Crucial role of a takeout protein in white-backed planthopper Sogatella furcifera (Horváth) orientation towards its host rice plants

Authors: HE, MING - Guizhou University; LONG, GUI-JUN - Guizhou University; FENG, HONG-YAN - Guizhou University; ZHAO, YA-QIN - Guizhou University; ZHOU, YANG-YUNTAO - Guizhou University; ZHANG, MENG-QI - Guizhou University; MA, YUN-FENG - Guizhou University; GONG, LANG-LANG - Guizhou University; Hull, Jimmy; ZOTTI, MOISES - Federal University Of Pelotas; DEWER, YOUSSEF - Agricultural Research Center Of Egypt; HE, PENG - Guizhou University; SMAGGHE, GUY - Guizhou University

Submitted to: Pest Management Science
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 9/26/2024
Publication Date: 11/1/2025
Citation: He, M., Long, G., Feng, H., Zhao, Y., Zhou, Y., Zhang, M., Ma, Y., Gong, L., Hull, J.J., Zotti, M.J., Dewer, Y., He, P., Smagghe, G. 2025. Crucial role of a takeout protein in white-backed planthopper Sogatella furcifera (Horváth) orientation towards its host rice plants. Pest Management Science. 81(11):7390-7402. https://doi.org/10.1002/ps.8474.
DOI: https://doi.org/10.1002/ps.8474

Interpretive Summary: The insect olfactory system arises from the interplay of multiple highly evolved protein families that function to convert volatile odorant molecules into behavioral responses that impact diverse behavioral and physiological activities such as host location, oviposition site selection, and defense. Although most of the main proteins involved in olfaction have been characterized, the antennal-specific expression of some members of the takeout (TO) protein family suggests they too may function in olfaction. To gain insights into the olfactory systems of insect pests that infest rice crops, the full complement of TO genes was identified from genomic and transcriptomic resources for three species of planthoppers. Among these genes, the TO17 gene was found to be predominantly expressed in antennae. In further support of an olfactory role, RNAi-mediated knockdown of TO17 transcripts impaired host plant recognition and recombinantly expressed TO17 protein was capable of binding common rice plant odorants. These findings provide insights into planthopper olfaction and suggest that targeted disruption of these genes may be a useful pest management strategy.

Technical Abstract: Although the takeout (TO) gene family impacts diverse physiological and behavioral functions in insects, specific olfactory-associated roles for the family have yet to be fully elucidated. To provide insights into TO function in rice planthoppers, the genomes of three rice planthoppers (white-backed planthopper, brown planthopper and small brown planthopper) were searched for TO homologs and their degree of conservation assessed via chromosomal localization, exon-intron boundaries, phylogenetic relationships, and protein domains/motifs. We performed a tissue-specific expression analysis of the 20 TO genes in the white-backed planthopper (WBPH, Sogatella furcifera) and found that SfTO17 is enriched in adult antennae. RNAi-mediated knockdown of SfTO17 impaired WBPH olfaction and reduced host seeking responses following exposure to rice plants. The binding profile of ß-ionone, hexyl benzoate and benzyl benzoate with recombinant SfTO17 was evaluated via competitive fluorescence binding assays. Conformational prediction of SfTO17 coupled with molecular docking analyses revealed several amino acid residues potentially critical for odorant binding. This study demonstrates the olfactory function of SfTO17 in WBPH and highlights its potential as a target for controlling this rice pest.