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Nanoparticle-delivered RNAi-based pesticide target screening for the rice pest white-backed planthopper and risk assessment for a natural predator

Vacuolar-type (H+)-ATPase (vATPase) is a conserved multi-subunit eukaryotic enzyme composed of 14 subunits that form a functional complex consisting of an ATP-hydrolytic domain (V1) and a proton-translocation domain (V0). ATP hydrolysis and subsequent H+ translocation rely heavily on a fully assembl...

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Published in:The Science of the total environment 2024-05, Vol.926, p.171286-171286, Article 171286
Main Authors: Ma, Yun-Feng, Zhao, Ya-Qin, Zhou, Yang-yuntao, Feng, Hong-Yan, Gong, Lang-Lang, Zhang, Meng-Qi, Hull, J. Joe, Dewer, Youssef, Roy, Amit, Smagghe, Guy, He, Ming, He, Peng
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creator Ma, Yun-Feng
Zhao, Ya-Qin
Zhou, Yang-yuntao
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Dewer, Youssef
Roy, Amit
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description Vacuolar-type (H+)-ATPase (vATPase) is a conserved multi-subunit eukaryotic enzyme composed of 14 subunits that form a functional complex consisting of an ATP-hydrolytic domain (V1) and a proton-translocation domain (V0). ATP hydrolysis and subsequent H+ translocation rely heavily on a fully assembled V1/V0 complex. Since vATPase is crucial for insect survival, it is a viable molecular target for pest control. However, detailed functional analyses of the 14 subunits and their suitability for pest control have not been fully explored in a single insect species. In this study, we identified 22 vATPase subunit transcripts that correspond to 13 subunits (A1, A2, B, C, D, E, F, G, H, a1, a2, c and d) in the white-backed planthopper (WBPH), Sogatella furcifera, a major hemipteran pest of rice. RNAi screens using microinjection and spray-based methods revealed that the SfVHA-F, SfVHA-a2 and SfVHA-c2 subunits are critical. Furthermore, star polymer (SPc) nanoparticles were utilized to conduct spray-induced and nanoparticle-delivered gene silencing (SI-NDGS) to evaluate the pest control efficacy of RNAi targeting the SfVHA-F, SfVHA-a2 and SfVHA-c2 transcripts. Target mRNA levels and vATPase enzymatic activity were both reduced. Honeydew excreta was likewise reduced in WBPH treated with dsRNAs targeting SfVHA-F, SfVHA-a2 and SfVHA-c2. To assess the environmental safety of the nanoparticle-wrapped dsRNAs, Cyrtorhinus lividipennis Reuter, a major natural enemy of planthoppers, was also sprayed with dsRNAs targeting SfVHA-F, SfVHA-a2 and SfVHA-c2. Post-spray effects of dsSfVHA-a2 and dsSfVHA-c2 on C. lividipennis were innocuous. This study identifies SfVHA-a2 and SfVHA-c2 as promising targets for biorational control of WBPH and lays the foundation for developing environment-friendly RNAi biopesticides. [Display omitted] •Twenty-two vATPase subunit transcripts were identified in Sogatella furcifera.•vATPase subunit transcripts were screened by RNAi as potential control targets.•Nanoparticle-delivery was used to increase the pest control efficacy.•Assessment of potential non-target organism effects in Cyrtorhinus lividipennis
doi_str_mv 10.1016/j.scitotenv.2024.171286
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In this study, we identified 22 vATPase subunit transcripts that correspond to 13 subunits (A1, A2, B, C, D, E, F, G, H, a1, a2, c and d) in the white-backed planthopper (WBPH), Sogatella furcifera, a major hemipteran pest of rice. RNAi screens using microinjection and spray-based methods revealed that the SfVHA-F, SfVHA-a2 and SfVHA-c2 subunits are critical. Furthermore, star polymer (SPc) nanoparticles were utilized to conduct spray-induced and nanoparticle-delivered gene silencing (SI-NDGS) to evaluate the pest control efficacy of RNAi targeting the SfVHA-F, SfVHA-a2 and SfVHA-c2 transcripts. Target mRNA levels and vATPase enzymatic activity were both reduced. Honeydew excreta was likewise reduced in WBPH treated with dsRNAs targeting SfVHA-F, SfVHA-a2 and SfVHA-c2. To assess the environmental safety of the nanoparticle-wrapped dsRNAs, Cyrtorhinus lividipennis Reuter, a major natural enemy of planthoppers, was also sprayed with dsRNAs targeting SfVHA-F, SfVHA-a2 and SfVHA-c2. 