Self-Assembled Nanonematicide Induces Adverse Effects on Oxidative Stress, Succinate Dehydrogenase Activity, and ATP Generation

ACS Appl Mater Interfaces. 2023 Jul 5;15(26):31173-31184. doi: 10.1021/acsami.3c03634. Epub 2023 Jun 20.

Abstract

Long-term overuse of chemical nematicides has resulted in low control efficacy toward destructive root-knot nematodes, and continuous development in nanotechnology is supposed to enhance the utilization efficiency of nematicides to meet practical needs. Herein, a cationic star polymer (SPc) was constructed to load fluopyram (flu) and prepare a flu nanoagent. Hydrogen bonding and van der Waals forces facilitated the self-assembly of the flu nanoagent, leading to the breakdown of self-aggregated flu and reducing its particle size to 60 nm. The bioactivity of flu was remarkably improved, with the half lethal concentration 50 from 8.63 to 5.70 mg/L due to the help of SPc. Transcriptome analysis found that a large number of transport-related genes were upregulated in flu nanoagent-exposed nematodes, while the expression of many energy-related genes was disturbed, suggesting that the enhanced uptake of flu nanoagents by nematodes might lead to the disturbance of energy synthesis and metabolism. Subsequent experiments confirmed that exposure to flu nanoagents markedly increased the reactive oxygen species (ROS) level of nematodes. Compared to flu treatment alone, succinate dehydrogenase (SDH) activity was inhibited in flu nanoagent-exposed nematodes with an increase in the pIC50 from 8.81 to 11.04, which further interfered with adenosine triphosphate (ATP) biosynthesis. Furthermore, the persistence of SPc-loaded flu in soil was prolonged by 2.33 times at 50 days after application. The protective effects of flu nanoagents on eggplant seedlings were significantly improved in both greenhouse and field trials, and the root-knot number was consistently smaller in roots treated with flu nanoagents than in those treated with flu alone. Overall, this study successfully constructed a self-assembled flu nanoagent with amplified effects on oxidative stress, SDH activity, and ATP generation, leading to highly effective control of root-knot nematodes in the field.

Keywords: ATP generation; SDH activity; drug delivery; nanocarrier; nanonematicide.

MeSH terms

  • Adenosine Triphosphate* / metabolism
  • Antinematodal Agents / pharmacology
  • Oxidative Stress
  • Reactive Oxygen Species / metabolism
  • Succinate Dehydrogenase* / metabolism
  • Succinate Dehydrogenase* / pharmacology

Substances

  • Succinate Dehydrogenase
  • Adenosine Triphosphate
  • Antinematodal Agents
  • Reactive Oxygen Species
  • N-(2-(3-chloro-5-(trifluoromethyl)-2-pyridyl)ethyl)-alpha,alpha,alpha-trifluoro-o-toluamide