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The Trichoderma harzianum Kelch Protein ThKEL1 Plays a Key Role in Root Colonization and the Induction of Systemic Defense in Brassicaceae Plants.

ABSTRACT: The fungal genus Trichoderma includes strains with biocontrol and/or biostimulant potential and is recognized as a source of genes with biotechnological value. In a previous study the Kelch domain protein, encoded by the Thkel1 gene of Trichoderma harzianum T34, was found to confer tolerance to salt stress when expressed in plants of Arabidopsis thaliana. In the present work, we have overexpressed Thkel1 in rapeseed plants in order to generate an additional biotechnological tool for analyzing the role of this gene in Trichoderma-plant interactions. The overexpression of this gene in Brassicaceae plants improves responses to pathogens through the induction of systemic defenses mediated by jasmonic acid, facilitates root colonization by modulating the myrosinase activity, and, as a result, increases plant productivity. These effects were also observed in Thkel1 overexpressing plants subjected to abiotic stress conditions. Additionally, the differences detected in root colonization levels by T. harzianum wild type and Thkel1 silenced transformants between Arabidopsis or rapeseed and tomato plants indicate that ThKEL1 interacts in different ways in Brassicaceae and non-Brassicaceae plants.

SUBMITTER: Poveda J

PROVIDER: S-EPMC6873215 | biostudies-literature | 2019

REPOSITORIES: biostudies-literature

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The Trichoderma harzianum Kelch Protein ThKEL1 Plays a Key Role in Root Colonization and the Induction of Systemic Defense in Brassicaceae Plants.

Poveda Jorge J Hermosa Rosa R Monte Enrique E Nicolás Carlos C

Frontiers in plant science 20191115

The fungal genus Trichoderma includes strains with biocontrol and/or biostimulant potential and is recognized as a source of genes with biotechnological value. In a previous study the Kelch domain protein, encoded by the Thkel1 gene of Trichoderma harzianum T34, was found to confer tolerance to salt stress when expressed in plants of Arabidopsis thaliana. In the present work, we have overexpressed Thkel1 in rapeseed plants in order to generate an additional bio ...[more]

PMID: 31803213

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Project description:Numerous microbial root symbionts are known to induce different levels of enhanced plant protection against a variety of pathogens. However, more recent studies have demonstrated that beneficial microbes are able to induce plant systemic resistance that confers some degree of protection against insects. Here, we report how treatments with the fungal biocontrol agent Trichoderma atroviride strain P1 in tomato plants induce responses that affect pest insects with different feeding habits: the noctuid moth Spodoptera littoralis (Boisduval) and the aphid Macrosiphum euphorbiae (Thomas). We observed that the tomato plant-Trichoderma P1 interaction had a negative impact on the development of moth larvae and on aphid longevity. These effects were attributed to a plant response induced by Trichoderma that was associated with transcriptional changes of a wide array of defense-related genes. While the impact on aphids could be related to the up-regulation of genes involved in the oxidative burst reaction, which occur early in the defense reaction, the negative performance of moth larvae was associated with the enhanced expression of genes encoding for protective enzymes (i.e., Proteinase inhibitor I (PI), Threonine deaminase, Leucine aminopeptidase A1, Arginase 2, and Polyphenol oxidase) that are activated downstream in the defense cascade. In addition, Trichoderma P1 produced alterations in plant metabolic pathways leading to the production and release of volatile organic compounds (VOCs) that are involved in the attraction of the aphid parasitoid Aphidius ervi, thus reinforcing the indirect plant defense barriers. Our findings, along with the evidence available in the literature, indicate that the outcome of the tripartite interaction among plant, Trichoderma, and pests is highly specific and only a comprehensive approach, integrating both insect phenotypic changes and plant transcriptomic alterations, can allow a reliable prediction of its potential for plant protection.

