Herbicide 2,4-dichlorophenoxyacetic acid interferes with MAP kinase signaling in Fusarium graminearum and is inhibitory to fungal growth and pathogenesis

Abstract Plant hormones are important for regulating growth, development, and plant-pathogen interactions. Some of them are inhibitory to growth of fungal pathogens but the underlying mechanism is not clear. In this study, we found that hyphal growth of Fusarium graminearum was significantly reduced...

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Main Authors: Kaili Duan, Qifang Shen, Yu Wang, Ping Xiang, Yutong Shi, Chenfei Yang, Cong Jiang, Guanghui Wang, Jin-Rong Xu, Xue Zhang
Format: Article
Language:English
Published: Springer 2023-08-01
Series:Stress Biology
Subjects:
Online Access:https://doi.org/10.1007/s44154-023-00109-x
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author Kaili Duan
Qifang Shen
Yu Wang
Ping Xiang
Yutong Shi
Chenfei Yang
Cong Jiang
Guanghui Wang
Jin-Rong Xu
Xue Zhang
author_facet Kaili Duan
Qifang Shen
Yu Wang
Ping Xiang
Yutong Shi
Chenfei Yang
Cong Jiang
Guanghui Wang
Jin-Rong Xu
Xue Zhang
author_sort Kaili Duan
collection DOAJ
description Abstract Plant hormones are important for regulating growth, development, and plant-pathogen interactions. Some of them are inhibitory to growth of fungal pathogens but the underlying mechanism is not clear. In this study, we found that hyphal growth of Fusarium graminearum was significantly reduced by high concentrations of IAA and its metabolically stable analogue 2,4-dichlorophenoxyacetic acid (2,4-D). Besides inhibitory effects on growth rate, treatments with 2,4-D also caused significant reduction in conidiation, conidium germination, and germ tube growth. Treatments with 2,4-D had no obvious effect on sexual reproduction but significantly reduced TRI gene expression, toxisome formation, and DON production. More importantly, treatments with 2,4-D were inhibitory to infection structure formation and pathogenesis at concentrations higher than 100 µM. The presence of 1000 µM 2,4-D almost completely inhibited plant infection and invasive growth. In F. graminearum, 2,4-D induced ROS accumulation and FgHog1 activation but reduced the phosphorylation level of Gpmk1 MAP kinase. Metabolomics analysis showed that the accumulation of a number of metabolites such as glycerol and arabitol was increased by 2,4-D treatment in the wild type but not in the Fghog1 mutant. Transformants expressing the dominant active FgPBS2 S451D T455D allele were less sensitive to 2,4-D and had elevated levels of intracellular glycerol and arabitol induced by 2,4-D in PH-1. Taken together, our results showed that treatments with 2,4-D interfere with two important MAP kinase pathways and are inhibitory to hyphal growth, DON biosynthesis, and plant infection in F. graminearum.
