A 3R-MYB transcription factor is involved in Methyl Jasmonate-Induced disease resistance in Agaricus bisporus and has implications for disease resistance in Arabidopsis

Introduction: Methyl jasmonate (MeJA) and MYB transcription factors (TFs) play important roles in pathogen resistance in several plants, but MYB TFs in conjunction with MeJA-induced defense against Pseudomonas tolaasii in edible mushrooms remain unknown. Objectives: To investigate the role of a nove...

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Main Authors: Shuai Yuan, Hanyue Jiang, Yating Wang, Lei Zhang, Zixuan Shi, Lu Jiao, Demei Meng
Format: Article
Language:English
Published: Elsevier 2025-07-01
Series:Journal of Advanced Research
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Online Access:http://www.sciencedirect.com/science/article/pii/S2090123224003801
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author Shuai Yuan
Hanyue Jiang
Yating Wang
Lei Zhang
Zixuan Shi
Lu Jiao
Demei Meng
author_facet Shuai Yuan
Hanyue Jiang
Yating Wang
Lei Zhang
Zixuan Shi
Lu Jiao
Demei Meng
author_sort Shuai Yuan
collection DOAJ
description Introduction: Methyl jasmonate (MeJA) and MYB transcription factors (TFs) play important roles in pathogen resistance in several plants, but MYB TFs in conjunction with MeJA-induced defense against Pseudomonas tolaasii in edible mushrooms remain unknown. Objectives: To investigate the role of a novel 3R-MYB transcription factor (AbMYB11) in MeJA-induced disease resistance of Agaricus bisporus and in the resistance of transgenic Arabidopsis to P. tolaasii. Methods: Mushrooms were treated with MeJA alone or in combination with phenylpropanoid pathway inhibitors, and the effects of the treatments on the disease-related and physiological indicators of the mushrooms were determined to assess the role of MeJA in inducing resistance and the importance of the phenylpropanoid pathway involved. Subcellular localization, gene expression analysis, dual-luciferase reporter assay, electrophoretic mobility shift assay, and transgenic Arabidopsis experiments were performed to elucidate the molecular mechanism of AbMYB11 in regulating disease resistance. Results: MeJA application greatly improved mushroom resistance to P. tolaasii infection, and suppression of the phenylpropanoid pathway significantly weakened this effect. MeJA treatment stimulated the accumulation of phenylpropanoid metabolites, which was accompanied by increased the activities of biosynthetic enzymes and the expression of phenylpropanoid pathway-related genes (AbPAL1, Ab4CL1, AbC4H1) and an AbPR-like gene, further confirming the critical role of the phenylpropanoid pathway in MeJA-induced responses to P. tolaasii. Importantly, AbMYB11, localized in the nucleus, was rapidly induced by MeJA treatment under P. tolaasii infection; it transcriptionally activated the phenylpropanoid pathway-related and AbPR-like genes, and AbMYB11 overexpression in Arabidopsis significantly increased the transcription of phenylpropanoid-related genes, the accumulation of total phenolics and flavonoids, and improved resistance to P. tolaasii. Conclusion: This study clarified the pivotal role of AbMYB11 as a regulator in disease resistance by modulating the phenylpropanoid pathway, providing a novel idea for the breeding of highly disease-resistant edible mushrooms and plants.
