The N‐terminal subunit of vitellogenin in planthopper eggs and saliva acts as a reliable elicitor that induces defenses in rice

Abstract

Summary Vitellogenins (Vgs) are critical for the development and fecundity of insects. As such, these essential proteins can be used by plants to reliably sense the presence of insects. We addressed this with a combination of molecular and chemical analyses, genetic transformation, bioactivity tests, and insect performance assays. The small N‐terminal subunit of Vgs of the planthopper Nilaparvata lugens (NlVgN) was found to trigger strong defense responses in rice when it enters the plants during feeding or oviposition by the insect. The defenses induced by NlVgN not only decreased the hatching rate of N. lugens eggs, but also induced volatile emissions in plants, which rendered them attractive to a common egg parasitoid. VgN of other planthoppers triggered the same defenses in rice. We further show that VgN deposited during planthopper feeding compared with during oviposition induces a somewhat different response, probably to target the appropriate developmental stage of the insect. We also confirm that NlVgN is essential for planthopper growth, development, and fecundity. This study demonstrates that VgN in planthopper eggs and saliva acts as a reliable and unavoidable elicitor of plant defenses. Its importance for insect performance precludes evolutionary adaptions to prevent detection by rice plants.

Interaction between the flagellum of Candidatus Liberibacter asiaticus and the vitellogenin-like protein of Diaphorina citri significantly influences CLas titer

“…With the advancement of high-throughput sequencing and proteomic technologies, Vg has recently been discovered in insect salivary glands ( Ji et al, 2013 ; Huang et al, 2018 ). Vg is also used as a saliva protein ( Huang et al, 2021 ; Ji et al, 2021 ; Zeng et al, 2023 ). Transcriptome and hemolymph protein studies have revealed that Vg is upregulated in C Las-infected D. citri ( Kruse et al, 2018 ; Jaiswal et al, 2021 ).…”

Leafhopper salivary vitellogenin mediates horizontal virus transmission to plant phloem

“…Vg has been acknowledged as crucial in providing nutrients for oocytes, regulating immune defense, and facilitating the vertical transmission of viruses across insect generations 21,22,23,24,44 . While numerous studies have focused on the function of NcVg within insect bodies, research on the salivary Vg of piercing-sucking insects has been limited, including the pathway of Vg release from the salivary glands and its function postrelease, until recent reports on the suppressive effect of planthopper NcVg on H2O2 and the triggering of JA and JA-Ile production in rice 28,29 . The C-terminal of Vg in small planthopper acts as an effector to attenuate H2O2 accumulation of rice via interacting with the OsWRKY71, which is involved in induction of H2O2 accumulation 28 .…”

“…The C-terminal of Vg in small planthopper acts as an effector to attenuate H2O2 accumulation of rice via interacting with the OsWRKY71, which is involved in induction of H2O2 accumulation 28 . While the N-terminal of Vg in brown planthopper acts as a reliable elicitor that induces defenses in rice 29 .…”

“…Vg is also released to the plant host through insect saliva when piercing-sucking insects feed on plants 27 . The Vg protein of the small brown planthopper, SpVg, serves as an effector that weakens plant defense by interacting with rice immunity regulator OsWRKY71, while Vg in saliva or eggs of the small brown planthopper can act as an elicitor of plant defenses by inducing the production of H2O2, JA, and JA-Ile 28,29 . However, it is unknown whether salivary Vg of other piercing-sucking insects functions during plant defense or viral transmission.…”

Field evidence for the role of plant volatiles induced by caterpillar-derived elicitors in the prey location behavior of predatory social wasps

“…Various elicitors (e.g., caeliferins, Alborn et al, 2007; β-glucosidase, Mattiacci et al, 1995; vitellogenin, Zeng et al, 2023), have been identified within the oral secretions of herbivores, including Spodoptera caterpillars (volicitin, Alborn et al, 1997; inceptin, Schmelz et al, 2006). Simulated herbivory experiments have consistently revealed rapid emission of terpenoids and other important volatiles involved plant-insect signaling following the application of Spodoptera caterpillar oral secretions to mechanically inflicted wounds compared to plants that were only subjected to mechanical wounding (Turlings et al, 1993, 2000).…”