Flooding impairs plant resistance to piercing-sucking insects via ethylene-mediated suppression of callose deposition.

Abstract

BACKGROUND Flooding, a common natural disaster, frequently triggers outbreaks of herbivorous insects on plants. However, the molecular mechanisms underlying how flooding stress compromises plant defense against herbivores remain poorly understood. RESULTS This study establishes that flooding significantly compromises plant resistance to herbivores. We found that this effect is mediated by enhanced ethylene production, a key hypoxia response triggered by flooding. Crucially, exogenous application of the ethylene precursor 1-aminocyclopropane-1-carboxylic acid (ACC) mimicked the flooding phenotype, leading to a significant increase in the fecundity of both whitefly (Bemisia tabaci (Gennadius)) and aphid (Myzus persicae (Sulzer)) compared to control plants. Further investigation revealed that both flooding stress and ACC treatment substantially diminished callose accumulation - a critical physical barrier - at feeding sites induced by these herbivores. Mechanistically, this reduction in callose deposition was attributed to the down-regulation of PLASMODESMATA-LOCATED PROTEIN 5 (AtPDLP5), a key positive regulator of callose biosynthesis. Genetic evidence using Atpdlp5 mutants confirmed their reduced callose deposition and enhanced susceptibility to herbivores. CONCLUSION In summary, we demonstrate that flooding-induced ethylene signaling impairs herbivore resistance by inhibiting callose deposition via the down-regulation of AtPDLP5. This study elucidates how plants cope with concurrent biotic and abiotic stresses, revealing the molecular mechanisms underlying enhanced herbivore susceptibility in flooded plants. © 2025 Society of Chemical Industry.