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.
This is a preview of subscription content, access via your institution
Access options
Access Nature and 54 other Nature Portfolio journals
Get Nature+, our best-value online-access subscription
$29.99 / 30 days
cancel any time
Subscribe to this journal
Receive 12 print issues and online access
$259.00 per year
only $21.58 per issue
Buy this article
- Purchase on Springer Link
- Instant access to full article PDF
Prices may be subject to local taxes which are calculated during checkout
Similar content being viewed by others
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.
References
White, J. C. & Gardea-Torresdey, J. Achieving food security through the very small. Nat. Nanotechnol. 13, 627–629 (2018).
Casey, W., Kinrade, S., Knight, C., Rains, D. & Epstein, E. Aqueous silicate complexes in wheat, Triticum aestivum L. Plant Cell Environ. 27, 51–54 (2004).
Ma, J. F. & Yamaji, N. Silicon uptake and accumulation in higher plants. Trends Plant Sci. 11, 392–397 (2006).
Choppin, G. R., Pathak, P. & Thakur, P. Polymerization and complexation behavior of silicic acid: a review. Main Group Met. Chem. 31, 53–72 (2008).
Bélanger, R. R., Bowen, P. A., Ehret, D. L. & Menzies, J. G. Soluble silicon—its role in crop and disease management of greenhouse crops. Plant Dis. 79, 329–336 (1995).
Abdel-Haliem, M. E., Hegazy, H. S., Hassan, N. S. & Naguib, D. M. Effect of silica ions and nano silica on rice plants under salinity stress. Ecol. Eng. 99, 282–289 (2017).
Luyckx, M., Hausman, J.-F., Lutts, S. & Guerriero, G. Silicon and plants: current knowledge and technological perspectives. Front. Plant Sci. 8, 411 (2017).
Slomberg, D. L. & Schoenfisch, M. H. Silica nanoparticle phytotoxicity to Arabidopsis thaliana. Environ. Sci. Technol. 46, 10247–10254 (2012).
Eichert, T., Kurtz, A., Steiner, U. & Goldbach, H. E. Size exclusion limits and lateral heterogeneity of the stomatal foliar uptake pathway for aqueous solutes and water-suspended nanoparticles. Physiol. Plant. 134, 151–160 (2008).
Schwab, F. et al. Barriers, pathways and processes for uptake, translocation and accumulation of nanomaterials in plants–critical review. Nanotoxicology 10, 257–278 (2016).
Jones, J. D. & Dangl, J. L. The plant immune system. Nature 444, 323–329 (2006).
Conrath, U. et al. Priming: getting ready for battle. Mol. Plant Microbe Interact. 19, 1062–1071 (2006).
Mauch-Mani, B., Baccelli, I., Luna, E. & Flors, V. Defense priming: an adaptive part of induced resistance. Annu. Rev. Plant Biol. 68, 485–512 (2017).
Ryals, J. A. et al. Systemic acquired resistance. Plant Cell 8, 1809–1819 (1996).
Ross, A. F. Systemic acquired resistance induced by localized virus infections in plants. Virology 14, 340–358 (1961).
Durrant, W. E. & Dong, X. Systemic acquired resistance. Annu. Rev. Phytopathol. 42, 185–209 (2004).
Mauch, F. et al. Manipulation of salicylate content in Arabidopsis thaliana by the expression of an engineered bacterial salicylate synthase. Plant J. 25, 67–77 (2001).
Wang, C. et al. Free radicals mediate systemic acquired resistance. Cell Rep. 7, 348–355 (2014).
El-Shetehy, M. et al. Nitric oxide and reactive oxygen species are required for systemic acquired resistance in plants. Plant Signal. Behav. 10, e998544 (2015).
Louws, F. et al. Field control of bacterial spot and bacterial speck of tomato using a plant activator. Plant Dis. 85, 481–488 (2001).
Romero, A., Kousik, C. & Ritchie, D. Resistance to bacterial spot in bell pepper induced by acibenzolar-S-methyl. Plant Dis. 85, 189–194 (2001).
Kim, S. G., Kim, K. W., Park, E. W. & Choi, D. Silicon-induced cell wall fortification of rice leaves: a possible cellular mechanism of enhanced host resistance to blast. Phytopathology 92, 1095–1103 (2002).
Wang, M. et al. Role of silicon on plant–pathogen interactions. Front. Plant Sci. 8, 701 (2017).
Liang, Y., Si, J. & Römheld, V. Silicon uptake and transport is an active process in Cucumis sativus. New Phytol. 167, 797–804 (2005).
van Bockhaven, J. et al. Silicon induces resistance to the brown spot fungus Cochliobolus miyabeanus by preventing the pathogen from hijacking the rice ethylene pathway. New Phytol. 206, 761–773 (2015).
