Colonization of root endophytic fungus Serendipita indica improves drought tolerance of Pinus taeda seedlings by regulating metabolome and proteome
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SUBMITTER: Wu C
PROVIDER: S-EPMC10978793 | biostudies-literature | 2024 Jan
REPOSITORIES: biostudies-literature
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Project description:Specialised metabolites produced during plant-fungal associations often define how symbiosis between the plant and the fungus proceeds. They also play a role in the establishment of additional interactions between the symbionts and other organisms present in the niche. However, specialised metabolism and its products are sometimes overlooked when studying plant-microbe interactions. This limits our understanding of the specific symbiotic associations and potentially future perspectives of their application in agriculture. In this study, we used the interaction between the root endophyte Serendipita indica and tomato (Solanum lycopersicum) plants to explore how specialised metabolism of the host plant is regulated upon a mutualistic symbiotic association. To do so, tomato seedlings were inoculated with S. indica chlamydospores and subjected to RNAseq analysis. Gene expression of the main tomato specialised metabolism pathways was compared between roots and leaves of endophyte-colonised plants and tissues of endophyte-free plants. S. indica colonisation resulted in a strong transcriptional response in the leaves of colonised plants. Furthermore, the presence of the fungus in plant roots appears to induce expression of genes involved in the biosynthesis of lignin-derived compounds, polyacetylenes, and specific terpenes in both roots and leaves, whereas pathways producing glycoalkaloids and flavonoids were expressed in lower or basal levels.
| S-EPMC8778627 | biostudies-literature
Project description:Interactions between plant-associated fungi and their hosts are characterized by a continuous crosstalk of chemical molecules. Specialized metabolites are often produced during these associations and play important roles in the symbiosis between the plant and the fungus, as well as in the establishment of additional interactions between the symbionts and other organisms present in the niche. Serendipita indica, a root endophytic fungus from the phylum Basidiomycota, is able to colonize a wide range of plant species, conferring many benefits to its hosts. The genome of S. indica possesses only few genes predicted to be involved in specialized metabolite biosynthesis, including a putative terpenoid synthase gene (SiTPS). In our experimental setup, SiTPS expression was upregulated when the fungus colonized tomato roots compared to its expression in fungal biomass growing on synthetic medium. Heterologous expression of SiTPS in Escherichia coli showed that the produced protein catalyzes the synthesis of a few sesquiterpenoids, with the alcohol viridiflorol being the main product. To investigate the role of SiTPS in the plant-endophyte interaction, an SiTPS-over-expressing mutant line was created and assessed for its ability to colonize tomato roots. Although overexpression of SiTPS did not lead to improved fungal colonization ability, an in vitro growth-inhibition assay showed that viridiflorol has antifungal properties. Addition of viridiflorol to the culture medium inhibited the germination of spores from a phytopathogenic fungus, indicating that SiTPS and its products could provide S. indica with a competitive advantage over other plant-associated fungi during root colonization.
| S-EPMC8234273 | biostudies-literature
Project description:Most plants in nature establish symbiotic associations with endophytic fungi in soil. Beneficial endophytic fungi induce a systemic response in the aboveground parts of the host plant, thus promoting the growth and fitness of host plants. Meanwhile, temperature elevation from climate change widely affects global plant biodiversity as well as crop quality and yield. Over the past decades, great progresses have been made in the response of plants to high ambient temperature and to symbiosis with endophytic fungi. However, little is known about their synergistic effect on host plants. The endophytic fungus Serendipita indica colonizes the roots of a wide range of plants, including Arabidopsis. Based on the Arabidopsis-S. indica symbiosis experimental system, we analyzed the synergistic effect of high ambient temperature and endophytic fungal symbiosis on host plants. By transcriptome analysis, we found that DNA replication-related genes were significantly upregulated during the systemic response of Arabidopsis aboveground parts to S. indica colonization. Plant hormones, such as jasmonic acid (JA) and ethylene (ET), play important roles in plant growth and systemic responses. We found that high ambient temperature repressed the JA and ET signaling pathways of Arabidopsis aboveground parts during the systemic response to S. indica colonization in roots. Meanwhile, PIF4 is the central hub transcription factor controlling plant thermosensory growth under high ambient temperature in Arabidopsis. PIF4 is also involving JA and/or ET signaling pathway. We found that PIF4 target genes overlapped with many differentially expressed genes (DEGs) during the systemic response, and further showed that the growth promotion efficiency of S. indica on the pif4 mutant was higher than that on the wild-type plants. In short, our data showed that high ambient temperature strengthened the growth promotion effect of S. indica fungi on the aboveground parts of the host plant Arabidopsis, and the growth promotion effect of the systemic response under high ambient temperature was regulated by PIF4.
