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

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 novel role of the PtrRZFP4-PtrJAZ2 module in plant JA
signaling and resistance to insect herbivory, highlighting its potential
for biotechnological applications in improving insect resistance in forest
trees.