The PtrRZFP4-PtrJAZ2 module regulates the jasmonic acid signaling pathway involved in the interaction between poplar and herbivorous insects

Abstract

The plant hormone jasmonic acid (JA) is pivotal in regulating plant growth and defense mechanisms. Despite extensive research on the JA signaling network, the integration of other factors with JAZ (jasmonate ZIM domain) proteins to modulate JA signaling in response to diverse herbivore attacks remains unclear. In this study, we employed molecular biology and multi-omics techniques to identify an E3 ubiquitin ligase, PtrRZFP4. This E3 ubiquitin ligase exerts a positive regulatory effect on the JA signaling pathway, yet demonstrates differential responses to distinct insect types. We found that upon insect attack, the expression of PtrRZFP4 transcripts is upregulated. In addition, PtrRZFP4 is able to interact with PtrJAZ2 and promote the ubiquitination and degradation of PtrJAZ2 protein. Furthermore, PtrRZFP4 activates the jasmonic acid (JA) signaling pathway at both the transcriptional and metabolic levels, triggering the synthesis of a large number of secondary metabolites related to insect resistance, such as terpenoids and alkaloids. This ultimately enhances the plant's defense against insect herbivory. The larvae of the specialist insect showed a strong preference for feeding on the leaves of transgenic poplar overexpressing PtrRZFP4 (OX-PtrRZFP4), which contain elevated levels of secondary metabolites. In contrast, the larvae of the generalist insect avoid leaves with increased secondary metabolite levels. However, PtrJAZ2 exhibits an opposite function to PtrRZFP4 in the resistance of poplar trees to different herbivores. Therefore, our study uncovers the significant role of the PtrRZFP4-PtrJAZ2 module in plant JA signaling and resistance to insect herbivory, highlighting its potential for biotechnological applications in improving herbivore resistance in forest trees.