| S-EPMC8966885 | biostudies-literature
Project description:Drought stress is one of major environmental stresses affecting plant growth and yield. Although Pinus taeda trees are planted in rainy southern China, local drought sometime occurs and can last several months, further affecting their growth and resin production. In this study, P. taeda seedlings were treated with long-term drought (42 d), and then targeted and untargeted metabolomics analysis were carried out to evaluate drought tolerance of P. taeda. Targeted metabolomics analysis showed that levels of some sugars, phytohormones, and amino acids significantly increased in the roots and needles of water-stressed (WS) P. taeda seedlings, compared with well-watered (WW) pine seedlings. These metabolites included sucrose in pine roots, the phytohormones abscisic acid and sacylic acid in pine needles, the phytohormone gibberellin (GA4) and the two amino acids, glycine and asparagine, in WS pine roots. Compared with WW pine seedlings, the neurotransmitter acetylcholine significantly increased in needles of WS pine seedlings, but significantly reduced in their roots. The neurotransmitters L-glutamine and hydroxytyramine significantly increased in roots and needles of WS pine seedlings, respectively, compared with WW pine seedlings, but the neurotransmitter noradrenaline significantly reduced in needles of WS pine seedlings. Levels of some unsaturated fatty acids significantly reduced in roots or needles of WS pine seedlings, compared with WW pine seedlings, such as linoleic acid, oleic acid, myristelaidic acid, myristoleic acid in WS pine roots, and palmitelaidic acid, erucic acid, and alpha-linolenic acid in WS pine needles. However, three saturated fatty acids significantly increased in WS pine seedlings, i.e., dodecanoic acid in WS pine needles, tricosanoic acid and heptadecanoic acid in WS pine roots. Untargeted metabolomics analysis showed that levels of some metabolites increased in WS pine seedlings, especially sugars, long-chain lipids, flavonoids, and terpenoids. A few of specific metabolites increased greatly, such as androsin, piceatanol, and panaxatriol in roots and needles of WS pine seedlings. Comparing with WW pine seedlings, it was found that the most enriched pathways in WS pine needles included flavone and flavonol biosynthesis, ABC transporters, diterpenoid biosynthesis, plant hormone signal transduction, and flavonoid biosynthesis; in WS pine roots, the most enriched pathways included tryptophan metabolism, caffeine metabolism, sesquiterpenoid and triterpenoid biosynthesis, plant hormone signal transduction, biosynthesis of phenylalanine, tyrosine, and tryptophan. Under long-term drought stress, P. taeda seedlings showed their own metabolomics characteristics, and some new metabolites and biosynthesis pathways were found, providing a guideline for breeding drought-tolerant cultivars of P. taeda.
| S-EPMC9927248 | biostudies-literature
Project description:BackgroundSeptoria tritici blotch (STB) caused by fungus Zymoseptoria tritici, is one of the important wheat (Triticum aestivum L.) diseases difficult to control because of the lack of wheat resistant cultivars. The use of biological control agents is one possible way for triggering host plant resistance to biotic and abiotic stresses.ObjectiveIn this study, we examined the ability of Serendipita indica and Pseudomonas protegens CHA0-mCherry in inducing the local wheat cultivar Tajan resistance to STB.Materials and methodsThe interaction between biological control agents and the roots of wheat was evaluated. The experiment was conducted in a completely randomized design by three replicates. Spore suspension was supplied at concentrations of 107 and 109 for S. indica and bacteria isolate (CHA0-mCherry) respectively. Five treatments were applied including S. indica, CHA0-mCherry, S. indica and CHA0-mCherry co-inoculation, positive and negative control. Twenty-one days after inoculation, the interaction between biological agents and plant roots were evaluated through morphological traits and qPCR. The plant resistance, disease severity, and the correlation between resistance and disease severity were assessed. Pycnidial variation and agronomic traits were also evaluated.ResultsTwenty-one days after inoculation, both biological agents clearly colonized all treated roots of all treatments except in control plants as demonstrated by qPCR analysis. Chlamydospores were observed in the S. indica-treated hosts with the CHA0-mCherry colonizing assessment showing 5×109 CFU g-1 in the root. The asexual phase of the fungal pathogen, pycnidial diameter, was reduced in S. indica treated plants more considerably than in the other treatments. There was a positive correlation between resistance and disease severity mean when calculated by Pearson's correlation. There was a significant difference between the root length, fresh, and dry weight of root. Spore density was inversely correlated to resistance and disease severity, when compared with control, with CHA0-mCherry being the most effective in reducing the spore density. S. indica was the most effective in promoting root growth and stem biomass, when compared with control.ConclusionsSerendipita indica and Pseudomonas protegens CHA0-mCherry colonies showed a potential biological control activity and efficiently enhanced the plant resistance to Z. tritici in the treated wheat roots. The microbial biological control agents are very practical in crop protection against plant disease and can be very useful in sustainable agriculture.AbbreviationsPLSN: percentage of leave surface necrosis, DPI: day past inoculation, PLACL: percentage of leaf area covered by lesions, PPMLA: pycnidia per millimeter in leaf area.