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spelling doaj-art-13fd7ed292ab4c39bbe91c988fbdebd82025-08-20T03:47:16ZengElsevierJournal of Advanced Research2090-12322025-07-017311713110.1016/j.jare.2024.08.037A 3R-MYB transcription factor is involved in Methyl Jasmonate-Induced disease resistance in Agaricus bisporus and has implications for disease resistance in ArabidopsisShuai Yuan0Hanyue Jiang1Yating Wang2Lei Zhang3Zixuan Shi4Lu Jiao5Demei Meng6State Key Laboratory of Food Nutrition and Safety, College of Food Science and Engineering, Tianjin University of Science & Technology, Tianjin 300457, PR ChinaState Key Laboratory of Food Nutrition and Safety, College of Food Science and Engineering, Tianjin University of Science & Technology, Tianjin 300457, PR ChinaState Key Laboratory of Food Nutrition and Safety, College of Food Science and Engineering, Tianjin University of Science & Technology, Tianjin 300457, PR ChinaState Key Laboratory of Food Nutrition and Safety, College of Food Science and Engineering, Tianjin University of Science & Technology, Tianjin 300457, PR ChinaState Key Laboratory of Food Nutrition and Safety, College of Food Science and Engineering, Tianjin University of Science & Technology, Tianjin 300457, PR ChinaState Key Laboratory of Food Nutrition and Safety, College of Food Science and Engineering, Tianjin University of Science & Technology, Tianjin 300457, PR ChinaCorresponding author.; State Key Laboratory of Food Nutrition and Safety, College of Food Science and Engineering, Tianjin University of Science & Technology, Tianjin 300457, PR ChinaIntroduction: Methyl jasmonate (MeJA) and MYB transcription factors (TFs) play important roles in pathogen resistance in several plants, but MYB TFs in conjunction with MeJA-induced defense against Pseudomonas tolaasii in edible mushrooms remain unknown. Objectives: To investigate the role of a novel 3R-MYB transcription factor (AbMYB11) in MeJA-induced disease resistance of Agaricus bisporus and in the resistance of transgenic Arabidopsis to P. tolaasii. Methods: Mushrooms were treated with MeJA alone or in combination with phenylpropanoid pathway inhibitors, and the effects of the treatments on the disease-related and physiological indicators of the mushrooms were determined to assess the role of MeJA in inducing resistance and the importance of the phenylpropanoid pathway involved. Subcellular localization, gene expression analysis, dual-luciferase reporter assay, electrophoretic mobility shift assay, and transgenic Arabidopsis experiments were performed to elucidate the molecular mechanism of AbMYB11 in regulating disease resistance. Results: MeJA application greatly improved mushroom resistance to P. tolaasii infection, and suppression of the phenylpropanoid pathway significantly weakened this effect. MeJA treatment stimulated the accumulation of phenylpropanoid metabolites, which was accompanied by increased the activities of biosynthetic enzymes and the expression of phenylpropanoid pathway-related genes (AbPAL1, Ab4CL1, AbC4H1) and an AbPR-like gene, further confirming the critical role of the phenylpropanoid pathway in MeJA-induced responses to P. tolaasii. Importantly, AbMYB11, localized in the nucleus, was rapidly induced by MeJA treatment under P. tolaasii infection; it transcriptionally activated the phenylpropanoid pathway-related and AbPR-like genes, and AbMYB11 overexpression in Arabidopsis significantly increased the transcription of phenylpropanoid-related genes, the accumulation of total phenolics and flavonoids, and improved resistance to P. tolaasii. Conclusion: This study clarified the pivotal role of AbMYB11 as a regulator in disease resistance by modulating the phenylpropanoid pathway, providing a novel idea for the breeding of highly disease-resistant edible mushrooms and plants.http://www.sciencedirect.com/science/article/pii/S2090123224003801Brown spot diseaseButton mushroomMethyl jasmonatePseudomonas tolaasiiPhenylpropanoid metabolism
spellingShingle Shuai Yuan
Hanyue Jiang
Yating Wang
Lei Zhang
Zixuan Shi
Lu Jiao
Demei Meng
A 3R-MYB transcription factor is involved in Methyl Jasmonate-Induced disease resistance in Agaricus bisporus and has implications for disease resistance in Arabidopsis
Journal of Advanced Research
Brown spot disease
Button mushroom
Methyl jasmonate
Pseudomonas tolaasii
Phenylpropanoid metabolism
title A 3R-MYB transcription factor is involved in Methyl Jasmonate-Induced disease resistance in Agaricus bisporus and has implications for disease resistance in Arabidopsis
title_full A 3R-MYB transcription factor is involved in Methyl Jasmonate-Induced disease resistance in Agaricus bisporus and has implications for disease resistance in Arabidopsis
title_fullStr A 3R-MYB transcription factor is involved in Methyl Jasmonate-Induced disease resistance in Agaricus bisporus and has implications for disease resistance in Arabidopsis
title_full_unstemmed A 3R-MYB transcription factor is involved in Methyl Jasmonate-Induced disease resistance in Agaricus bisporus and has implications for disease resistance in Arabidopsis
title_short A 3R-MYB transcription factor is involved in Methyl Jasmonate-Induced disease resistance in Agaricus bisporus and has implications for disease resistance in Arabidopsis
title_sort 3r myb transcription factor is involved in methyl jasmonate induced disease resistance in agaricus bisporus and has implications for disease resistance in arabidopsis
topic Brown spot disease
Button mushroom
Methyl jasmonate
Pseudomonas tolaasii
Phenylpropanoid metabolism
url http://www.sciencedirect.com/science/article/pii/S2090123224003801
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