Endophytic Fungus Drives Nodulation and N<sub>2</sub> Fixation Attributable to Specific Root Exudates

ABSTRACT Endophytic fungi play important roles in the modification of ecosystem productivity; however, the underlying mechanisms are only partly understood. A 2-year field plot experiment verified that the endophytic fungus Phomopsis liquidambaris increased peanut (Arachis hypogaea L.) yields and si...

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Autores principales: Xing-Guang Xie, Feng-Min Zhang, Teng Yang, Yan Chen, Xiao-Gang Li, Chuan-Chao Dai
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Publicado: American Society for Microbiology 2019
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spelling oai:doaj.org-article:94276f5f166446e1bdc6cbd63e0e7c7d2021-11-15T16:22:09ZEndophytic Fungus Drives Nodulation and N<sub>2</sub> Fixation Attributable to Specific Root Exudates10.1128/mBio.00728-192150-7511https://doaj.org/article/94276f5f166446e1bdc6cbd63e0e7c7d2019-08-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.00728-19https://doaj.org/toc/2150-7511ABSTRACT Endophytic fungi play important roles in the modification of ecosystem productivity; however, the underlying mechanisms are only partly understood. A 2-year field plot experiment verified that the endophytic fungus Phomopsis liquidambaris increased peanut (Arachis hypogaea L.) yields and significantly increased nodulation and N2 fixation regardless of whether N fertilizers were added. Root exudates collected from P. liquidambaris-colonized plants significantly improved nodulation and N2 fixation. Rhizosphere stimulation experiments further showed that colonized root exudates had significantly decreased soil nitrate (NO3−) concentrations, with decreased abundance and diversity of ammonia oxidizing archaea (AOA). In contrast, the abundance and diversity of diazotrophs significantly increased, and most diazotrophs identified were peanut nodulation-related strains (Bradyrhizobium sp.). P. liquidambaris symbiosis increased the expression of phenolic and flavonoid synthesis-related genes, and the derived phenolics and flavonoids could effectively increase the chemotaxis, biofilm formation, and nodC gene expression (nodulation-related biological processes) of the Bradyrhizobium strain. Metabolic pattern analysis showed that phenolics and flavonoids are more likely to accumulate to higher levels in the rhizosphere soil of peanuts colonized with P. liquidambaris. Finally, a synthetic root exudate experiment further confirmed the underlying mechanisms for the P. liquidambaris-induced improvement in nodulation and N2 fixation, i.e., that the specific root exudates derived from P. liquidambaris colonization decrease nitrate concentration and increase the population and biological activities of peanut nodulation-related Bradyrhizobium species, which beneficially enhance peanut-Bradyrhizobium interactions. Therefore, this study is the first to provide new insight into a positive relationship between an exotic endophytic fungus, crop nodulation, and N2 fixation increase. IMPORTANCE Endophytic fungi play an important role in balancing the ecosystem and boosting host growth; however, the underpinning mechanisms remain poorly understood. Here, we found that endophytic fungal colonization with P. liquidambaris significantly increased the productivity, nodulation, and N2 fixation of peanuts through the secretion of specific root exudates. We provide a reasonable mechanism explaining how P. liquidambaris promotes peanut nodulation and N2 fixation, whereby the specific root exudates produced by P. liquidambaris colonization decrease rhizosphere soil nitrate (NO3−) and increase the population and biological activities of peanut-nodulating-related Bradyrhizobium strains, which is beneficial to enhancing the peanut-Bradyrhizobium symbiotic interaction. Our study provides reliable empirical evidence to show the mechanism of how an exotic endophytic fungus drives an increase in nodulation and N2 fixation, which will be helpful in erecting a resource-efficient and sustainable agricultural system.Xing-Guang XieFeng-Min ZhangTeng YangYan ChenXiao-Gang LiChuan-Chao DaiAmerican Society for MicrobiologyarticleArachis hypogaea L.Bradyrhizobiumendophytic fungus Phomopsis liquidambaris (Phomopsis/Diaporthe)nodulation and N2 fixationphenolic and flavonoid compoundsroot exudatesMicrobiologyQR1-502ENmBio, Vol 10, Iss 4 (2019)
institution DOAJ
collection DOAJ
language EN
topic Arachis hypogaea L.
Bradyrhizobium
endophytic fungus Phomopsis liquidambaris (Phomopsis/Diaporthe)
nodulation and N2 fixation
phenolic and flavonoid compounds
root exudates
Microbiology
QR1-502
spellingShingle Arachis hypogaea L.
