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Cross Talk between GlAQP and NOX Modulates the Effects of ROS Balance on Ganoderic Acid Biosynthesis of Ganoderma lucidum under Water Stress

Water stress affects both the growth and development of filamentous fungi; however, the mechanisms underlying their response to water stress remain unclear. In this study, water stress was found to increase intracellular reactive oxygen species (ROS) level, ganoderic acid (GA) content, and NADPH oxi...

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Autores principales: Zhu, Quanyu, Ren, Ang, Ding, Juan, He, Jian, Zhao, Mingwen, Jiang, Ailiang, Zhou, Xiaolin, Wang, Jieying, He, Qin
Formato: Online Artículo Texto
Lenguaje:English
Publicado: American Society for Microbiology 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9784773/
https://www.ncbi.nlm.nih.gov/pubmed/36321895
http://dx.doi.org/10.1128/spectrum.01297-22
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author Zhu, Quanyu
Ren, Ang
Ding, Juan
He, Jian
Zhao, Mingwen
Jiang, Ailiang
Zhou, Xiaolin
Wang, Jieying
He, Qin
author_facet Zhu, Quanyu
Ren, Ang
Ding, Juan
He, Jian
Zhao, Mingwen
Jiang, Ailiang
Zhou, Xiaolin
Wang, Jieying
He, Qin
author_sort Zhu, Quanyu
collection PubMed
description Water stress affects both the growth and development of filamentous fungi; however, the mechanisms underlying their response to water stress remain unclear. In this study, water stress was found to increase intracellular reactive oxygen species (ROS) level, ganoderic acid (GA) content, and NADPH oxidase (NOX) activity of Ganoderma lucidum by 148.45%, 75.32%, and 161.61%, respectively. Water stress induced the expression of the G. lucidum aquaporin (GlAQP) gene, which facilitated water transfer for microbial growth. Compared to wild type (WT), exposure to water stress increased growth inhibition rate, ROS level, and GA content of GlAQP-silenced strains by 37 to 41%, 36 to 38%, and 25%, respectively. Furthermore, at the early stage of fermentation in GlAQP-silenced strains, water stress resulted in 16 to 17% and 9 to 10% lower ROS level and GA content compared to WT, respectively. However, in GlAQP-overexpressing strains, ROS level and GA content were 22 to 24% and 12 to 13% higher than in WT, respectively. In GlAQP-silenced strains, water stress at the late stage resulted in 35 to 37% and 29 to 30% higher ROS level and GA content, respectively, while in GlAQP-overexpressing strains, levels were 16 to 17% and 9% lower than WT, respectively. Cross talk between GlAQP and NOX positively regulated the GA biosynthesis of G. lucidum via ROS under water stress at the early stage but this regulation became negative at the late stage. This study deepens the understanding of fungal signaling transduction under water stress and provides a reference for analyzing environmental factors that influence the regulation of the fungal secondary metabolism. IMPORTANCE Ganoderma lucidum is an advanced basidiomycete that produces medicinally active secondary metabolites (especially ganoderic acid [GA]) with high commercial value. Water stress imposes an important environmental challenge to G. lucidum. The mechanism of GA biosynthesis under water stress and the role of G. lucidum aquaporin (GlAQP) during its biosynthesis remain unclear. Moreover, the effect of the relationship between GlAQP and NADPH oxidase (NOX) on the level of reactive oxygen species and GA production under water stress is unknown. This study provides information on the biological response mechanism of G. lucidum to water stress. A new theory on the cell signaling cascade of G. lucidum tolerance to water stress is provided that also incorporates the biosynthesis of secondary metabolites involved in NOX and GlAQP.
