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Research Highlights: The molecular mechanisms underlying woody plant resistance upon oviposition by herbivores remain unclear, as studies have focused on herbaceous plants. The effect of oviposition on gene expression in neighboring plants has also not been reported. Elucidating these molecular responses can help cultivate insect-resistant trees. Background and Objectives: Oviposition by herbivorous insects acts as an early warning signal, inducing plant resistance responses. Here, we employed poplar as a model woody plant to elucidate gene expression and the molecular mechanisms underlying plant resistance after oviposition by Micromelalopha sieversi (Staudinger) (Lepidoptera: Notodontidae). Materials and Methods: The differences in gene expression of two Populus section Aigeiros clones (‘108’ (Populus × euramericana ‘Guariento’) and ‘111’ (Populus × euramericana ‘Bellotto’)) were analyzed via high-throughput sequencing of oviposited, neighboring, and control plants. Results: We obtained 304,526,107 reads, with an average length of 300 bp and a total size of 40.77 Gb. Differentially expressed genes (DEGs) in gene ontology terms of biological process, cellular component, and molecular function were mainly enriched in the “cell part”, “catalytic”, and “metabolic process” functions. Moreover, DEGs were mainly enriched in the following pathways: plant-pathogen interaction, linoleic acid metabolism, and cyanoamino acid metabolism (108-O vs. 108-C); metabolic pathways, photosynthesis, photosynthesis-antenna proteins, nitrogen metabolism, and linoleic acid metabolism (111-O vs. 111-C); metabolic pathways and biosynthesis of secondary metabolites (111-N vs. 111-C); no pathways were significantly enriched in 108-N vs. 108-C. Up-regulated defense genes were associated with pathogenesis-related protein function, innate immune regulation, and biological stress response, with differences in specific genes. All genes related to photosynthetic activity were significantly down-regulated in oviposited and neighboring leaves of the two clones. Conclusions: Oviposited and neighboring ‘108’ and ‘111’ plants exhibited varying degrees of resistance upon oviposition, involving the up-regulation of various defense genes, decreased photosynthesis and nutrient accumulation, and increased secondary metabolic synthesis.

Effect of Micromelalopha sieversi (Staudinger) Oviposition Behavior on the Transcriptome of Two Populus Section Aigeiros Clones