β-Cyclodextrin-optimized supramolecular nanovesicles enhance the droplet/foliage interface interactions and inhibition of succinate dehydrogenase (SDH) for efficient treatment of fungal diseases

Deng-Xuan Guo; Li Song; Jing-Han Yang; Xin-Yu He; Pan Liu; Pei-Yi Wang

doi:10.1186/s12951-024-02849-y

β-Cyclodextrin-optimized supramolecular nanovesicles enhance the droplet/foliage interface interactions and inhibition of succinate dehydrogenase (SDH) for efficient treatment of fungal diseases

J Nanobiotechnology. 2024 Sep 20;22(1):581. doi: 10.1186/s12951-024-02849-y.

Authors

Deng-Xuan Guo^#¹, Li Song^#¹, Jing-Han Yang¹, Xin-Yu He¹, Pan Liu¹, Pei-Yi Wang²

Affiliations

¹ State Key Laboratory of Green Pesticide, Key Laboratory of Green Pesticide and Agricultural Bioengineering, Ministry of Education, Center for Research and Development of Fine Chemicals of Guizhou University, Guiyang, 550025, China.
² State Key Laboratory of Green Pesticide, Key Laboratory of Green Pesticide and Agricultural Bioengineering, Ministry of Education, Center for Research and Development of Fine Chemicals of Guizhou University, Guiyang, 550025, China. pywang@gzu.edu.cn.

^# Contributed equally.

PMID: 39304921
DOI: 10.1186/s12951-024-02849-y

Abstract

Background: Plant fungal diseases present a major challenge to global agricultural production. Despite extensive efforts to develop fungicides, particularly succinate dehydrogenase inhibitors (SDHIs), their effectiveness is often limited by poor retention of fungicide droplets on hydrophobic leaves. The off-target losses and unintended release cause fungal resistance and severe environmental pollution.

Results: To update the structure of existing SDHIs and synchronously realize the efficient utilization, we have employed a sophisticated supramolecular strategy to optimize a structurally novel SDH inhibitor (AoH25), creating an innovative supramolecular SDH fungicide (AoH25@β-CD), driven by the host-guest recognition principle between AoH25 and β-cyclodextrin (β-CD). Intriguingly, AoH25@β-CD self-assembles into biocompatible supramolecular nanovesicles, which reinforce the droplet/foliage (liquid-solid) interface interaction and the effective wetting and retention on leaf surfaces, setting the foundation for enhancing fungicide utilization. Mechanistic studies revealed that AoH25@β-CD exhibited significantly higher inhibition of SDH (IC₅₀ = 1.56 µM) compared to fluopyram (IC₅₀ = 244.41 µM) and AoH25 alone (IC₅₀ = 2.29 µM). Additionally, AoH25@β-CD increased the permeability of cell membranes in Botryosphaeria dothidea, facilitating better penetration of active ingredients into pathogenic cells. Further experimental outcomes confirmed that AoH25@β-CD was 88.5% effective against kiwifruit soft rot at a low-dose of 100 µg mL^-1, outperforming commercial fungicides such as fluopyram (52.4%) and azoxystrobin (65.4%). Moreover, AoH25@β-CD showed broad-spectrum bioactivity against oilseed rape sclerotinia, achieving an efficacy of 87.2%, outstripping those of fluopyram (48.7%) and azoxystrobin (76.7%).

Conclusion: This innovative approach addresses key challenges related to fungicide deposition and resistance, improving the bioavailability of agricultural chemicals. The findings highlight AoH25@β-CD as a novel supramolecular SDH inhibitor, demonstrating its potential as an efficient and sustainable solution for plant disease management.

Keywords: Antifungal; Foliar deposition; Improved utilization; Supramolecular SDH inhibitors.

Abstract

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