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spelling doaj.art-eb9fec55709c42b58b52e069fce215762023-11-26T12:22:51ZengSpringerStress Biology2731-04502023-08-013111710.1007/s44154-023-00109-xHerbicide 2,4-dichlorophenoxyacetic acid interferes with MAP kinase signaling in Fusarium graminearum and is inhibitory to fungal growth and pathogenesisKaili Duan0Qifang Shen1Yu Wang2Ping Xiang3Yutong Shi4Chenfei Yang5Cong Jiang6Guanghui Wang7Jin-Rong Xu8Xue Zhang9State Key Laboratory of Crop Stress Biology for Arid Areas, College of Plant Protection, Northwest A&F UniversityState Key Laboratory of Crop Stress Biology for Arid Areas, College of Plant Protection, Northwest A&F UniversityState Key Laboratory of Crop Stress Biology for Arid Areas, College of Plant Protection, Northwest A&F UniversityState Key Laboratory of Crop Stress Biology for Arid Areas, College of Plant Protection, Northwest A&F UniversityState Key Laboratory of Crop Stress Biology for Arid Areas, College of Plant Protection, Northwest A&F UniversityState Key Laboratory of Crop Stress Biology for Arid Areas, College of Plant Protection, Northwest A&F UniversityState Key Laboratory of Crop Stress Biology for Arid Areas, College of Plant Protection, Northwest A&F UniversityState Key Laboratory of Crop Stress Biology for Arid Areas, College of Plant Protection, Northwest A&F UniversityDepartment of Botany and Plant Pathology, Purdue UniversityState Key Laboratory of Crop Stress Biology for Arid Areas, College of Plant Protection, Northwest A&F UniversityAbstract Plant hormones are important for regulating growth, development, and plant-pathogen interactions. Some of them are inhibitory to growth of fungal pathogens but the underlying mechanism is not clear. In this study, we found that hyphal growth of Fusarium graminearum was significantly reduced by high concentrations of IAA and its metabolically stable analogue 2,4-dichlorophenoxyacetic acid (2,4-D). Besides inhibitory effects on growth rate, treatments with 2,4-D also caused significant reduction in conidiation, conidium germination, and germ tube growth. Treatments with 2,4-D had no obvious effect on sexual reproduction but significantly reduced TRI gene expression, toxisome formation, and DON production. More importantly, treatments with 2,4-D were inhibitory to infection structure formation and pathogenesis at concentrations higher than 100 µM. The presence of 1000 µM 2,4-D almost completely inhibited plant infection and invasive growth. In F. graminearum, 2,4-D induced ROS accumulation and FgHog1 activation but reduced the phosphorylation level of Gpmk1 MAP kinase. Metabolomics analysis showed that the accumulation of a number of metabolites such as glycerol and arabitol was increased by 2,4-D treatment in the wild type but not in the Fghog1 mutant. Transformants expressing the dominant active FgPBS2 S451D T455D allele were less sensitive to 2,4-D and had elevated levels of intracellular glycerol and arabitol induced by 2,4-D in PH-1. Taken together, our results showed that treatments with 2,4-D interfere with two important MAP kinase pathways and are inhibitory to hyphal growth, DON biosynthesis, and plant infection in F. graminearum.https://doi.org/10.1007/s44154-023-00109-xFungal pathogenesisMAP kinase pathways2,4-DFusarium graminearum
spellingShingle Kaili Duan
Qifang Shen
Yu Wang
Ping Xiang
Yutong Shi
Chenfei Yang
Cong Jiang
Guanghui Wang
Jin-Rong Xu
Xue Zhang
Herbicide 2,4-dichlorophenoxyacetic acid interferes with MAP kinase signaling in Fusarium graminearum and is inhibitory to fungal growth and pathogenesis
Stress Biology
Fungal pathogenesis
MAP kinase pathways
2,4-D
Fusarium graminearum
title Herbicide 2,4-dichlorophenoxyacetic acid interferes with MAP kinase signaling in Fusarium graminearum and is inhibitory to fungal growth and pathogenesis
title_full Herbicide 2,4-dichlorophenoxyacetic acid interferes with MAP kinase signaling in Fusarium graminearum and is inhibitory to fungal growth and pathogenesis
title_fullStr Herbicide 2,4-dichlorophenoxyacetic acid interferes with MAP kinase signaling in Fusarium graminearum and is inhibitory to fungal growth and pathogenesis
title_full_unstemmed Herbicide 2,4-dichlorophenoxyacetic acid interferes with MAP kinase signaling in Fusarium graminearum and is inhibitory to fungal growth and pathogenesis
title_short Herbicide 2,4-dichlorophenoxyacetic acid interferes with MAP kinase signaling in Fusarium graminearum and is inhibitory to fungal growth and pathogenesis
title_sort herbicide 2 4 dichlorophenoxyacetic acid interferes with map kinase signaling in fusarium graminearum and is inhibitory to fungal growth and pathogenesis
topic Fungal pathogenesis
MAP kinase pathways
2,4-D
Fusarium graminearum
url https://doi.org/10.1007/s44154-023-00109-x
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