ABSTRACT
Deoxynivalenol (DON) is a vital virulence factor of Fusarium graminearum, which causes Fusarium head blight (FHB). We recently found that validamycin A (VMA), an aminoglycoside antibiotic, can be used to control FHB and inhibit DON contamination, but its molecular mechanism is still unclear. In this study, we found that both neutral and acid trehalase (FgNTH and FgATH) are the targets of VMA in F. graminearum, and the deficiency of FgNTH and FgATH reduces the sensitivity to VMA by 2.12- and 1.79-fold, respectively, indicating that FgNTH is the main target of VMA. We found FgNTH is responsible for vegetative growth, FgATH is critical to sexual reproduction, and both of them play an important role in conidiation and virulence in F. graminearum. We found that FgNTH resided in the cytoplasm, affected the localization of FgATH, and positively regulated DON biosynthesis; however, FgATH resided in vacuole and negatively regulated DON biosynthesis. FgNTH interacted with FgPK (pyruvate kinase), a key enzyme in glycolysis, and the interaction was reduced by VMA; the deficiency of FgNTH affected the localization of FgPK under DON induction condition. Strains with a deficiency of FgNTH were more sensitive to demethylation inhibitor (DMI) fungicides. FgNTH regulated the expression level of FgCYP51A and FgCYP51B by interacting with FgCYP51B. Taken together, VMA inhibits DON biosynthesis by targeting FgNTH and reducing the interaction between FgNTH and FgPK, and synergizes with DMI fungicides against F. graminearum by decreasing FgCYP51A and FgCYP51B expression.
Subject(s)
Fungicides, Industrial/pharmacology , Fusarium/genetics , Inositol/analogs & derivatives , Plant Diseases/microbiology , Trehalase/antagonists & inhibitors , Trichothecenes/metabolism , Triticum/microbiology , Cytochrome P450 Family 51/genetics , Cytochrome P450 Family 51/metabolism , Drug Synergism , Fungal Proteins/antagonists & inhibitors , Fungal Proteins/metabolism , Fusarium/drug effects , Fusarium/pathogenicity , Inositol/pharmacology , Pyruvate Kinase/genetics , Pyruvate Kinase/metabolism , Trehalase/genetics , Trehalase/metabolism , VirulenceABSTRACT
Validamycin A (VMA) is an aminoglycoside antibiotic used to control rice sheath blight. Although it has been reported that VMA can induce the plant defense responses, the mechanism remains poorly understood. Here, we found that reactive oxygen species (ROS) bursts and callose deposition in Arabidopsis thaliana, rice (Oryza sativa L.), and wheat (Triticum aestivum L.) were induced by VMA and were most intense with 10 µg of VMA per milliliter at 24 h. Moreover, we showed that VMA induced resistance against Pseudomonas syringae, Botrytis cinerea, and Fusarium graminearum in Arabidopsis leaves, indicating that VMA induces broad-spectrum disease resistance in both dicots and monocots. In addition, VMA-mediated resistance against P. syringae was not induced in NahG transgenic plants, was partially decreased in npr1 mutants, and VMA-mediated resistance to B. cinerea was not induced in npr1, jar1, and ein2 mutants. These results strongly indicated that VMA triggers plant defense responses to both biotrophic and necrotrophic pathogens involved in salicylic acid (SA) and jasmonic acid/ethylene (JA/ET) signaling pathways and is dependent on NPR1. In addition, transcriptome analysis further revealed that VMA regulated the expression of genes involved in SA, JA/ET, abscisic acid (ABA), and auxin signal pathways. Taken together, VMA induces systemic resistance involving in SA and JA/ET signaling pathways and also exerts a positive influence on ABA and auxin signaling pathways. Our study highlights the creative application of VMA in triggering plant defense responses against plant pathogens, providing a valuable insight into applying VMA to enhance plant resistance and reduce the use of chemical pesticides.[Formula: see text] Copyright © 2020 The Author(s). This is an open access article distributed under the CC BY-NC-ND 4.0 International license.
Subject(s)
Arabidopsis , Cyclopentanes , Disease Resistance , Inositol/analogs & derivatives , Oxylipins , Salicylic Acid , Signal Transduction , Arabidopsis/drug effects , Arabidopsis/microbiology , Arabidopsis Proteins/genetics , Arabidopsis Proteins/metabolism , Botrytis/physiology , Cyclopentanes/metabolism , Disease Resistance/drug effects , Ethylenes/metabolism , Fusarium/physiology , Inositol/pharmacology , Oxylipins/metabolism , Plant Diseases/microbiology , Salicylic Acid/metabolism , Signal Transduction/drug effectsABSTRACT
Validamycin, known to interfere with fungal energy metabolism by inhibiting trehalase, has been extensively used to control plant diseases caused by Rhizoctonia spp. However, the effect of validamycin on controlling Fusarium graminearum has not been previously reported. In this study, when applied to F. graminearum in vitro, validamycin inhibited the synthesis of deoxynivalenol (DON), which is a mycotoxin and virulence factor, by decreasing trehalase activity and the production of glucose and pyruvate, which are precursors of DON biosynthesis. Because FgNTH encodes the main trehalase in F. graminearum, these effects were nullified in the FgNTH deletion mutant ΔFgNTH but restored in the complemented strain ΔFgNTHC. In addition, validamycin also increased the expression of pathogenesis-related genes (PRs) PR1, PR2, and PR5 in wheat, inducing resistance responses of wheat against F. graminearum. Therefore, validamycin exhibits dual efficacies on controlling Fusarium head blight (FHB) caused by F. graminearum: inhibition of DON biosynthesis and induction of host resistance. In addition, field trials further confirmed that validamycin increased FHB control and reduced DON contamination in grain. Control of FHB and DON contamination by validamycin increased when the antibiotic was applied with the triazole fungicide metconazole. Overall, this study is a successful case from foundational research to applied research, providing useful information for wheat protection programs against toxigenic fungi responsible for FHB and the consequent mycotoxin accumulation in grains.