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Drought dramatically affects plant growth and yield. A previous study indicated that endophytic fungus Phomopsis liquidambaris can improve the drought resistance of peanuts, which is related with the root arbuscular mycorrhizal fungi (AMF) community; however, how root endophytes mediate AMF assembly to affect plant drought resistance remains unclear. Here, we explored the mechanism by which endophytic fungus recruits AMF symbiotic partners via rhizodeposits to improve host drought resistance. The results showed that Ph. liquidambaris enhanced peanut drought resistance by enriching the AMF genus Claroideoglomus of the rhizosphere. Furthermore, metabolomic analysis indicated that Ph. liquidambaris significantly promoted isoformononetin and salicylic acid (SA) synthesis in rhizodeposits, which were correlated with the increase in Claroideoglomus abundance following Ph. liquidambaris inoculation. Coinoculation experiments confirmed that isoformononetin and SA could enrich Claroideoglomus etunicatum in the rhizosphere, thereby improving the drought resistance. This study highlights the crucial role of fungal consortia in plant stress resistance.

Endophytic symbioses between plants and fungi are a dominant feature of many terrestrial ecosystems, yet little is known about the signaling that defines these symbiotic associations. Hydrogen peroxide (H2O2) is recognized as a key signal mediating the plant adaptive response to both biotic and abiotic stresses. However, the role of H2O2 in plant-fungal symbiosis remains elusive. Using a combination of physiological analysis, plant and fungal deletion mutants, and comparative transcriptomics, we reported that various environmental conditions differentially affect the interaction between Arabidopsis and the root endophyte Phomopsis liquidambaris, and link this process to alterations in H2O2 levels and H2O2 fluxes across root tips. We found that enhanced H2O2 efflux leading to a moderate increase in H2O2 levels at the plant-fungal interface is required for maintaining plant-fungal symbiosis. Disturbance of plant H2O2 homeostasis compromises the symbiotic ability of plant roots. Moreover, the fungus-regulated H2O2 dynamics modulate the rhizosphere microbiome by selectively enriching for the phylum Cyanobacteria, with strong antioxidant defenses. Our results demonstrated that the regulation of H2O2 dynamics at the plant-fungal interface affects the symbiotic outcome in response to external conditions and highlight the importance of the root endophyte in reshaping the rhizosphere microbiota., (© The Author(s) 2024. Published by Oxford University Press on behalf of the Society for Experimental Biology. All rights reserved. For commercial re-use, please contact reprints@oup.com for reprints and translation rights for reprints. All other permissions can be obtained through our RightsLink service via the Permissions link on the article page on our site—for further information please contact journals.permissions@oup.com.)

Anthropogenic nitrogen inputs lead to a high ammonium (NH 4 + )/nitrate (NO 3 - ) ratio in the soil, which restricts hyphal spreading of soil fungi. Access of symbiotic fungi to roots is a prerequisite for plant-fungal interactions. Hyphosphere bacteria protect fungi from environmental stress, yet the impact of hyphosphere bacteria on adaptation of host fungi to NH 4 + -enriched conditions remains unclear. By developing soil microcosm assays, we report that a plant-symbiotic fungus, Phomopsis liquidambaris, harbors specific hyphosphere bacteria that facilitate hyphal spreading and assist in the root colonization in NH 4 + -enriched soil. Genetic manipulation, 16S rRNA gene analysis and coinoculation assays revealed that the genus Enterobacter was enriched in the hyphosphere of NH 4 + -sensitive wild-type compared to NH 4 + -enriched soil. Our study reveals the essential role of hyphosphere microorganism-based hyphal spreading in plant-fungal symbiosis establishment within nitrogen-affected agroecosystems.4 + :NO 3 - ratio following SZ2 inoculation. Microbial supplementation and inhibitor assays showed that AOA-mediated reduction in NH 4 + :NO 3 - ratio is responsible for SZ2-enhanced fungal adaptation to NH 4 + -enriched conditions. The Ph. liquidambaris-Enterobacter-AOA triple interaction promoted rice growth in NH 4 + -enriched soil. Our study reveals the essential role of hyphosphere microorganism-based hyphal spreading in plant-fungal symbiosis establishment within nitrogen-affected agroecosystems., (© 2023. The Author(s), under exclusive licence to International Society for Microbial Ecology.)

