Molecular insights into fusaric acid-induced cellular damage and hormonal modulation in watermelon suspension cells

IF 6.8 Q1 PLANT SCIENCES

Plant Stress Pub Date : 2025-08-28 DOI:10.1016/j.stress.2025.101019

Xiaoqing Wang , Zhuoying Ding , Yu Gao , Huapeng Sun , Muhammad Mubashar Zafar , Xuefei Jiang , Fei Qiao , Muhammad Shahzaib

{"title":"Molecular insights into fusaric acid-induced cellular damage and hormonal modulation in watermelon suspension cells","authors":"Xiaoqing Wang , Zhuoying Ding , Yu Gao , Huapeng Sun , Muhammad Mubashar Zafar , Xuefei Jiang , Fei Qiao , Muhammad Shahzaib","doi":"10.1016/j.stress.2025.101019","DOIUrl":null,"url":null,"abstract":"<div><div>Watermelon (<em>Citrullus lanatus</em>), a key global crop in the Cucurbitaceae family, is significantly impacted by wilt disease caused by <em>Fusarium oxysporum</em>. This study used suspension-cultured watermelon cells to examine the physiological and molecular effects of fusaric acid (FA), a major phytotoxin produced by the pathogen, at final concentrations of 0, 50, 100, 200, and 300 μM. The 100 μM FA treatment, used for most assays, reduced fresh cell weight by ∼52 %, decreased packed cell volume by ∼70 %, and more than doubled malondialdehyde (MDA) content, indicating severe lipid peroxidation. Antioxidant enzyme activities showed differential responses: superoxide dismutase (SOD) activity declined significantly at both 2 h and 24 h, peroxidase (POD) remained largely unchanged, and catalase (CAT) showed no significant variation. FA exposure also caused a progressive increase in extracellular pH and conductivity, reflecting loss of membrane integrity. Pretreatment with exogenous plant hormones (IAA, MeJA, ABA, SA; 100 μM each for 12 h) mitigated several FA-induced effects, with SA showing the greatest recovery in fresh weight and most pronounced reduction of POD activity. Transcriptome profiling revealed thousands of FA-responsive genes within 2–24 h, and inhibition of DNA methylation with 5-azacytidine altered the expression of multiple hormone-related genes. These results demonstrate that FA rapidly impairs growth, membrane stability, and antioxidant defense in watermelon cells, and that targeted hormonal and epigenetic interventions can partially counteract these effects. The findings provide a mechanistic basis for developing priming strategies to enhance watermelon resistance to Fusarium wilt.</div></div>","PeriodicalId":34736,"journal":{"name":"Plant Stress","volume":"18 ","pages":"Article 101019"},"PeriodicalIF":6.8000,"publicationDate":"2025-08-28","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":"0","resultStr":null,"platform":"Semanticscholar","paperid":null,"PeriodicalName":"Plant Stress","FirstCategoryId":"1085","ListUrlMain":"https://www.sciencedirect.com/science/article/pii/S2667064X25002878","RegionNum":0,"RegionCategory":null,"ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"","PubModel":"","JCR":"Q1","JCRName":"PLANT SCIENCES","Score":null,"Total":0}

引用次数: 0

Abstract

Watermelon (Citrullus lanatus), a key global crop in the Cucurbitaceae family, is significantly impacted by wilt disease caused by Fusarium oxysporum. This study used suspension-cultured watermelon cells to examine the physiological and molecular effects of fusaric acid (FA), a major phytotoxin produced by the pathogen, at final concentrations of 0, 50, 100, 200, and 300 μM. The 100 μM FA treatment, used for most assays, reduced fresh cell weight by ∼52 %, decreased packed cell volume by ∼70 %, and more than doubled malondialdehyde (MDA) content, indicating severe lipid peroxidation. Antioxidant enzyme activities showed differential responses: superoxide dismutase (SOD) activity declined significantly at both 2 h and 24 h, peroxidase (POD) remained largely unchanged, and catalase (CAT) showed no significant variation. FA exposure also caused a progressive increase in extracellular pH and conductivity, reflecting loss of membrane integrity. Pretreatment with exogenous plant hormones (IAA, MeJA, ABA, SA; 100 μM each for 12 h) mitigated several FA-induced effects, with SA showing the greatest recovery in fresh weight and most pronounced reduction of POD activity. Transcriptome profiling revealed thousands of FA-responsive genes within 2–24 h, and inhibition of DNA methylation with 5-azacytidine altered the expression of multiple hormone-related genes. These results demonstrate that FA rapidly impairs growth, membrane stability, and antioxidant defense in watermelon cells, and that targeted hormonal and epigenetic interventions can partially counteract these effects. The findings provide a mechanistic basis for developing priming strategies to enhance watermelon resistance to Fusarium wilt.

查看原文本刊更多论文

镰刀酸诱导的西瓜悬浮细胞损伤和激素调节的分子机制

西瓜（Citrullus lanatus）是葫芦科重要的全球作物，受到尖孢镰刀菌（Fusarium oxysporum）引起的枯萎病的严重影响。本研究利用悬浮培养的西瓜细胞，研究了病原菌产生的主要植物毒素镰刀酸（FA）在最终浓度为0、50、100、200和300 μM时的生理和分子效应。大多数实验使用100 μM FA处理，新鲜细胞重量减少~ 52%，填充细胞体积减少~ 70%，丙二醛（MDA）含量增加一倍以上，表明严重的脂质过氧化。抗氧化酶活性表现出差异反应：超氧化物歧化酶（SOD）活性在2 h和24 h均显著下降，过氧化物酶（POD）活性基本保持不变，过氧化氢酶（CAT）活性无显著变化。FA暴露也导致细胞外pH值和电导率逐渐升高，反映了膜完整性的丧失。外源植物激素（IAA、MeJA、ABA、SA，各100 μM，处理12 h）可以减轻fa诱导的几种效应，其中SA对鲜重的恢复效果最大，对POD活性的降低效果最明显。转录组分析在2-24小时内揭示了数千个fa应答基因，5-氮杂胞苷抑制DNA甲基化改变了多个激素相关基因的表达。这些结果表明，FA会迅速损害西瓜细胞的生长、膜稳定性和抗氧化防御，而有针对性的激素和表观遗传干预可以部分抵消这些影响。该研究结果为制定提高西瓜枯萎病抗性的引物策略提供了机理依据。

本文章由计算机程序翻译，如有差异，请以英文原文为准。

求助全文

约1分钟内获得全文求助全文

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.