Abstract
The Asian long-horned beetle (ALB), Anoplophora glabripennis, is a serious invasive forest pest in several countries, including the USA. Currently, there are no effective methods available to manage this pest without adverse impacts on the environment, but RNA interference (RNAi) technology may provide a more environmentally friendly pest control option. To identify target genes for control of ALB, we screened 48 candidate genes in larvae and selected several effective target genes. Injection of double-stranded RNA (dsRNA) targeting the gene coding for the inhibitor of apoptosis (dsIAP) or vacuolar sorting protein, SNF7 (dsSNF7), into larvae and adults resulted in a significant knockdown of these genes and caused 100% mortality in both larvae and adults. As microinjection of dsRNA is not a feasible option for field applications, delivery through oral route was then attempted. Oral delivery of naked dsRNA did not cause mortality in larvae and adults. However, feeding heat-killed bacteria containing dsIAP or dsSNF7 induced mortality and knockdown of target genes in larvae and adults. In conclusion, the utilization of heat-killed bacteria for delivery of dsRNA targeting IAP or SNF7 gene may serve as a potential pest control method for ALB.
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References
Attasart P, Naramoon O, Kongphom U, Chimwai C, Panyim S (2013) Ingestion of bacteria expressing dsRNA triggers specific RNA silencing in shrimp. Virus Res 171:252–256. https://doi.org/10.1016/j.virusres.2012
Baum JA, Bogaert T, Clinton W, Heck GR, Feldmann P, Ilagan O, Johnson S, Plaetinck G, Munyikwa T, Pleau M, Vaughn T (2007) Control of coleopteran insect pests through RNA interference. Nat Biotechnol 25(11):1322. https://doi.org/10.1038/nbt1359
Bellés X (2010) Beyond Drosophila: RNAi in vivo and functional genomics in insects. Annu Rev Entomol 55:111–128. https://doi.org/10.1146/annurev-ento-112408-085301
Cao M, Gatehouse JA, Fitches EC (2018) A systematic study of RNAi Effects and dsRNA stability in Tribolium castaneum and Acyrthosiphon pisum, following injection and ingestion of analogous dsRNAs. Int J Mol Sci 19(4):1079. https://doi.org/10.3390/ijms19041079
Chiu YL, Rana TM (2002) RNAi in human cells: basic structural and functional features of small interfering RNA. Mol Cell 10(3):549–561. https://doi.org/10.1016/S1097-2765(02)00652-4
Christiaens O, Swevers L, Smagghe G (2014) dsRNA degradation in the pea aphid (Acyrthosiphon pisum) associated with lack of response in RNAi feeding and injection assay. Peptides 53:307–314
Das S, Debnath N, Cui Y, Unrine J, Palli SR (2015) Chitosan, carbon quantum dot, and 533 silica nanoparticle mediated dsRNA delivery for gene silencing in Aedes aegypti: a comparative analysis. ACS Appl Mater Int 7:19530–19535
Dhandapani RK, Gurusamy D, Howell JL, Palli SR (2019) Development of CS-TPP-dsRNA nanoparticles for induction of RNAi in the yellow fever mosquito. Aedes Aegypt Sci Rep 9:8775
Fire A, Xu S, Montgomery MK, Kostas SA, Driver SE, Mello CC (1998) Potent and specific genetic interference by double-stranded RNA in Caenorhabditis elegans. Nature 391(6669):806. https://doi.org/10.1038/35888
Haack RA, Hérard F, Sun J, Turgeon JJ (2010) Managing invasive populations of Asian longhorned beetle and citrus longhorned beetle: a worldwide perspective. Annu Rev Entomol 55:521–546. https://doi.org/10.1146/annurev-ento-112408-085427
Hu P, Wang J, Cui M, Tao J, Luo Y (2016a) Antennal transcriptome analysis of the Asian longhorned beetle Anoplophora glabripennis. Sci Rep 6:26652. https://doi.org/10.1038/srep26652
Hu X et al (2016b) Discovery of midgut genes for the RNA interference control of corn rootworm. Sci Rep 6:30542
Huvenne H, Smagghe G (2010) Mechanisms of dsRNA uptake in insects and potential of RNAi for pest control: a review. J Insect Physiol 56(3):227–235
Keena MA (2005) Pourable artificial diet for rearing Anoplophora glabripennis (Coleoptera: Cerambycidae) and methods to optimize larval survival and synchronize development. Ann Entomol Soc Am 98:536–547
Knorr E, Fishilevich E, Tenbusch L, Frey ML, Rangasamy M, Billion A, Worden SE, Gandra P, Arora K, Lo W, Schulenberg G (2018) Gene silencing in Tribolium castaneum as a tool for the targeted identification of candidate RNAi targets in crop pests. Sci Rep 8(1):2061. https://doi.org/10.1038/s41598-018-20416-y
Kusaba M (2004) RNA interference in crop plants. Curr Opin Biotechnol 15(2):139–143. https://doi.org/10.1016/j.copbio.2004.02.004
