Flooding impairs plant resistance to piercing-sucking insects via ethylene-mediated suppression of callose deposition
- PMID: 40948149
- DOI: 10.1002/ps.70221
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.
Keywords: PDLP; aphid; callose; ethylene; flooding; whitefly.
© 2025 Society of Chemical Industry.
References
REFERENCES
-
- Bolan S, Padhye LP, Jasemizad T, Govarthanan M, Karmegam N, Wijesekara H et al., Impacts of climate change on the fate of contaminants through extreme weather events. Sci Total Environ 909:168388 (2024).
-
- Tellman B, Sullivan JA, Kuhn C, Kettner AJ, Doyle CS, Brakenridge GR et al., Satellite imaging reveals increased proportion of population exposed to floods. Nature 596:80–86 (2021).
-
- Kaur G, Singh G, Motavalli PP, Nelson KA, Orlowski JM and Golden BR, Impacts and management strategies for crop production in waterlogged or flooded soils: a review. Agron J 112:1475–1501 (2020).
-
- Schroeder LM and Lindelöw Å, Response of Ips typographus (Scolytidae: coleoptera) and other bark‐ and wood‐boring beetles to a flash‐flood event. Scand J For Res 18:218–224 (2012).
-
- Nakamura M, Utsumi S, Miki T and Ohgushi T, Flood initiates bottom‐up cascades in a tri‐trophic system: host plant regrowth increases densities of a leaf beetle and its predators. J Anim Ecol 74:683–691 (2005).