| S-EPMC8358168 | biostudies-literature
Project description:Serendipita (=Piriformospora) indica is a fungal endophytic symbiont with the capabilities to enhance plant growth and confer resistance to different stresses. However, the application of this fungus in the field has led to inconsistent results, perhaps due to antagonism with other microbes. Here, we studied the impact of individual bacterial isolates from the endophytic bacterial community on the in vitro growth of S. indica. We further analyzed how combinations of bacteria and S. indica influence plant growth and protection against the phytopathogens Fusarium oxysporum and Rhizoctonia solani. Bacterial strains of the genera Bacillus, Enterobacter and Burkholderia negatively affected S. indica growth on plates, whereas Mycolicibacterium, Rhizobium, Paenibacillus strains and several other bacteria from different taxa stimulated fungal growth. To further explore the potential of bacteria positively interacting with S. indica, four of the most promising strains belonging to the genus Mycolicibacterium were selected for further experiments. Some dual inoculations of S. indica and Mycolicibacterium strains boosted the beneficial effects triggered by S. indica, further enhancing the growth of tomato plants, and alleviating the symptoms caused by the phytopathogens F. oxysporum and R. solani. However, some combinations of S. indica and bacteria were less effective than individual inoculations. By analyzing the genomes of the Mycolicibacterium strains, we revealed that these bacteria encode several genes predicted to be involved in the stimulation of S. indica growth, plant development and tolerance to abiotic and biotic stresses. Particularly, a high number of genes related to vitamin and nitrogen metabolism were detected. Taking into consideration multiple interactions on and inside plants, we showed in this study that some bacterial strains may induce beneficial effects on S. indica and could have an outstanding influence on the plant-fungus symbiosis.
| S-EPMC6930893 | biostudies-literature
Project description:Thiamine, or vitamin B1 plays an indispensable role as a cofactor in crucial metabolic reactions including glycolysis, pentose phosphate pathway and the tricarboxylic acid cycle in all living organisms. Thiamine has been shown to play a role in plant adaptation toward biotic and abiotic stresses. The modulation of thiamine biosynthetic genes in oil palm seedlings was evaluated in response to root colonization by endophytic Hendersonia toruloidea. Seven-month-old oil palm seedlings were inoculated with H. toruloidea and microscopic analyses were performed to visualize the localization of endophytic H. toruloidea in oil palm roots. Transmission electron microscopy confirmed that H. toruloidea colonized cortical cells. The expression of thiamine biosynthetic genes and accumulation of total thiamine in oil palm seedlings were also evaluated. Quantitative real-time PCR was performed to measure transcript abundances of four key thiamine biosynthesis genes (THI4, THIC, TH1, and TPK) on days 1, 7, 15, and 30 in response to H. toruloidea colonization. The results showed an increase of up to 12-fold in the expression of all gene transcripts on day 1 post-inoculation. On days 7, 15, and 30 post-inoculation, the relative expression levels of these genes were shown to be downregulated. Thiamine accumulation was observed on day 7 post-colonization and subsequently decreased until day 30. This work provides the first evidence for the enhancement of thiamine biosynthesis by endophytic colonization in oil palm seedlings.
