Functional characterization of five developmental signaling network genes in the white-backed planthopper: Potential application for pest management

Authors: LIU, XUAN-ZHENG - Guizhou University; LONG, GUI-JUN - Guizhou University; GUO, HUAN - Guizhou University; MA, YUN-FENG - Guizhou University; GONG, LANG-LANG - Guizhou University; ZHANG, MENG-QI - Guizhou University; Hull, Joe; DEWER, YOUSSEF - Agricultural Research Center Of Egypt; LIU, LIE-WEI - Guizhou University; HE, MING - Guizhou University; HE, PENG - Guizhou University

Submitted to: Pest Management Science
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 2/14/2023
Publication Date: 3/21/2023
Citation: Liu, X., Long, G., Guo, H., Ma, Y., Gong, L., Zhang, M., Hull, J.J., Dewer, Y., Liu, L., He, M., He, P. 2023. Functional characterization of five developmental signaling network genes in the white-backed planthopper: Potential application for pest management. Pest Management Science. 79(8):2869-2881. https://doi.org/10.1002/ps.7464.
DOI: https://doi.org/10.1002/ps.7464

Interpretive Summary: For many insects, flight is essential for foraging, risk avoidance, and courtship. Consequently, the targeted disruption of genes involved in wing development has potential to be developed as a novel pest management strategy for winged insects. To examine the utility of this approach, the functional roles of five genes (apterous A, armadillo, dachs, scalloped, and yorkie) were characterized in the white-backed planthopper, a common pest of rice. Injection-based RNA interference (RNAi), a cellular mechanism that regulates target mRNA transcript levels in response to injected nucleic acids, was used to examine how each of the five genes affects wing development in adult planthopper. Compared with control injections, the RNAi injected insects had reduced target transcript levels, increased mortality, and malformed wings frequently characterized by atypical curling. The most pronounced defects were seen after targeted knockdown of armadillo expression. For field applications, however, a more efficient means of delivering the nucleic acids that trigger the RNAi effect is needed. To assess the efficacy of topical RNAi, a sprayable formulation of armadillo dsRNAs complexed with nanoparticle carriers was developed and tested. Phenotypes comparable to those observed in the microinjection experiments (high mortality and deformed wings) support the utility of the topical approach and highlight the potential that targeted disruption of wing development genes may have for pest management.

Technical Abstract: BACKGROUND: The white-backed planthopper (WBPH, Sogatella furcifera) is a major rice pest that exhibits condition dependent wing dimorphisms – a macropterous (long wing) form and a brachypterous (short wing) form. Although, the gene cascade that regulates wing development and dimorphic differentiation has been largely defined, the utility of these genes as targets for pest control has yet to be fully explored. RESULTS: Five genes typically associated with the developmental signaling network, armadillo (arm), apterous A (apA), scalloped (sd), dachs (d), and yorkie (yki) were identified from the WBPH genome and their roles in wing development assessed following RNA interference (RNAi)- mediated knockdown. At 5 days-post injection, transcript levels for all five targets were substantially decreased compared with the dsGFP control group. Among the treatment groups, those injected with dsSfarm had the most pronounced effects on transcript reduction, mortality (95 ± 3%), and incidence (45 ± 3%) of wing deformities, whereas those injected with dsSfyki had the lowest incidence (6.7 ± 4%). To assess the utility of topical RNAi for Sfarm, we used a spray-based approach that complexed a large-scale, bacteria-based double-stranded RNA (dsRNA) expression pipeline with star polycation (SPc) nanoparticles. Rice seedlings infested with third and fourth instar nymphs were sprayed with SPc–dsRNA formulations and RNAi phenotypic effects were assessed over time. At 2 days post-spray, Sfarm transcript levels decreased by 86 ± 9.5% compared with dsGFP groups, and the subsequent incidences of mortality and wing defects were elevated in the treatment group. CONCLUSIONS: This study characterized five genes in the WBPH developmental signaling cascade, assessed their impact on survival and wing development via RNAi, and developed a nanoparticle-dsRNA spray approach for potential field control of WBPH. © 2023 Society of Chemical Industry.