Insects manipulate host nuclear trafficking and epigenetic regulation to facilitate herbivory

Effectors secreted by pathogens or insects manipulate host plant cellular processes depending on their target destination. However, our current knowledge regarding nucleus-localized effectors from herbivorous insects remains limited. Here, we demonstrate that Nilaparvata lugens evolve a nuclear localization signal (NLS)-containing salivary effector NlAMSP that is specialized for targeting host plants. NlAMSP resides in the cytoplasm of insect salivary glands, but, upon secretion, migrates into the nucleus of rice cells. This nuclear translocation is enabled by the cleavage of its signal peptide, allowing the NLS-dependent import via the host importin-α/β pathway. SUMOylation at sites within the NLS is essential for the NlAMSP function, enhancing its nuclear localization and protein stability by preventing autophagy-associated degradation. In plants, NlAMSP interacts with the histone deacetylase OsHDA706 and redirects it from the cytoplasm to the nucleus, thereby disrupting its interaction with the JA biosynthesis regulator OsLOX14 in the cytoplasm. This interference reduces OsLOX14 accumulation and suppresses the JA-associated defense responses. Furthermore, nucleus-localized OsHDA706 diminishes histone H4K5ac and H4K8ac, thereby suppressing the expression of NLR and WRKY genes essential for rice resistance to N. lugens. Our findings uncover a mechanism by which an insect effector manipulates host nuclear trafficking and epigenetic regulation to facilitate herbivory.