A salivary elicitor in Laedelphax stiatellus positively regulates plant defenses on optimal and suboptimal hosts.

While herbivorous insects often secrete effector proteins to suppress plant immunity, alternative adaptation strategies remain less explored. Here, we report a counterintuitive approach in the small brown planthopper, Laodelphax striatellus. SBPH downregulated a salivary gland-specific elicitor gene, LsG40, when transferred from the optimal host rice to the suboptimal host corn. When expressed in plants, including the model organism tobacco and the two host plants corn and rice, LsG40 acts as a defense elicitor triggering calcium-dependent reactive oxygen species burst, cell death, callose deposition, and jasmonic acid signaling. Interestingly, LsG40 induced the emission of insect-resistant but enemy-attractive volatiles in corn seedlings, including heptadecane to repel SBPH and Spodoptera frugiperda, and (E)-β-farnesene to attract natural enemy Hippodamia variegata, thereby coordinating direct and indirect defenses. Meanwhile, between the two hosts, LsG40-induced rice plants exhibited weaker defense. In further RNA interference, down-regulating LsG40 enhanced SBPH feeding and fecundity by attenuating plant defenses. In contrast to the well-documented role of insect effectors in suppressing plant defense, we demonstrate that SBPH feeding on suboptimal host corn downregulated LsG40, a salivary protein that triggers plant defense. This discovery uncovers a novel adaptive strategy whereby insects fine-tune plant immunity by modulating the expression of a defense elicitor within itself, rather than by suppressing it through secreted effectors. The differential expression of salivary protein gene LsG40 may reflect that SBPH actively manages host defense, including optimal and suboptimal host plants.