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Trichoderma harzianum Peptaibols Stimulate Plant Plasma Membrane H⁺-ATPase Activity.

ABSTRACT: Because of their ability to promote growth, act as biopesticides, and improve abiotic stress tolerance, Trichoderma spp. have been used for plant seed coating. However, the mechanism for the promotion of plant growth remains unknown. In this study, we investigate the effect of fungal extracts on the plant plasma membrane (PM) H⁺-ATPase, which is essential for plant growth and often a target of plant-associated microbes. We show that Trichoderma harzianum extract increases H⁺-ATPase activity, and by fractionation and high-resolution mass spectrometry (MS), we identify the activating components trichorzin PA (tPA) II and tPA VI that belong to the class of peptaibols. Peptaibols are nonribosomal peptides that can integrate into membranes and form indiscriminate ion channels, which causes pesticidal activity. To further investigate peptaibol-mediated H⁺-ATPase activation, we compare the effect of tPA II and VI to that of the model peptaibol alamethicin (AlaM). We show that AlaM increases H⁺-ATPase turnover rates in a concentration-dependent manner, with a peak in activity measured at 31.25 μM, above which activity decreases. Using fluorescent probes and light scattering, we find that the AlaM-mediated increase in activity is not correlated to increased membrane fluidity or vesicle integrity, whereas the activity decrease at high AlaM concentrations is likely due to PM overloading of AlaM pores. Overall, our results suggest that the symbiosis of fungi and plants, specifically related to peptaibols, is a concentration-dependent balance, where peptaibols do not act only as biocontrol agents but also as plant growth stimulants.

SUBMITTER: Bjork PK

PROVIDER: S-EPMC10536087 | biostudies-literature | 2023 Sep

REPOSITORIES: biostudies-literature

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Trichoderma harzianum Peptaibols Stimulate Plant Plasma Membrane H+-ATPase Activity.

Bjørk Peter Klemmed PK Johansen Nicolai Tidemand NT Havshøi Nanna Weise NW Rasmussen Silas Anselm SA Ipsen Johan Ørskov JØ Isbrandt Thomas T Larsen Thomas Ostenfeld TO Fuglsang Anja Thoe AT

ACS omega 20230914 38

Because of their ability to promote growth, act as biopesticides, and improve abiotic stress tolerance, Trichoderma spp. have been used for plant seed coating. However, the mechanism for the promotion of plant growth remains unknown. In this study, we investigate the effect of fungal extracts on the plant plasma membrane (PM) H+-ATPase, which is essential for plant growth and often a target of plant-associated microbes. We show that Trichoderma harzianum extract increase ...[more]

PMID: 37779967

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Project 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.

Dataset Information

Trichoderma harzianum Peptaibols Stimulate Plant Plasma Membrane H⁺-ATPase Activity.

Publications

<i>Trichoderma harzianum</i> Peptaibols Stimulate Plant Plasma Membrane H<sup>+</sup>-ATPase Activity.

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