Manganese-Enhanced Nanopesticides Augment Plant Resistance against Viral Infection via an Untapped Macroautophagy Pathway

Manganese is vital for plant growth and disease resistance but remains underutilized as a bioactive agent due to its toxicity at high concentrations. Here, an effective antiviral nanopesticide system utilizing Mn ions (Mn²⁺) within safe limits is described. Briefly, cellulose nanocrystals (CNCs) are employed as bio-sourced carrier surfaces and polydopamine (PDA) as a stabilizing and chelating agent for Mn²⁺. By impregnating Mn²⁺ onto PDA-coated CNCs, the stable CNC@PDA@Mn²⁺ (CPM) composite is fabricated. The CPM composite exhibits a substantially strengthened inhibitory effect on virus infectivity and curtails virus accumulation in Nicotiana benthamiana. The synergistic effects of CPM stem from its ability to directly disrupt viral particles and activate the plant-immunity-related antioxidant systems. Additionally, H₂O₂ generated by the CPM-activated superoxide dismutase potentially serves as a molecular signal to overexpress the disease-resistance gene harpin-induced 1 (NbHin1) by sulfinylating CCA1 Hiking Expedition and enhance its binding to NbHin1 promoter. Subsequently, this upregulation coordinates the activation of NbHin1-dependent macroautophagy, triggering multiple antiviral defense mechanisms. Thus, this design achieves highly potent broad-spectrum antiviral activity at low concentrations of manganese (16 µg mL⁻¹). Notably, this work pioneers the use of Mn²⁺ in triggering plant antiviral defense, offering a solid foundation for designing novel antiviral agents.