Rouhani, M., Samih, M. & Kalantari, S. Insecticidal effect of silica and silver nanoparticles on the cowpea seed beetle, Callosobruchus maculatus F.(Col.: Bruchidae). J. Entomol. Res. 4, 297–305 (2013).
El-Helaly, A., El-Bendary, H., Abdel-Wahab, A., El-Sheikh, M. & Elnagar, S. The silica-nano particles treatment of squash foliage and survival and development of Spodoptera littoralis (Bosid.) larvae. J. Entomol. Zool. 4, 175–180 (2016).
Kunkel, B. N., Bent, A. F., Dahlbeck, D., Innes, R. W. & Staskawicz, B. J. RPS2, an Arabidopsis disease resistance locus specifying recognition of Pseudomonas syringae strains expressing the avirulence gene avrRpt2. Plant Cell 5, 865–875 (1993).
Chen, Z., Kloek, A. P., Boch, J., Katagiri, F. & Kunkel, B. N. The Pseudomonas syringae avrRpt2 gene product promotes pathogen virulence from inside plant cells. Mol. Plant Microbe Interact. 13, 1312–1321 (2000).
Exley, C. A possible mechanism of biological silicification in plants. Front. Plant Sci. 6, 853 (2015).
Bossert, D. et al. A hydrofluoric acid-free method to dissolve and quantify silica nanoparticles in aqueous and solid matrices. Sci. Rep. 9, 7938 (2019).
Schwab, F. & Maceroni, M. A controlled release silica-based nanoparticle composition, method of production and fertilization methods. Patent WO2020212526A1 (2020).
Ross, A. & Somssich, I. E. A DNA-based real-time PCR assay for robust growth quantification of the bacterial pathogen Pseudomonas syringae on Arabidopsis thaliana. Plant Methods 12, 48 (2016).
Sewelam, N., Kazan, K., Hüdig, M., Maurino, V. G. & Schenk, P. M. The AtHSP17. 4C1 gene expression is mediated by diverse signals that link biotic and abiotic stress factors with ROS and can be a useful molecular marker for oxidative stress. Int. J. Mol. Sci. 20, 3201 (2019).
An, C. & Mou, Z. Salicylic acid and its function in plant immunity. J. Integr. Plant Biol. 53, 412–428 (2011).
Nawrath, C. & Métraux, J.-P. Salicylic acid induction–deficient mutants of Arabidopsis express PR-2 and PR-5 and accumulate high levels of camalexin after pathogen inoculation. Plant Cell 11, 1393–1404 (1999).
Ye, M. et al. Priming of jasmonate-mediated antiherbivore defense responses in rice by silicon. Proc. Natl Acad. Sci. USA 110, E3631–E3639 (2013).
Ziaee, M. & Ganji, Z. Insecticidal efficacy of silica nanoparticles against Rhyzopertha dominica F. and Tribolium confusum Jacquelin du Val. J. Plant Prot. Res. 56, 250–256 (2016).
La, V. H. et al. Salicylic acid improves drought-stress tolerance by regulating the redox status and proline metabolism in Brassica rapa. Hortic. Environ. Biotechnol. 60, 31–40 (2019).
Krajíčková, A. & Mejstřik, V. The effect of fly ash particles on the plugging of stomata. Environ. Pollut. A 36, 83–93 (1984).
Burkhardt, J., Basi, S., Pariyar, S. & Hunsche, M. Stomatal penetration by aqueous solutions—an update involving leaf surface particles. New Phytol. 196, 774–787 (2012).
Amrullah, D. S. & Junaedi, A. Influence of nano-silica on the growth of rice plant (Oryza sativa L.). Asian J. Agric. Res. 9, 33–37 (2015).
Karunakaran, G. et al. Effect of nanosilica and silicon sources on plant growth promoting rhizobacteria, soil nutrients and maize seed germination. IET Nanobiotechnol. 7, 70–77 (2013).
Cameron, R. K., Pavia, N. K., Lamb, C. J. & Dixon, R. A. Accumulation of salicylic acid and PR-1 gene transcripts in relation to the systemic acquired resistance (SAR) response induced by Pseudomonas syringae pv. tomato in Arabidopsis. Physiol. Mol. Plant Pathol. 55, 121–130 (1999).
Malamy, J., Carr, J. P., Klessig, D. F. & Raskin, I. Salicylic acid: a likely endogenous signal in the resistance response of tobacco to viral infection. Science 250, 1002–1004 (1990).
Fauteux, F., Chain, F., Belzile, F., Menzies, J. G. & Bélanger, R. R. The protective role of silicon in the Arabidopsis–powdery mildew pathosystem. Proc. Natl Acad. Sci. USA 103, 17554–17559 (2006).