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[Display omitted] •Twenty-two vATPase subunit transcripts were identified in Sogatella furcifera.•vATPase subunit transcripts were screened by RNAi as potential control targets.•Nanoparticle-delivery was used to increase the pest control efficacy.•Assessment of potential non-target organism effects in Cyrtorhinus lividipennis</description><identifier>ISSN: 0048-9697</identifier><identifier>EISSN: 1879-1026</identifier><identifier>DOI: 10.1016/j.scitotenv.2024.171286</identifier><identifier>PMID: 38428617</identifier><language>eng</language><publisher>Netherlands: Elsevier B.V</publisher><subject>Adenosine Triphosphate ; Animals ; Hemiptera ; Heteroptera ; Natural enemy ; Oryza - genetics ; Pesticides ; Risk Assessment ; RNA Interference ; Spray-induced and nanoparticle-delivered gene silencing ; Star polymer ; vATPase ; White-backed planthopper</subject><ispartof>The Science of the total environment, 2024-05, Vol.926, p.171286-171286, Article 171286</ispartof><rights>2024</rights><rights>Copyright © 2024. 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ATP hydrolysis and subsequent H+ translocation rely heavily on a fully assembled V1/V0 complex. Since vATPase is crucial for insect survival, it is a viable molecular target for pest control. However, detailed functional analyses of the 14 subunits and their suitability for pest control have not been fully explored in a single insect species. In this study, we identified 22 vATPase subunit transcripts that correspond to 13 subunits (A1, A2, B, C, D, E, F, G, H, a1, a2, c and d) in the white-backed planthopper (WBPH), Sogatella furcifera, a major hemipteran pest of rice. RNAi screens using microinjection and spray-based methods revealed that the SfVHA-F, SfVHA-a2 and SfVHA-c2 subunits are critical. Furthermore, star polymer (SPc) nanoparticles were utilized to conduct spray-induced and nanoparticle-delivered gene silencing (SI-NDGS) to evaluate the pest control efficacy of RNAi targeting the SfVHA-F, SfVHA-a2 and SfVHA-c2 transcripts. Target mRNA levels and vATPase enzymatic activity were both reduced. Honeydew excreta was likewise reduced in WBPH treated with dsRNAs targeting SfVHA-F, SfVHA-a2 and SfVHA-c2. To assess the environmental safety of the nanoparticle-wrapped dsRNAs, Cyrtorhinus lividipennis Reuter, a major natural enemy of planthoppers, was also sprayed with dsRNAs targeting SfVHA-F, SfVHA-a2 and SfVHA-c2. Post-spray effects of dsSfVHA-a2 and dsSfVHA-c2 on C. lividipennis were innocuous. This study identifies SfVHA-a2 and SfVHA-c2 as promising targets for biorational control of WBPH and lays the foundation for developing environment-friendly RNAi biopesticides. [Display omitted] •Twenty-two vATPase subunit transcripts were identified in Sogatella furcifera.•vATPase subunit transcripts were screened by RNAi as potential control targets.•Nanoparticle-delivery was used to increase the pest control efficacy.•Assessment of potential non-target organism effects in Cyrtorhinus lividipennis</abstract><cop>Netherlands</cop><pub>Elsevier B.V</pub><pmid>38428617</pmid><doi>10.1016/j.scitotenv.2024.171286</doi><tpages>1</tpages></addata></record>
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identifier ISSN: 0048-9697
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source ScienceDirect Freedom Collection
subjects Adenosine Triphosphate
Animals
Hemiptera
Heteroptera
Natural enemy
Oryza - genetics
Pesticides
Risk Assessment
RNA Interference
Spray-induced and nanoparticle-delivered gene silencing
Star polymer
vATPase
White-backed planthopper
title Nanoparticle-delivered RNAi-based pesticide target screening for the rice pest white-backed planthopper and risk assessment for a natural predator
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