Silverleaf Nightshade (Solanum elaeagnifolium) Undergoes Guild-Specific Transcriptomic Reprogramming Against Chewing Versus Piercing Sucking Herbivory.

Abstract

Solanum elaeagnifolium (silverleaf nightshade, SLN) is a globally invasive perennial weed with reproductive plasticity and complex defence systems that significantly impact crop yields by invading fields of staple, commercial and ornamental crops. Despite being a host to multiple insect herbivores, the molecular programming enabling its rapid adaptation to defend against diverse feeding guilds remains poorly resolved. Here, we report a comprehensive de novo transcriptomic assembly and comparative analysis of S. elaeagnifolium challenged by two distinct herbivores: the piercing-sucking generalist cowpea aphid, Aphis craccivora and the chewing specialist tobacco hornworm, Manduca sexta. Differential gene expression analysis revealed a massive difference in the scale of the plant's response; aphid infestation resulted in 14,799 differentially expressed genes (DEGs), whereas hornworm feeding triggered a more localized response of 4235 DEGs. Guild-specific co-expression networks and transcription-factor enrichment (907 DEGs in aphid-challenged versus 196 in hornworm-challenged) point to two distinct regulatory responses. This reprogramming strategy was characterized by enriched KEGG pathways for sphingolipid metabolism and MAPK signalling in aphids. Conversely, hornworm infestation resulted in significant enrichment of cell wall organization, pectin catabolism and callose synthesis. Functional enrichment of network hub genes further revealed aphid-specific chromatin remodelling and DNA repair activity, while hornworm hub genes were associated with ribosome biogenesis and auxin-responsive GH3-family enzymes implicated in jasmonate conjugation. These contrasting findings indicate that SLN does not deploy a generic wound response but instead reallocates transcriptional resources according to feeding mode. This guild-specific defensive plasticity likely underlies part of the exceptional invasive success of SLN across diverse environments.