Jiang, N., Fan, X., Lin, W., Wang, G. & Cai, K. Transcriptome analysis reveals new insights into the bacterial wilt resistance mechanism mediated by silicon in tomato. Int. J. Mol. Sci. 20, 761 (2019).
Lavers, A. Guidelines on Good Practice for Ground Application of Pesticides (Food and Agriculture Organization of the United Nations, 2001).
Schreiber, L. Polar paths of diffusion across plant cuticles: new evidence for an old hypothesis. Ann. Bot. 95, 1069–1073 (2005).
Kookana, R. S. et al. Nanopesticides: guiding principles for regulatory evaluation of environmental risks. J. Agric. Food Chem. 62, 4227–4240 (2014).
Kah, M., Tufenkji, N. & White, J. C. Nano-enabled strategies to enhance crop nutrition and protection. Nat. Nanotechnol. 14, 532–540 (2019).
Bourquin, J. et al. Biodistribution, clearance, and long-term fate of clinically relevant nanomaterials. Adv. Mater. 30, e1704307 (2018).
Mebert, A. M., Baglole, C. J., Desimone, M. F. & Maysinger, D. Nanoengineered silica: properties, applications and toxicity. Food Chem. Toxicol. 109, 753–770 (2017).
Chen, Z. et al. Pseudomonas syringae type III effector AvrRpt2 alters Arabidopsis thaliana auxin physiology. Proc. Natl. Acad. Sci. USA 104, 20131–20136 (2007).
El-Shetehy, M. et al. Silica nanoparticles enhance disease resistance in Arabidopsis plants—raw data. Zenodo https://doi.org/10.5281/zenodo.4131137 (2020).
Stöber, W., Fink, A. & Bohn, E. Controlled growth of monodisperse silica spheres in the micron size range. J. Colloid Interface Sci. 26, 62–69 (1968).
Stegemeier, J. P. et al. Speciation matters: bioavailability of silver and silver sulfide nanoparticles to alfalfa (Medicago sativa). Environ. Sci. Technol. 49, 8451–8460 (2015).
Bustin, S. A. et al. The MIQE guidelines: minimum information for publication of quantitative real-time PCR experiments. Clin. Chem. 55, 611–622 (2009).
Rao, X., Huang, X., Zhou, Z. & Lin, X. An improvement of the 2ˆ (–delta delta CT) method for quantitative real-time polymerase chain reaction data analysis. Biostat. Bioinforma. Biomath. 3, 71 (2013).
Czechowski, T., Stitt, M., Altmann, T., Udvardi, M. K. & Scheible, W.-R. Genome-wide identification and testing of superior reference genes for transcript normalization in Arabidopsis. Plant Physiol. 139, 5–17 (2005).
Tomczynska, I., Stumpe, M. & Mauch, F. A conserved RxLR effector interacts with host RABA-type GTPases to inhibit vesicle-mediated secretion of antimicrobial proteins. Plant J. 95, 187–203 (2018).
Joller, C. et al. S-methyl methanethiosulfonate: promising late blight inhibitor or broad range toxin? Pathogens 9, 496 (2020).
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.
Author information
Authors and Affiliations
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
Ethics declarations
Competing interests
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.
Additional information
Peer review information Nature Nanotechnology thanks Rai Kookana and the other, anonymous, reviewer(s) for their contribution to the peer review of this work.
Publisher’s note Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary information
Supplementary Information
Supplementary Figs. 1–3, Tables 1 and 2 and text.
Rights and permissions
About this article
Cite this article
El-Shetehy, M., Moradi, A., Maceroni, M. et al. Silica nanoparticles enhance disease resistance in Arabidopsis plants. Nat. Nanotechnol. 16, 344–353 (2021). https://doi.org/10.1038/s41565-020-00812-0
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1038/s41565-020-00812-0
This article is cited by
-
Influence of a nanoscale coating on plucking fingers and stainless steel on attachment and detachment of Salmonella Enteritidis, Escherichia coli and Campylobacter jejuni
Folia Microbiologica (2024)
-
Is silicon beneficial for cassava (Manihot esculenta Crantz)?
Plant and Soil (2024)
-
Novel carbon nanoparticles derived from Bougainvillea modulate vegetative growth via auxin–cytokinin signaling in Arabidopsis
Chemical Papers (2024)
-
Silicon Nanoparticle Application on Thymus serpyllum Under Drought and Salinity Stress in Vitro
BioNanoScience (2024)
-
Nanoparticles in plant resistance against bacterial pathogens: current status and future prospects
Molecular Biology Reports (2024)