| S-EPMC5651052 | biostudies-literature
Project description:Serendipita indica (former Piriformospora indica) is a non-obligate endophytic fungus and generally a plant growth and defence promoter with high potential to be used in agriculture. However, S. indica may switch from biotrophy to saprotrophy losing its plant growth promoting traits. Our aim was to understand if the free-living stage growth conditions (namely C availability) regulate S. indica's phenotype, and its potential as plant-growth-promoting-microbe (PGPM). We grew S. indica in its free-living stage under increasing C availabilities (2-20 g L-1 of glucose or sucrose). We first characterised the effect of C availability during free-living stage growth on fungal phenotype: colonies growth and physiology (plasma membrane proton pumps, stable isotopic signatures, and potential extracellular decomposing enzymes). The effect of the C availability during the free-living stage of the PGPM was evaluated on wheat. We observed that C availability during the free-living stage regulated S. indica's growth, ultrastructure and physiology, resulting in two distinct colony phenotypes: compact and explorer. The compact phenotype developed at low C, used peptone as the major C and N source, and displayed higher decomposing potential for C providing substrates; while the explorer phenotype developed at high C, used glucose and sucrose as major C sources and casein and yeast extract as major N sources, and displayed higher decomposing potential for N and P providing substrates. The C availability, or the C/N ratio, during the free-living stage left a legacy to the symbiosis stage, regulating S. indica's potential to promote plant growth: wheat growth promotion by the explorer phenotype was ± 40% higher than that by the compact phenotype. Our study highlights the importance of considering microbial ecology in designing PGPM/biofertilizers. Further studies are needed to test the phenotypes under more extreme conditions, and to understand if the in vitro acquired characteristics persist under field conditions.
| S-EPMC7536269 | biostudies-literature
Project description:Extracellular adenosine 5'-triphosphate (eATP) is an essential signaling molecule that mediates different cellular processes through its interaction with membrane-associated receptor proteins in animals and plants. eATP regulates plant growth, development, and responses to biotic and abiotic stresses. Its accumulation in the apoplast induces ROS production and cytoplasmic calcium increase mediating a defense response to invading microbes. We show here that perception of extracellular nucleotides, such as eATP, is important in plant-fungus interactions and that during colonization by the beneficial root endophyte Serendipita indica eATP accumulates in the apoplast at early symbiotic stages. Using liquid chromatography-tandem mass spectrometry, and cytological and functional analysis, we show that S. indica secrets SiE5'NT, an enzymatically active ecto-5'-nucleotidase capable of hydrolyzing nucleotides in the apoplast. Arabidopsis thaliana lines producing extracellular SiE5'NT are significantly better colonized, have reduced eATP levels, and altered responses to biotic stresses, indicating that SiE5'NT functions as a compatibility factor. Our data suggest that extracellular bioactive nucleotides and their perception play an important role in fungus-root interactions and that fungal-derived enzymes can modify apoplastic metabolites to promote fungal accommodation.
| S-EPMC6362346 | biostudies-literature
Project description:Conifers have complex defense responses to initial attacks by insects and pathogens that can have cascading effects on success of subsequent colonizers. However, drought can affect a plant's ability to respond to biotic agents by potentially altering the resources needed for the energetically costly production of induced defense chemicals. We investigated the impact of reduced water on induced chemical defenses of jack pine (Pinus banksiana) seedlings from initial attack by biotic agents and resistance to subsequent challenge inoculation with a pathogenic fungal associate of mountain pine beetle (Dendroctonus ponderosae), Grosmannia clavigera. Applications of phytohormones (methyl salicylate and methyl jasmonate) and G. clavigera were used for initial induction of defenses. Monoterpene concentrations varied with initial induction from fungal and phytohormone application while watering treatment had no effect. Seedlings treated with G. clavigera and methyl jasmonate had the greatest monoterpene concentrations compared to the control and methyl salicylate-treated seedlings. However, the monoterpene response to the challenge inoculation varied with watering treatments, not with prior induction treatments, with lower monoterpene concentrations in fungal lesions on seedlings in the low to moderate watering treatments compared to normal watering treatment. Furthermore, prior induction from phytohormones resulted in systemic cross-induction of resistance to G. clavigera under normal watering treatment but susceptibility under low watering treatment. Seedlings stressed by low water conditions, which also had lower stomatal conductance than seedlings in the normal watering treatment, likely allocated resources to initial defense response but were left unable to acquire further resources for subsequent responses. Our results demonstrate that drought can affect interactions among tree-infesting organisms through systemic cross-induction of susceptibility.
| S-EPMC5720781 | biostudies-literature