Lynch JA, Desplan CA (2006) Method for parental RNA interference in the wasp Nasonia vitripennis. Nat Protoc 1(1):486. https://doi.org/10.1038/nprot.2006.70
Martín D, Maestro O, Cruz J, Mane-Padros D, Belles X (2006) RNAi studies reveal a conserved role for RXR in molting in the cockroach Blattella germanica. J Insect Physiol 52(4):410–416. https://doi.org/10.1016/j.jinsphys.2005.12.002
McKenna DD, Scully ED, Pauchet Y, Hoover K, Kirsch R, Geib SM, Mitchell RF, Waterhouse RM, Ahn SJ, Arsala D, Benoit JB (2016) Genome of the Asian longhorned beetle (Anoplophora glabripennis), a globally significant invasive species, reveals key functional and evolutionary innovations at the beetle–plant interface. Genome Biol 17(1):227. https://doi.org/10.1186/s13059-016-1088-8
Mysore K et al (2017) Yeast interfering RNA larvicides targeting neural genes induce high rates of Anopheles larval mortality. Malar J 16(1):461
Poland TM, Haack RA, Petrice TR, Miller DL, Bauer LS, Gao R (2006) Field evaluations of systemic insecticides for control of Anoplophora glabripennis (Coleoptera: Cerambycidae) in China. J Econ Entomol 99(2):383–392
Rodrigues TB, Dhandapani RK, Duan JJ, Palli SR (2017) RNA interference in the Asian longhorned beetle: identification of key RNAi genes and reference genes for RT-qPCR. Sci Rep 7(1):8913. https://doi.org/10.1038/s41598-017-08813-1
Scully ED, Hoover K, Carlson JE, Tien M, Geib SM (2013) Midgut transcriptome profiling of Anoplophora glabripennis, a lignocellulose degrading cerambycid beetle. BMC Genom 14(1):850. https://doi.org/10.1186/1471-2164-14-850
Shukla JN, Kalsi M, Sethi A, Narva KE, Fishilevich E, Singh S, Mogilicherla K, Palli SR (2016) Reduced stability and intracellular transport of dsRNA contribute to poor RNAi response in lepidopteran insects. RNA Biol 13(7):656–669. https://doi.org/10.1080/15476286.2016.1191728
Singh IK, Singh S, Mogilicherla K, Shukla JN, Palli SR (2017) Comparative analysis of double-stranded RNA degradation and processing in insects. Sci Rep 7(1):17059. https://doi.org/10.1038/s41598-017-17134-2
Taning CN, Andrade EC, Hunter WB, Christiaens O, Smagghe G (2016a) Asian citrus psyllid RNAi pathway—RNAi evidence. Sci Rep 6:38082
Taning CNT, Christiaens O, Berkvens N, Casteels H, Maes M, Smagghe G (2016b) Oral RNAi to control Drosophila suzukii: laboratory testing against larval and adult stages. J Pest Sci 89(3):803–814. https://doi.org/10.1007/s10340-016-0736-9
Tian H, Peng H, Yao Q, Chen H, Xie Q, Tang B, Zhang W (2009) Developmental control of a lepidopteran pest Spodoptera exigua by ingestion of bacteria expressing dsRNA of a non-midgut gene. PLoS ONE 4(7):e6225
Ulrich J, Majumdar U, Schmitt-Engel C, Schwirz J, Schultheis D, Ströhlein N, Troelenberg N, Grossmann D, Richter T, Dönitz J, Gerischer L (2015) Large scale RNAi screen in Tribolium reveals novel target genes for pest control and the proteasome as prime target. BMC Genom 16(1):674. https://doi.org/10.1186/s12864-015-1880-y
Yoon JS, Mogilicherla K, Gurusamy D, Chen X, Chereddy SCRR, Palli SR (2018) Double-stranded RNA binding protein, Staufen, is required for the initiation of RNAi in coleopteran insects. Proc Natl Acad Sci USA 115(33):8334–8339. https://doi.org/10.1073/pnas.1809381115
Zhou X, Wheeler MM, Oi FM, Scharf ME (2008) RNA interference in the termite Reticulitermes flavipes through ingestion of double-stranded RNA. Insect Biochem Mol Biol 38(8):805–815. https://doi.org/10.1016/j.ibmb.2008.05.005
Zhu F, Xu J, Palli R, Ferguson J, Palli SR (2011) Ingested RNA interference for managing the populations of the Colorado potato beetle, Leptinotarsa decemlineata. Pest Manag Sci 67(2):175–182. https://doi.org/10.1002/ps.2048
Acknowledgements
We thank Jonathan Schmude and Cherie Keenan (USDA ARS BIIRU) and Jeff Howell of University of Kentucky for assistance with the mortality bioassays with larvae and adults of Asian longhorned beetles, and Linda Saundra, Daria Tatman and Ellen Apacio for help with Asian longhorned beetle rearing at BIIRU.
Funding
This work was funded by USDA Farm Bill Section 10007 (FY2018-AP18PPQS&T00C179) and by the National Institute of Food and Agriculture, USDA, HATCH under 2351177000.
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Dhandapani, R.K., Gurusamy, D., Duan, J.J. et al. RNAi for management of Asian long-horned beetle, Anoplophora glabripennis: identification of target genes. J Pest Sci 93, 823–832 (2020). https://doi.org/10.1007/s10340-020-01197-8
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DOI: https://doi.org/10.1007/s10340-020-01197-8