The role of flowering in root-fungal symbiosis is not well understood. Because flowering and fungal symbionts are supported by carbohydrates, we hypothesized that flowering modulates root-beneficial fungal associations through alterations in carbohydrate metabolism and transport. We monitored fungal colonization and soluble sugars in the roots of Arabidopsis thaliana following inoculation with a mutualistic fungus Phomopsis liquidambari across different plant developmental stages. Jasmonate signalling of wild-type plants, sugar transport, and root invertase of wild-type and jasmonate-insensitive plants were exploited to assess whether and how jasmonate-dependent sugar dynamics are involved in flowering-mediated fungal colonization alterations. We found that flowering restricts root-fungal colonization and activates root jasmonate signalling upon fungal inoculation. Jasmonates reduce the constitutive and fungus-induced accumulation of root glucose and fructose at the flowering stage. Further experiments with sugar transport and metabolism mutant lines revealed that root glucose and fructose positively influence fungal colonization. Diurnal, jasmonate-dependent inhibitions of sugar transport and soluble invertase activity were identified as likely mechanisms for flowering-mediated root sugar depletion upon fungal inoculation. Collectively, our results reveal that flowering drives root-fungus cooperation loss, which is related to jasmonate-dependent root soluble sugar depletion. Limiting the spread of root-fungal colonization may direct more resources to flower development., (© 2019 John Wiley & Sons Ltd.)

Aims: To explore if and how symbiotic Phomopsis liquidambari-rice system influences below-ground straw decomposition and then nitrogen(N) transformation in response to environmental N levels., Methods and Results: Litter bag experiments were utilized to trace the decay process during rice growth phases (seedling (T1), tillering (T2), heading (T3) and maturing (T4) stage), with (E+) and without endophyte (E-), under low (LN), medium (MN) and high nitrogen (HN) supply. Litter, soil and plant samples were collected to evaluate the decay process, N transformations, plant quality and relative abundance of soil ammonia-oxidizing archaea (AOA), ammonia-oxidizing bacteria (AOB) and P. liquidambari. The results showed that straw decomposition increased by 19·76% (LN, T2 stage), 14·05% (MN, T3 stage) and 16·88% (MN, T4 stage) in E+ pots when compared with E- pots. Further analysis revealed that no significant endophyte × N interaction was found for straw decay rate and that the decay rate was reduced by a higher N supply (LN, 37·16 ± 0·65%; MN, 32·27 ± 1·72%; HN, 29·44 ± 1·22%) at the T1 stage, whereas straw decay rate and N release increased by 9·38 and 11·16%, respectively, mainly by endophyte colonization at the T4 stage. The abundance of AOA and AOB were altered, corresponding with the decay rate. Soil mineral N, straw mineral N and plant quality were shown to increase in E+ pots, depending on environmental N conditions and growth phase. The yield increased by 2·98% for E+ plants under MN level., Conclusions: Symbiotic P. liquidambari-rice system promoted below-ground straw decomposition and N transformation, depending on environmental N levels and plant growth phase., Significance and Impact of the Study: This study provides evidence that fungal endophyte-plant systems are able to promote N transformation by increasing straw decomposition. A reasonable combination of N inputs could enhance its advantage in agriculture ecosystems., (© 2018 The Society for Applied Microbiology.)

The fungal endophyte Phomopsis liquidambari can improve nitrification rates and alter the abundance and composition of ammonia-oxidizers in the soil rhizosphere of rice. Aerenchyma is related to oxygen transport efficiency and contributes to the enhanced rhizospheric nitrification under flooding conditions. However, whether and how P. liquidambari affects aerenchyma formation is largely unknown. We therefore conducted pot and hydroponic experiments to investigate the changes of aerenchyma area, ethylene and indole-3-acetic acid (IAA) levels in rice with or without P. liquidambari infection. Our results showed that the larger aerenchyma area in rice roots with P. liquidambari inoculation was associated with markedly up-regulated expression of genes related to aerenchyma formation. Meanwhile, P. liquidambari inoculation substantially elevated root porosity (POR) and radial oxygen loss (ROL), leading to the enhancement of oxidation-reduction potential (ORP) under pot condition. Besides, P. liquidambari significantly increased IAA and ethylene levels in rice by stimulating the expression of genes involved in auxin and ethylene biosyntheses. Furthermore, auxin that partly acting upstream of ethylene signalling played an essential role in P. liquidambari-promoted aerenchyma formation. These results verified the direct contribution of P. liquidambari in promoting aerenchyma formation via the accumulation of IAA and ethylene in rice roots, which provides a constructive suggestion for improving hypoxia tolerance through plant-endophyte interactions., (Copyright © 2018 Elsevier Masson SAS. All rights reserved.)

Filamentous ascomycete Phomopsis sp. are common inhabitants of natural ecosystems and, as saprophytes, are largely responsible for the destructive decay of litterfall, promoting the carbon and nitrogen cycles. Phomopsis liquidambari B3 can establish mutualistic symbiosis with a broad spectrum of crop plants. Colonizing dynamics observations and a growth promotion assay of rice and Arabidopsis thaliana revealed that the B3 colonization strategy is host-adapted and resulted in different growth promotions influenced by N availability. However, the biochemical mechanisms and underlying genetics of the saprophyte transition to an endophyte are poorly understood. Here, the transcriptome features of generalist P. liquidambari and highlighted gene sets involved in the lifestyle transition from saprophytism to endophytism were reported. Most notable were genes for translation, ribosome biogenesis and MAPK signaling, several of which were only up-regulated in endophytic B3. Coordinated up-regulation of genes encoding enzymes involved in phenylalanine, tyrosine and tryptophan biosynthesis were preceded by secondary metabolite induction, which was encountered with host defense. Quantitative PCR validates the reliability of RNA-seq. Dissection at the molecular level facilitated a deeper understanding of P. liquidambari adaptation to hosts and the complex natural environment to play a role in sustainable agriculture and carbon and nitrogen cycles., (Copyright © 2017 Elsevier GmbH. All rights reserved.)