Project description:Beneficial fungi in the genus Trichoderma are among the most widespread biocontrol agents of plant pathogens. Their role in triggering plant defenses against pathogens has been intensely investigated, while, in contrast, very limited information is available on induced barriers active against insects. The growing experimental evidence on this latter topic looks promising, and paves the way toward the development of Trichoderma strains and/or consortia active against multiple targets. However, the predictability and reproducibility of the effects that these beneficial fungi is still somewhat limited by the lack of an in-depth understanding of the molecular mechanisms underlying the specificity of their interaction with different crop varieties, and on how the environmental factors modulate this interaction. To fill this research gap, here we studied the transcriptome changes in tomato plants (cultivar "Dwarf San Marzano") induced by Trichoderma harzianum (strain T22) colonization and subsequent infestation by the aphid Macrosiphum euphorbiae. A wide transcriptome reprogramming, related to metabolic processes, regulation of gene expression and defense responses, was induced both by separate experimental treatments, which showed a synergistic interaction when concurrently applied. The most evident expression changes of defense genes were associated with the multitrophic interaction Trichoderma-tomato-aphid. Early and late genes involved in direct defense against insects were induced (i.e., peroxidase, GST, kinases and polyphenol oxidase, miraculin, chitinase), along with indirect defense genes, such as sesquiterpene synthase and geranylgeranyl phosphate synthase. Targeted and untargeted semi-polar metabolome analysis revealed a wide metabolome alteration showing an increased accumulation of isoprenoids in Trichoderma treated plants. The wide array of transcriptomic and metabolomics changes nicely fit with the higher mortality of aphids when feeding on Trichoderma treated plants, herein reported, and with the previously observed attractiveness of these latter toward the aphid parasitoid Aphidius ervi. Moreover, Trichoderma treated plants showed the over-expression of transcripts coding for several families of defense-related transcription factors (bZIP, MYB, NAC, AP2-ERF, WRKY), suggesting that the fungus contributes to the priming of plant responses against pest insects. Collectively, our data indicate that Trichoderma treatment of tomato plants induces transcriptomic and metabolomic changes, which underpin both direct and indirect defense responses.

Project description:Trichoderma spp. are versatile opportunistic plant symbionts which can colonize the apoplast of plant roots. Microarrays analysis of Arabidopsis thaliana roots inoculated with Trichoderma asperelloides T203, coupled with qPCR analysis of 137 stress responsive genes and transcription factors, revealed wide gene transcript reprogramming, proceeded by a transient repression of the plant immune responses supposedly to allow root colonization. Enhancement in the expression of WRKY18 and WRKY40, which stimulate JA-signaling via suppression of JAZ repressors and negatively regulate the expression of the defense genes FMO1, PAD3 and CYP71A13, was detected in Arabidopsis roots upon Trichoderma colonization. Reduced root colonization was observed in the wrky18/wrky40 double mutant line, while partial phenotypic complementation was achieved by over-expressing WRKY40 in the wrky18 wrky40 background. On the other hand increased colonization rate was found in roots of the FMO1 knockout mutant. Trichoderma spp. stimulate plant growth and resistance to a wide range of adverse environmental conditions. Arabidopsis and cucumber (Cucumis sativus L.) plants treated with Trichoderma prior to salt stress imposition show significantly improved seed germination. In addition, Trichoderma treatment affects the expression of several genes related to osmo-protection and general oxidative stress in roots of both plants. The MDAR gene coding for monodehydroascorbate reductase is significantly up-regulated and, accordingly, the pool of reduced ascorbic acid was found to be increased in Trichoderma treated plants. 1-Aminocyclopropane-1-carboxylate (ACC)-deaminase silenced Trichoderma mutants were less effective in providing tolerance to salt stress, suggesting that Trichoderma, similarly to ACC deaminase producing bacteria, can ameliorate plant growth under conditions of abiotic stress, by lowering ameliorating increases in ethylene levels as well as promoting an elevated antioxidative capacity.

Dataset Information

The Trichoderma harzianum Kelch Protein ThKEL1 Plays a Key Role in Root Colonization and the Induction of Systemic Defense in Brassicaceae Plants.

Publications

The <i>Trichoderma harzianum</i> Kelch Protein ThKEL1 Plays a Key Role in Root Colonization and the Induction of Systemic Defense in Brassicaceae Plants.

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