Zinc nanoparticles: Mode of action and efficacy against boscalid-resistant Alternaria alternata isolates

Anastasios A Malandrakis; Nektarios Kavroulakis; Constantinos V Chrysikopoulos

doi:10.1016/j.scitotenv.2022.154638

Zinc nanoparticles: Mode of action and efficacy against boscalid-resistant Alternaria alternata isolates

Sci Total Environ. 2022 Jul 10:829:154638. doi: 10.1016/j.scitotenv.2022.154638. Epub 2022 Mar 18.

Authors

Anastasios A Malandrakis¹, Nektarios Kavroulakis², Constantinos V Chrysikopoulos³

Affiliations

¹ School of Environmental Engineering, Technical University of Crete, 73100 Chania, Greece. Electronic address: tasmal@aua.gr.
² Hellenic Agricultural Organization "Demeter", Institute for Olive Tree, Subtropical Plants and Viticulture, Agrokipio-Souda, 73164 Chania, Greece.
³ School of Environmental Engineering, Technical University of Crete, 73100 Chania, Greece.

PMID: 35314223
DOI: 10.1016/j.scitotenv.2022.154638

Abstract

The antifungal potential of ZnO-NPs against Alternaria alternata isolates with reduced sensitivity to the succinate dehydrogenase inhibitor (SDHI) boscalid, resulting from target site modifications, was evaluated in vitro and in vivo. ZnO-NPs could effectively inhibit mycelial growth in a dose-dependent way in both boscalid (BOSC) sensitive (BOSC-S) and resistant (BOSC-R) isolates. The fungitoxic effect of ZnO-NPs against the pathogen was significantly enhanced when combined with boscalid compared to the individual treatments in all phenotype cases (BOSC-S/R) both in vitro and in vivo. Fungitoxic effect of ZnO-NPs could be, at least partly, attributed to zinc ion release as indicated by the positive correlation between sensitivities to the nanoparticles and their ionic counterpart ZnSO₄ and the alleviation of the ZnO-NPs fungitoxic action in the presence of the strong chelating agent EDTA. The superior effectiveness of ZnO-NPs against A. alternata, compared to ZnSO_4, could be due to nanoparticle properties interfering with cellular ion homeostasis mechanisms. The observed additive action of the oxidative phosphorylation-uncoupler fluazinam (FM) against all phenotypes indicates a possible role of ATP-dependent ion efflux mechanism in the mode of action of ZnO-NPs. A potential role of ROS production in the fungitoxic action of ZnO-NPs was evident by the additive/synergistic action of salicylhydroxamate (SHAM), which blocks the alternative oxidase antioxidant action. Mixture of ZnO-NPs and boscalid, resulting in a "capping" effect for the nanoparticles and significantly reducing their mean size, probably accounted for the synergistic effect of the mixture against both sensitive and resistant A. alternata isolates. Summarizing, results indicated that ZnO-NPs can be effectively used against A. alternata both alone or in combination with boscalid, providing an effective tool for combating SDHI-resistance and reducing the environmental fingerprint of synthetic fungicides.

Keywords: Carboxamides; Nanofungicides; Plant pathogens; Synergism; ZnO-NPs.

MeSH terms

Alternaria
Biphenyl Compounds
Drug Resistance, Fungal
Metal Nanoparticles* / toxicity
Nanoparticles*
Niacinamide / analogs & derivatives
Zinc / pharmacology
Zinc Oxide* / pharmacology

Substances

Biphenyl Compounds
Niacinamide
2-chloro-N-(4-chlorobiphenyl-2-yl)nicotinamide
Zinc
Zinc Oxide

Supplementary concepts

Alternaria alternata