Atractylodes lancea is a well-known, but endangered, Chinese medicinal plant whose volatile oils are its main active components. As the volatile oil content in cultivated A. lancea is much lower than that in the wild herb, the application of microbes or related elicitors to promote growth and volatile oil accumulation in the cultivated herb is an important area of research. This study demonstrates that the endophytic bacterium Pseudomonas fluorescens ALEB7B isolated from the geo-authentic A. lancea can release several nitrogenous volatiles, such as formamide and N,N-dimethyl-formamide, which significantly promote the growth of non-infected A. lancea. Moreover, the main bacterial volatile benzaldehyde significantly promotes volatile oil accumulation in non-infected A. lancea via activating plant defense responses. Notably, the bacterial nitrogenous volatiles cannot be detected in the A. lancea - Pseudomonas fluorescens symbiont while the benzaldehyde can be detected, indicating the nitrogenous volatiles or their precursors may have been consumed by the host plant. This study firstly demonstrates that the interaction between plant and endophytic bacterium is not limited to the commonly known physical contact, extending the ecological functions of endophyte in the phytosphere and deepening the understandings about the symbiotic interaction., (Copyright © 2016 Elsevier Masson SAS. All rights reserved.)

In peanut continuous cropping soil, the application of fungal endophyte Phomopsis liquidambari B3 showed peanut pod yield promotion and root nodule number increase. P. liquidambari improved soil environment by degrading allelochemicals and thus promoted peanut pod yield. Furthermore, peanut yield promotion is in part due to the root nodule increase since nodular nitrogen fixation provides the largest source of nitrogen for peanut. However, it is unknown whether this nodule number increase is induced by fungal endophyte. We therefore conducted several pot experiments using vermiculite to investigate the effects of P. liquidambari on peanut-bradyrhizobium nodulation. Our results showed that P. liquidambari co-inoculated with bradyrhizobium increased root nodule number and shoot accumulated nitrogen by 28.25% and 29.71%, respectively. Nodulation dynamics analysis showed that P. liquidambari accelerated nodule initiation and subsequent nodule development. Meanwhile, P. liquidambari was able to colonize the peanut root as an endophyte. The dynamics of P. liquidambari and bradyrhizobial root colonization analysis showed that P. liquidambari inoculation significantly increased the rate of bradyrhizobial colonization. Furthermore, P. liquidambari inoculation significantly increased flavonoids synthesis-related enzymes activities, two common types of flavonoid (luteolin and quercetin-peanut rhizobial nod gene inducer) secretion and lateral root (peanut rhizobial infection site) formation, indicating that P. liquidambari altered the peanut nodulation-related physiological and metabolic activities. These obtained results confirmed the direct contribution of P. liquidambari in enhancing peanut-bradyrhizobium interaction, nodulation and yield., (Copyright © 2015 Elsevier Masson SAS. All rights reserved.)

Many studies have examined pair-wise interactions between plants and endophytes, while overlooking the interplays among multiple endosymbionts and their combined impacts on hosts. In this study, Atractylodes lancea plantlets were inoculated with endophytic fungus Acremonium strictum AL16, or endophytic bacterium Acinetobacter sp., or both, to investigate the impacts of the three-way symbiosis on the host. Our results showed that defense-related responses of the co-inoculated plantlets were delayed and weakened relative to plantlets with single inoculants, but no detrimental effects on phyto-physiology (growth, photosynthesis) were observed after combined inoculations. Quantitative PCR analysis verified a decrease in AL16 colonization density within plants after co-inoculation with the endobacteria. An in vitro assay was then performed to elucidate the suppressed plant defense responses and reduced fungal colonization by dual inoculation. The data showed that the presence of Acinetobacter sp. reduced AL16 colony diameter and spore germination rate without negatively affecting fungal morphology. Additionally, direct hyphal attachment of the bacterium to AL16 in vitro was visualized by scanning electronic microscopy. Therefore, we propose that a balanced and compatible symbiosis might require constraints conferred by the antagonistic endophyte Acinetobacter sp. on the fungus AL16 in the tripartite endophytic bacterium-fungus-plant system., (© 2013 WILEY-VCH Verlag GmbH & Co. KGaA, Weinheim.)