Bradyrhizobium
endophytic fungus Phomopsis liquidambaris (Phomopsis/Diaporthe)
nodulation and N2 fixation
phenolic and flavonoid compounds
root exudates
Microbiology
QR1-502
Xing-Guang Xie
Feng-Min Zhang
Teng Yang
Yan Chen
Xiao-Gang Li
Chuan-Chao Dai
Endophytic Fungus Drives Nodulation and N<sub>2</sub> Fixation Attributable to Specific Root Exudates
description ABSTRACT Endophytic fungi play important roles in the modification of ecosystem productivity; however, the underlying mechanisms are only partly understood. A 2-year field plot experiment verified that the endophytic fungus Phomopsis liquidambaris increased peanut (Arachis hypogaea L.) yields and significantly increased nodulation and N2 fixation regardless of whether N fertilizers were added. Root exudates collected from P. liquidambaris-colonized plants significantly improved nodulation and N2 fixation. Rhizosphere stimulation experiments further showed that colonized root exudates had significantly decreased soil nitrate (NO3−) concentrations, with decreased abundance and diversity of ammonia oxidizing archaea (AOA). In contrast, the abundance and diversity of diazotrophs significantly increased, and most diazotrophs identified were peanut nodulation-related strains (Bradyrhizobium sp.). P. liquidambaris symbiosis increased the expression of phenolic and flavonoid synthesis-related genes, and the derived phenolics and flavonoids could effectively increase the chemotaxis, biofilm formation, and nodC gene expression (nodulation-related biological processes) of the Bradyrhizobium strain. Metabolic pattern analysis showed that phenolics and flavonoids are more likely to accumulate to higher levels in the rhizosphere soil of peanuts colonized with P. liquidambaris. Finally, a synthetic root exudate experiment further confirmed the underlying mechanisms for the P. liquidambaris-induced improvement in nodulation and N2 fixation, i.e., that the specific root exudates derived from P. liquidambaris colonization decrease nitrate concentration and increase the population and biological activities of peanut nodulation-related Bradyrhizobium species, which beneficially enhance peanut-Bradyrhizobium interactions. Therefore, this study is the first to provide new insight into a positive relationship between an exotic endophytic fungus, crop nodulation, and N2 fixation increase. IMPORTANCE Endophytic fungi play an important role in balancing the ecosystem and boosting host growth; however, the underpinning mechanisms remain poorly understood. Here, we found that endophytic fungal colonization with P. liquidambaris significantly increased the productivity, nodulation, and N2 fixation of peanuts through the secretion of specific root exudates. We provide a reasonable mechanism explaining how P. liquidambaris promotes peanut nodulation and N2 fixation, whereby the specific root exudates produced by P. liquidambaris colonization decrease rhizosphere soil nitrate (NO3−) and increase the population and biological activities of peanut-nodulating-related Bradyrhizobium strains, which is beneficial to enhancing the peanut-Bradyrhizobium symbiotic interaction. Our study provides reliable empirical evidence to show the mechanism of how an exotic endophytic fungus drives an increase in nodulation and N2 fixation, which will be helpful in erecting a resource-efficient and sustainable agricultural system.
format article
author Xing-Guang Xie
Feng-Min Zhang
Teng Yang
Yan Chen
Xiao-Gang Li
Chuan-Chao Dai
author_facet Xing-Guang Xie
Feng-Min Zhang
Teng Yang
Yan Chen
Xiao-Gang Li
Chuan-Chao Dai
author_sort Xing-Guang Xie
title Endophytic Fungus Drives Nodulation and N<sub>2</sub> Fixation Attributable to Specific Root Exudates
title_short Endophytic Fungus Drives Nodulation and N<sub>2</sub> Fixation Attributable to Specific Root Exudates
title_full Endophytic Fungus Drives Nodulation and N<sub>2</sub> Fixation Attributable to Specific Root Exudates
title_fullStr Endophytic Fungus Drives Nodulation and N<sub>2</sub> Fixation Attributable to Specific Root Exudates
title_full_unstemmed Endophytic Fungus Drives Nodulation and N<sub>2</sub> Fixation Attributable to Specific Root Exudates
title_sort endophytic fungus drives nodulation and n<sub>2</sub> fixation attributable to specific root exudates
publisher American Society for Microbiology
publishDate 2019
url https://doaj.org/article/94276f5f166446e1bdc6cbd63e0e7c7d
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