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Interactions between plant‐beneficial microorganisms in a consortium: Streptomyces microflavus and Trichoderma harzianum

The construction of microbial consortia is challenging due to many variables to be controlled, including the cross‐compatibility of the selected strains and their additive or synergistic effects on plants. In this work, we investigated the interactions in vitro, in planta, and at the molecular level...

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Autores principales: Prigigallo, Maria Isabella, Staropoli, Alessia, Vinale, Francesco, Bubici, Giovanni
Formato: Online Artículo Texto
Lenguaje:English
Publicado: John Wiley and Sons Inc. 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10686133/
https://www.ncbi.nlm.nih.gov/pubmed/37464583
http://dx.doi.org/10.1111/1751-7915.14311
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author Prigigallo, Maria Isabella
Staropoli, Alessia
Vinale, Francesco
Bubici, Giovanni
author_facet Prigigallo, Maria Isabella
Staropoli, Alessia
Vinale, Francesco
Bubici, Giovanni
author_sort Prigigallo, Maria Isabella
collection PubMed
description The construction of microbial consortia is challenging due to many variables to be controlled, including the cross‐compatibility of the selected strains and their additive or synergistic effects on plants. In this work, we investigated the interactions in vitro, in planta, and at the molecular level of two elite biological control agents (BCAs), that is Streptomyces microflavus strain AtB‐42 and Trichoderma harzianum strain M10, to understand their attitude to cooperate in a consortium. In vitro, we observed a strong cross‐antagonism between AtB‐42 and M10 in agar plates due to diffusible metabolites and volatile organic compounds. In liquid co‐cultures, M10 hindered the growth of AtB‐42 very likely because of secondary metabolites and strong competition for the nutrients. The interaction in the co‐culture induced extensive transcriptional reprogramming in both strains, especially in the pathways related to ribosomes, protein synthesis, and oxidoreductase activity, suggesting that each strain recognized the counterpart and activated its defence responses. The metabolome of both strains was also significantly affected. In contrast, in the soil, M10 growth was partially contrasted by AtB‐42. The roots of tomato seedlings inoculated with the consortium appeared smaller than the control and single‐strain‐inoculated plants, indicating that plants diverted some energy from the development to defence activation, as evidenced by the leaf transcriptome. The consortium induced a stronger transcriptional change compared to the single inoculants, as demonstrated by a higher number of differentially expressed genes. Although the cross‐antagonism observed in vitro, the two strains exerted a synergistic effect on tomato seedlings by inducing resistance responses stronger than the single inoculants. Our observations pose a question on the usefulness of the sole in vitro assays for selecting BCAs to construct a consortium. In vivo experiments should be preferred, and transcriptomics may greatly help to elucidate the activity of the BCAs beyond the phenotypic effects on the plant.
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spelling pubmed-106861332023-11-30 Interactions between plant‐beneficial microorganisms in a consortium: Streptomyces microflavus and Trichoderma harzianum Prigigallo, Maria Isabella Staropoli, Alessia Vinale, Francesco Bubici, Giovanni Microb Biotechnol Special Issue: Part 2: End Hunger: Enhancing Crop Yields with Microbes The construction of microbial consortia is challenging due to many variables to be controlled, including the cross‐compatibility of the selected strains and their additive or synergistic effects on plants. In this work, we investigated the interactions in vitro, in planta, and at the molecular level of two elite biological control agents (BCAs), that is Streptomyces microflavus strain AtB‐42 and Trichoderma harzianum strain M10, to understand their attitude to cooperate in a consortium. In vitro, we observed a strong cross‐antagonism between AtB‐42 and M10 in agar plates due to diffusible metabolites and volatile organic compounds. In liquid co‐cultures, M10 hindered the growth of AtB‐42 very likely because of secondary metabolites and strong competition for the nutrients. The interaction in the co‐culture induced extensive transcriptional reprogramming in both strains, especially in the pathways related to ribosomes, protein synthesis, and oxidoreductase activity, suggesting that each strain recognized the counterpart and activated its defence responses. The metabolome of both strains was also significantly affected. In contrast, in the soil, M10 growth was partially contrasted by AtB‐42. The roots of tomato seedlings inoculated with the consortium appeared smaller than the control and single‐strain‐inoculated plants, indicating that plants diverted some energy from the development to defence activation, as evidenced by the leaf transcriptome. The consortium induced a stronger transcriptional change compared to the single inoculants, as demonstrated by a higher number of differentially expressed genes. Although the cross‐antagonism observed in vitro, the two strains exerted a synergistic effect on tomato seedlings by inducing resistance responses stronger than the single inoculants. Our observations pose a question on the usefulness of the sole in vitro assays for selecting BCAs to construct a consortium. In vivo experiments should be preferred, and transcriptomics may greatly help to elucidate the activity of the BCAs beyond the phenotypic effects on the plant. John Wiley and Sons Inc. 2023-07-18 /pmc/articles/PMC10686133/ /pubmed/37464583 http://dx.doi.org/10.1111/1751-7915.14311 Text en © 2023 The Authors. Microbial Biotechnology published by Applied Microbiology International and John Wiley & Sons Ltd. https://creativecommons.org/licenses/by/4.0/This is an open access article under the terms of the http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.
spellingShingle Special Issue: Part 2: End Hunger: Enhancing Crop Yields with Microbes
Prigigallo, Maria Isabella
Staropoli, Alessia
Vinale, Francesco
Bubici, Giovanni
Interactions between plant‐beneficial microorganisms in a consortium: Streptomyces microflavus and Trichoderma harzianum
title Interactions between plant‐beneficial microorganisms in a consortium: Streptomyces microflavus and Trichoderma harzianum
title_full Interactions between plant‐beneficial microorganisms in a consortium: Streptomyces microflavus and Trichoderma harzianum
title_fullStr Interactions between plant‐beneficial microorganisms in a consortium: Streptomyces microflavus and Trichoderma harzianum
title_full_unstemmed Interactions between plant‐beneficial microorganisms in a consortium: Streptomyces microflavus and Trichoderma harzianum
title_short Interactions between plant‐beneficial microorganisms in a consortium: Streptomyces microflavus and Trichoderma harzianum
title_sort interactions between plant‐beneficial microorganisms in a consortium: streptomyces microflavus and trichoderma harzianum
topic Special Issue: Part 2: End Hunger: Enhancing Crop Yields with Microbes
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10686133/
https://www.ncbi.nlm.nih.gov/pubmed/37464583
http://dx.doi.org/10.1111/1751-7915.14311
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