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spelling pubmed-97847732022-12-24 Cross Talk between GlAQP and NOX Modulates the Effects of ROS Balance on Ganoderic Acid Biosynthesis of Ganoderma lucidum under Water Stress Zhu, Quanyu Ren, Ang Ding, Juan He, Jian Zhao, Mingwen Jiang, Ailiang Zhou, Xiaolin Wang, Jieying He, Qin Microbiol Spectr Research Article Water stress affects both the growth and development of filamentous fungi; however, the mechanisms underlying their response to water stress remain unclear. In this study, water stress was found to increase intracellular reactive oxygen species (ROS) level, ganoderic acid (GA) content, and NADPH oxidase (NOX) activity of Ganoderma lucidum by 148.45%, 75.32%, and 161.61%, respectively. Water stress induced the expression of the G. lucidum aquaporin (GlAQP) gene, which facilitated water transfer for microbial growth. Compared to wild type (WT), exposure to water stress increased growth inhibition rate, ROS level, and GA content of GlAQP-silenced strains by 37 to 41%, 36 to 38%, and 25%, respectively. Furthermore, at the early stage of fermentation in GlAQP-silenced strains, water stress resulted in 16 to 17% and 9 to 10% lower ROS level and GA content compared to WT, respectively. However, in GlAQP-overexpressing strains, ROS level and GA content were 22 to 24% and 12 to 13% higher than in WT, respectively. In GlAQP-silenced strains, water stress at the late stage resulted in 35 to 37% and 29 to 30% higher ROS level and GA content, respectively, while in GlAQP-overexpressing strains, levels were 16 to 17% and 9% lower than WT, respectively. Cross talk between GlAQP and NOX positively regulated the GA biosynthesis of G. lucidum via ROS under water stress at the early stage but this regulation became negative at the late stage. This study deepens the understanding of fungal signaling transduction under water stress and provides a reference for analyzing environmental factors that influence the regulation of the fungal secondary metabolism. IMPORTANCE Ganoderma lucidum is an advanced basidiomycete that produces medicinally active secondary metabolites (especially ganoderic acid [GA]) with high commercial value. Water stress imposes an important environmental challenge to G. lucidum. The mechanism of GA biosynthesis under water stress and the role of G. lucidum aquaporin (GlAQP) during its biosynthesis remain unclear. Moreover, the effect of the relationship between GlAQP and NADPH oxidase (NOX) on the level of reactive oxygen species and GA production under water stress is unknown. This study provides information on the biological response mechanism of G. lucidum to water stress. A new theory on the cell signaling cascade of G. lucidum tolerance to water stress is provided that also incorporates the biosynthesis of secondary metabolites involved in NOX and GlAQP. American Society for Microbiology 2022-11-02 /pmc/articles/PMC9784773/ /pubmed/36321895 http://dx.doi.org/10.1128/spectrum.01297-22 Text en Copyright © 2022 Zhu et al. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Research Article
Zhu, Quanyu
Ren, Ang
Ding, Juan
He, Jian
Zhao, Mingwen
Jiang, Ailiang
Zhou, Xiaolin
Wang, Jieying
He, Qin
Cross Talk between GlAQP and NOX Modulates the Effects of ROS Balance on Ganoderic Acid Biosynthesis of Ganoderma lucidum under Water Stress
title Cross Talk between GlAQP and NOX Modulates the Effects of ROS Balance on Ganoderic Acid Biosynthesis of Ganoderma lucidum under Water Stress
title_full Cross Talk between GlAQP and NOX Modulates the Effects of ROS Balance on Ganoderic Acid Biosynthesis of Ganoderma lucidum under Water Stress
title_fullStr Cross Talk between GlAQP and NOX Modulates the Effects of ROS Balance on Ganoderic Acid Biosynthesis of Ganoderma lucidum under Water Stress
title_full_unstemmed Cross Talk between GlAQP and NOX Modulates the Effects of ROS Balance on Ganoderic Acid Biosynthesis of Ganoderma lucidum under Water Stress
title_short Cross Talk between GlAQP and NOX Modulates the Effects of ROS Balance on Ganoderic Acid Biosynthesis of Ganoderma lucidum under Water Stress
title_sort cross talk between glaqp and nox modulates the effects of ros balance on ganoderic acid biosynthesis of ganoderma lucidum under water stress
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9784773/
https://www.ncbi.nlm.nih.gov/pubmed/36321895
http://dx.doi.org/10.1128/spectrum.01297-22
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