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RNA interference-mediated control of Asian citrus psyllid, the vector of the huanglongbing bacterial pathogen

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Abstract

Asian citrus psyllid, Diaphorina citri Kuwayama (Hemiptera: Liviidae), is the natural vector of the Huanglongbing (HLB) pathogen that presents an unparalleled challenge to citrus production. RNA interference (RNAi) has already shown great potential for insect pest management owing to its high specificity. RNAi technique relies on the delivery of exogenous double-stranded RNAs (dsRNAs) that target essential genes in insects. The D. citri genome possesses three dsRNase homologs and all core RNAi machinery genes, aside from the R2D2 that functions as a cofactor of Dicer-2 in the siRNA pathway. Nevertheless, ever-increasing research on the application of RNAi to suppress D. citri population has promulgated outstanding progress. Here, we provide a comprehensive review of the recent literature, and summarize the current understanding of RNAi mechanisms and advances in the applications of RNAi in D. citri. The major challenges including the potential of dsRNA degradation, target gene selection, and dsRNA delivery methods, as well as the implications of using RNAi for D. citri control are reviewed.

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References

  • Allen ML, Walker WB 3rd (2012) Saliva of Lygus lineolaris digests double stranded ribonucleic acids. Journal of Insect Physiology 58:391–396

    CAS  PubMed  Google Scholar 

  • Andrade EC, Hunter WB (2017) RNAi feeding bioassay: development of a non-transgenic approach to control Asian citrus psyllid and other hemipterans. Entomologia Experimentalis et Applicata 162:389–396

    CAS  Google Scholar 

  • Bachman PM, Bolognesi R, Moar WJ, Mueller GM, Paradise MS, Ramaseshadri P, Tan J, Uffman JP, Warren J, Wiggins BE, Levine SL (2013) Characterization of the spectrum of insecticidal activity of a double-stranded RNA with targeted activity against Western Corn Rootworm (Diabrotica virgifera virgifera LeConte). Transgenic Research 22:1207–1222

    CAS  PubMed  PubMed Central  Google Scholar 

  • Boina DR, Bloomquist JR (2015) Chemical control of the Asian citrus psyllid and of huanglongbing disease in citrus. Pest Management Science 71:808–823

    CAS  PubMed  Google Scholar 

  • Cappelle K, de Oliveira C, Van Eynde B, Christiaens O, Smagghe G (2016) The involvement of clathrin-mediated endocytosis and two Sid-1-like transmembrane proteins in double-stranded RNA uptake in the Colorado potato beetle midgut. Insect Molecular Biology 25:315–323

    CAS  PubMed  Google Scholar 

  • Christiaens O, Smagghe G (2014) The challenge of RNAi-mediated control of hemipterans. Current Opinion in Insect Science 6:15–21

    Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • da Graça JV, Douhan GW, Halbert SE, Keremane ML, Lee RF, Vidalakis G, Zhao H (2015) Huanglongbing: An overview of a complex pathosystem ravaging the world’s citrus. Journal of Integrative Plant Biology 58:373–387

    PubMed  Google Scholar 

  • De Smet L, Ravoet J, Wenseleers T, Graaf DC (2017) Expression of key components of the RNAi machinery are suppressed in Apis mellifera that suffer a high virus infection. Entomological Science 20:76–85

    Google Scholar 

  • El-Shesheny I, Hajeri S, El-Hawary I, Gowda S, Killiny N (2013) Silencing abnormal wing disc gene of the Asian citrus psyllid, Diaphorina citri disrupts adult wing development and increases nymph mortality. PLoS One 8:e65392

    CAS  PubMed  PubMed Central  Google Scholar 

  • Fishilevich E, Vélez AM, Storer NP, Li H, Bowling AJ, Rangasamy M, Worden SE, Narva KE, Siegfried BD (2016) RNAi as a management tool for the western corn rootworm, Diabrotica virgifera virgifera. Pest Management Science 72:1652–1663

    CAS  PubMed  Google Scholar 

  • Galdeano DM, Breton MC, Lopes JRS, Falk BW, Machado MA (2017) Oral delivery of double-stranded RNAs induces mortality in nymphs and adults of the Asian citrus psyllid, Diaphorina citri. PloS One 12:e0171847

    PubMed  PubMed Central  Google Scholar 

  • Grafton-Cardwell EE, Stelinski LL, Stansly PA (2013) Biology and management of Asian citrus psyllid, vector of the huanglongbing pathogens. Annual Review Entomology 58:413–432

