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Silica nanoparticles enhance disease resistance in Arabidopsis plants

Abstract

In plants, pathogen attack can induce an immune response known as systemic acquired resistance that protects against a broad spectrum of pathogens. In the search for safer agrochemicals, silica nanoparticles (SiO2 NPs; food additive E551) have recently been proposed as a new tool. However, initial results are controversial, and the molecular mechanisms of SiO2 NP-induced disease resistance are unknown. Here we show that SiO2 NPs, as well as soluble Si(OH)4, can induce systemic acquired resistance in a dose-dependent manner, which involves the defence hormone salicylic acid. Nanoparticle uptake and action occurred exclusively through the stomata (leaf pores facilitating gas exchange) and involved extracellular adsorption in the air spaces in the spongy mesophyll of the leaf. In contrast to the treatment with SiO2 NPs, the induction of systemic acquired resistance by Si(OH)4 was problematic since high Si(OH)4 concentrations caused stress. We conclude that SiO2 NPs have the potential to serve as an inexpensive, highly efficient, safe and sustainable alternative for plant disease protection.

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Fig. 1: SiO2 NPs under investigation.
Fig. 2: TEM of SiO2 NP distribution and physiological effects in Arabidopsis leaves.
Fig. 3: Enhanced local and systemic disease resistance in wild-type Col-0 Arabidopsis to P. syringae induced by SiO2 NPs or Si(OH)4.
Fig. 4: SiO2 NPs confer SAR in a dose-dependent manner.
Fig. 5: Dynamic range for SAR induced in distal leaves by SiO2 NPs in A. thaliana, and model summarizing the observed plant-defence-enhancing actions of SiO2 NPs and Si(OH)4.
Fig. 6: SiO2 NPs induce disease resistance based on SA-dependent pathway.

Data availability

The datasets that support the findings of the current study are available in the Zenodo repository with the identifier https://doi.org/10.5281/zenodo.4131137. Additional data related to this study are available from the corresponding authors upon reasonable request.

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Acknowledgements

M.E.-S. was supported by the Swiss State Secretariat for Education, Research and Innovation by a Swiss Government Excellence Scholarship for Foreign Scholars. F.S. and M.M. were supported by the Swiss National Science Foundation under the Ambizione grant ‘Enhancing Legume Defenses’ (168187) and Innosuisse (project 38515.1 IP-EE). We are grateful to N. Schäppi for his help with the graphic design and M. Schorderet for excellent technical assistance with microtoming. This work benefitted from support from the Swiss National Science Foundation through the National Centerof Competence in Research Bio-Inspired Materials. This research was also supported by the Adolphe Merkle Foundation and the University of Fribourg.

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Contributions

M.E.-S., F.S. and F.M. conceived and designed the study. F.S. led the team, rationally designed the SiO2 NPs to induce optimal plant defence, performed initial germination tests to establish the dosing regimen, contributed to the mechanistic understanding of silica and with plant TEM and has drawn the artwork. M.M. synthesized and characterized the SiO2 NPs. A.M. cultured the Arabidopsis plants and conducted the C. elegans experiments. D.R. provided access to his microtome and a technician that trained F.S. in microtoming. M.E.-S. performed all the Arabidopsis experiments and their statistical evaluation and wrote the manuscript draft with contributions by F.S. (figures and text) and F.M. (text). F.M. contributed to the mechanistic understanding of the gene expression results and molecular mechanisms of SAR. The manuscript was critically reviewed by A.P.-F., B.R.-R. and D.R. All the co-authors read and approved the manuscript before submission.

Corresponding authors

Correspondence to Mohamed El-Shetehy or Fabienne Schwab.

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Any opinions, findings, conclusions or recommendations expressed in this material are those of the authors and do not necessarily reflect the views of the Swiss National Science Foundation or the government. This work has not been subjected to Swiss National Science Foundation review, and no official endorsement should be inferred. F.S. and M.M. have a patent pending on a SiO2 NP plant growth enhancer. F.S. was supported by Innosuisse (project no. 38515.1 IP-EE). Other than that, the authors have declared no conflict of interest and are responsible for the content and writing of the article.

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El-Shetehy, M., Moradi, A., Maceroni, M. et al. Silica nanoparticles enhance disease resistance in Arabidopsis plants. Nat. Nanotechnol. (2020). https://doi.org/10.1038/s41565-020-00812-0

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