism, tyrosine metabolism and phenylalanine metabolism. Taken together, these results elucidate a multitarget inhibitory mechanism of <em>trans</em>-2-decenal against <em>P. capsici</em>, and highlight its potential as an eco-friendly agent for the sustainable management of <em>Phytophthora</em>-induced plant diseases.</div></div>\",\"PeriodicalId\":19828,\"journal\":{\"name\":\"Pesticide Biochemistry and Physiology\",\"volume\":\"215 \",\"pages\":\"Article 106673\"},\"PeriodicalIF\":4.0000,\"publicationDate\":\"2025-09-01\",\"publicationTypes\":\"Journal Article\",\"fieldsOfStudy\":null,\"isOpenAccess\":false,\"openAccessPdf\":\"\",\"citationCount\":\"0\",\"resultStr\":null,\"platform\":\"Semanticscholar\",\"paperid\":null,\"PeriodicalName\":\"Pesticide Biochemistry and Physiology\",\"FirstCategoryId\":\"97\",\"ListUrlMain\":\"https://www.sciencedirect.com/science/article/pii/S0048357525003864\",\"RegionNum\":1,\"RegionCategory\":\"农林科学\",\"ArticlePicture\":[],\"TitleCN\":null,\"AbstractTextCN\":null,\"PMCID\":null,\"EPubDate\":\"\",\"PubModel\":\"\",\"JCR\":\"Q2\",\"JCRName\":\"BIOCHEMISTRY & MOLECULAR BIOLOGY\",\"Score\":null,\"Total\":0}","platform":"Semanticscholar","paperid":null,"PeriodicalName":"Pesticide Biochemistry and Physiology","FirstCategoryId":"97","ListUrlMain":"https://www.sciencedirect.com/science/article/pii/S0048357525003864","RegionNum":1,"RegionCategory":"农林科学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"","PubModel":"","JCR":"Q2","JCRName":"BIOCHEMISTRY & MOLECULAR BIOLOGY","Score":null,"Total":0}
Trans-2-decenal inhibits Phytophthora capsici by inducing ROS accumulation and mitochondrial dysfunction
Phytophthora capsici is a highly destructive plant-pathogenic oomycete that poses a severe threat to global agricultural production. Trans-2-decenal is a natural plant-derived unsaturated aliphatic aldehyde, whose antimicrobial properties against plant pathogens remain poorly understood. In this study, its inhibitory efficacy and underlying mechanisms against P. capsici were systematically investigated. Trans-2-decenal exhibited potent inhibitory activity against P. capsici via biofumigation, with an EC50 value of 12.37 μg/mL. It not only impacted normal hyphal morphology and ultrastructure, but also inhibited sporangia formation, zoospore release, and germination in a dose-dependent manner. Calcofluor white staining showed that trans-2-decenal disrupted cell wall integrity. Trans-2-decenal treatment compromised cell membrane integrity and permeability, accompanied by DNA and soluble protein leakage. Additionally, trans-2-decenal triggered intracellular ROS accumulation, reduced glutathione levels, and disrupted mitochondrial membrane potential, ultimately leading to cellular dysfunction and death. In planta assays validated its robust control efficacy against P. capsici infection. Transcriptomic analysis further identified 2557 differentially expressed genes, with significant downregulation in critical metabolic pathways such as nitrogen metabolism, tyrosine metabolism and phenylalanine metabolism. Taken together, these results elucidate a multitarget inhibitory mechanism of trans-2-decenal against P. capsici, and highlight its potential as an eco-friendly agent for the sustainable management of Phytophthora-induced plant diseases.
期刊介绍:
Pesticide Biochemistry and Physiology publishes original scientific articles pertaining to the mode of action of plant protection agents such as insecticides, fungicides, herbicides, and similar compounds, including nonlethal pest control agents, biosynthesis of pheromones, hormones, and plant resistance agents. Manuscripts may include a biochemical, physiological, or molecular study for an understanding of comparative toxicology or selective toxicity of both target and nontarget organisms. Particular interest will be given to studies on the molecular biology of pest control, toxicology, and pesticide resistance.
Research Areas Emphasized Include the Biochemistry and Physiology of:
• Comparative toxicity
• Mode of action
• Pathophysiology
• Plant growth regulators
• Resistance
• Other effects of pesticides on both parasites and hosts.