Jasmonate ZIM-domain (JAZ) proteins are core components of jasmonic acid signalling and play critical roles in plant growth, development and stress defence. Nevertheless, poplar JAZ functions in herbivore resistance remain poorly understood. This study characterized the JAZ gene family in poplar 741 and explored the anti-insect function of PtoJAZ10. In total, 39 JAZ family members were identified in poplar 741 and designated PtoJAZ1 to PtoJAZ39 by chromosomal position. Phylogenetic analysis classified them into six subclades; most encoded proteins contained conserved C-terminal motifs 1–3. Collinearity and promoter analyses revealed close evolutionary relationships with JAZ homologs in Eucalyptus grandis, together with abundant hormone- and stress-responsive cis-elements in their promoters. PtoJAZ10 expression was strongly induced by methyl jasmonate, abscisic acid and Helicoverpa armigera feeding, showing a 17.5-fold increase after 24 h of herbivory, and was therefore selected for functional study. Subcellular localization confirmed that PtoJAZ10 encodes a nuclear protein. Heterologous overexpression of PtoJAZ10 in tobacco markedly reduced leaf consumption and suppressed larval growth of H. armigera. Upon insect attack, transgenic tobacco accumulated higher jasmonic acid, abscisic acid and lignin, with elevated antioxidant and phenylpropanoid biosynthetic enzyme activities and lower malondialdehyde content compared with wild-type plants. Transcriptome profiling further indicated that PtoJAZ10 may coordinately enhance insect resistance and stress tolerance by regulating core genes of the mitogen-activated protein kinase signalling pathway (e.g., MPK3/6) and the phenylpropanoid biosynthesis pathway (e.g., CCoAOMT1 and CCoAOMT2). This study systematically characterizes the JAZ gene family in poplar 741 and verifies that heterologous overexpression of PtoJAZ10 in tobacco improves insect resistance, laying a foundation for exploring the molecular mechanisms of poplar insect defence. PtoJAZ10 is strongly induced by insect herbivory in poplar 741. Heterologous overexpression of PtoJAZ10 in tobacco enhances resistance to Helicoverpa armigera. Several defense-related genes, including MPK3/6, WRKY33, and CCoAOMT1, showed increased expression in PtoJAZ10-overexpressing tobacco plants.
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