1. Academic Validation
  2. TRPA1-kinase axis polarization: Nepetalactone drives pest repulsion and predator attraction via divergent PKC/CaMKII signaling

TRPA1-kinase axis polarization: Nepetalactone drives pest repulsion and predator attraction via divergent PKC/CaMKII signaling

  • J Adv Res. 2025 Jul 17:S2090-1232(25)00555-7. doi: 10.1016/j.jare.2025.07.026.
Jianying Li 1 Bo Wang 2 Yilin Wang 2 Fen Li 3 Zhen Li 2 Xiaoxia Liu 2 Songdou Zhang 4
Affiliations

Affiliations

  • 1 Plant Protection Research Institute, Guangdong Academy of Agricultural Sciences, Key Laboratory of Green Prevention and Control on Fruits and Vegetables in South China Ministry of Agriculture and Rural Affairs Guangdong Provincial Key Laboratory of High Technology for Plant Protection, Guangzhou 510640, China; Department of Entomology and MOA Key Lab of Pest Monitoring and Green Management, College of Plant Protection, China Agricultural University, Beijing 100193, China.
  • 2 Department of Entomology and MOA Key Lab of Pest Monitoring and Green Management, College of Plant Protection, China Agricultural University, Beijing 100193, China.
  • 3 Sanya Nanfan Research Institute, Hainan University, Yazhou, Sanya 572024, China.
  • 4 Plant Protection Research Institute, Guangdong Academy of Agricultural Sciences, Key Laboratory of Green Prevention and Control on Fruits and Vegetables in South China Ministry of Agriculture and Rural Affairs Guangdong Provincial Key Laboratory of High Technology for Plant Protection, Guangzhou 510640, China; Department of Entomology and MOA Key Lab of Pest Monitoring and Green Management, College of Plant Protection, China Agricultural University, Beijing 100193, China. Electronic address: zhangsongdou1128@126.com.
Abstract

Introduction: Nepetalactone, an iridoid compound derived from Nepeta cataria, is a potent TRPA1 agonist known to repel hematophagous insects. However, its ecological roles and molecular mechanisms within agricultural ecosystems remain largely unexplored.

Objectives: This study aimed to investigate: (1) the species-specific effects of nepetalactone on pests and predator insects, (2) its action on TRPA1 orthologs, and (3) its potential for push-pull pest control strategies.

Methods: We employed multi-tiered approaches including behavioral assays (two-choice tests, Y-tube olfactometry), molecular techniques (RNAi, qRT-PCR, FISH, Western blot), calcium imaging, and electrophysiology to assess behavioral responses and underlying mechanisms. Field trials further validated pest suppression efficacy.

Results: Nepetalactone exhibits dual functionality: it activates TRPA1 orthologs through conserved cysteine-rich domains, triggering calcium influx and aversion in three sap-sucking pests (Cacopsylla chinensis, Diaphorina citri, Megalurothrips usitatus; Order: Hemiptera). Conversely, it paradoxically attracts two predatory ladybeetles (Harmonia axyridis, Propylea japonica). Mechanistically, this behavioral dichotomy arises form divergent downstream kinase signaling - PKCα mediates repellency in pests, whereas CaMKII drives attraction in predators - despite conserved TRPA1 activation. Field trails validated operational synergy: nepetalactone combined with predatory ladybeetles achieving >90 % pest suppression through integrated push-pull effects. Our integrated approach (calcium imaging, RNAi, electrophysiology) reveals that TRPA1-kinase axis polarization governs species-specific chemoperception.

Conclusion: These findings resolve the ecological paradox wherein a single semiochemical elicits opposing trophic behaviors. nepetalactone is established as a keystone agent for sustainable pest management, providing a molecular blueprint for engineering TRPA1-targeted repellents. Furthermore, it advances push-pull strategies by exploiting predator-pest signaling networks.

Keywords

Chemoperception; Condylognatha pests; Kinase signaling; Nepetalactone; Push-pull strategy; TRPA1.

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