    CAS  Google Scholar 

  • Guan RB, Li HC, Miao XX (2017) Prediction of effective RNA interference targets and pathway-related genes in lepidopteran insects by RNA sequencing analysis. Insect Science 25:356–367

    PubMed  Google Scholar 

  • Haasnoot J, de Vries W, Geutjes EJ, Prins M, de Haan P, Berkhout B (2007) The Ebola virus VP35 protein is a suppressor of RNA silencing. PLoS Pathogens 3:e86

    PubMed  PubMed Central  Google Scholar 

  • Hajeri S, Killiny N, El-Mohtar C, Dawson WO, Gowda S (2014) Citrus tristeza virus-based RNAi in citrus plants induces gene silencing in Diaphorina citri, a phloem-sap sucking insect vector of citrus greening disease (Huanglongbing). Journal of Biotechnology 176:42–49

    CAS  PubMed  Google Scholar 

  • Hall DG, Richardson ML, Ammar ED, Halbert SE (2013) Asian citrus psyllid, Diaphorina citri, vector of citrus huanglongbing disease. Entomologia Experimentalis et Applicata 146:207–223

    Google Scholar 

  • Hodges A, Spreen T (2012) Economic impacts of citrus greening (HLB) in Florida, 2006/07–2010/11, Electronic Data Information Source (EDIS) FE903. University of Florida Gainesville, Gainesville, p 32611

    Google Scholar 

  • Hughes CL, Kaufman TC (2000) RNAi analysis of Deformed, proboscipedia and Sex combs reduced in the milkweed bug Oncopeltus fasciatus: novel roles for Hox genes in the hemipteran head. Development 127:3683–3694

    CAS  PubMed  Google Scholar 

  • Huvenne H, Smagghe G (2010) Mechanisms of dsRNA uptake in insects and potential of RNAi for pest control: a review. Journal of Insect Physiology 56:227–235

    CAS  Google Scholar 

  • Killiny N, Kishk A (2017) Delivery of dsRNA through topical feeding for RNA interference in the citrus sap piercing-sucking hemipteran, Diaphorina citri. Archives of Insect Biochemistry and Physiology 95:e21394

    Google Scholar 

  • Killiny N, Hajeri S, Tiwari S, Gowda S, Stelinski LL (2014) Double-Stranded RNA Uptake through Topical Application, Mediates Silencing of Five CYP4 Genes and Suppresses Insecticide Resistance in Diaphorina citri. Plos One 9:e110536

    PubMed  PubMed Central  Google Scholar 

  • Kishk A, Anber HAI, AbdEl-Raof TK, El-Sherbeni A-HD, Hamed S, Gowda S, Killiny N (2017a) RNA interference of carboxyesterases causes nymph mortality in the Asian citrus psyllid, Diaphorina citri. Archives of Insect Biochemistry and Physiology 94:e21377

    Google Scholar 

  • Kishk A, Hijaz F, Anber HA, AbdEl-Raof TK, El-Sherbeni A-HD, Hamed S, Killiny N (2017b) RNA interference of acetylcholinesterase in the Asian citrus psyllid, Diaphorina citri, increases its susceptibility to carbamate and organophosphate insecticides. Pesticide Biochemistry Physiology 143:81–89

    CAS  PubMed  Google Scholar 

  • Lee JM, Kojin Y, Tatsuke T, Mon H, Miyagawa Y, Kusakabe T (2013) Coexpression of Escherichia coli RNase III in silkworm cells improves the efficiency of RNA interference induced by long hairpin dsRNAs. Insect Science 20:69–77

    CAS  PubMed  Google Scholar 

  • Li H, Khajuria C, Rangasamy M, Gandra P, Fitter M, Geng C, Woosely A, Hasler J, Schulenberg G, Worden S (2015) Long dsRNA but not siRNA initiates RNAi in western corn rootworm larvae and adults. Journal of Applied Entomology 139:432–445

    CAS  Google Scholar 

  • Li T, Chen J, Fan X, Chen W, Zhang W (2017) MicroRNA and dsRNA targeting chitin synthase A reveal a great potential for pest management of the hemipteran insect Nilaparvata lugens. Pest Management Science 73:1529–1537

    CAS  PubMed  Google Scholar 

  • Li C, Tian F, Lin T, Wang Z, Liu J, Zeng X (2020) The expression and function of opsin genes related to the phototactic behavior of Asian citrus psyllid. Pest Management Science 76:1578–1587

    CAS  PubMed  Google Scholar 

  • Lin YH, Huang JH, Liu Y, Belles X, Lee HJ (2017) Oral delivery of dsRNA lipoplexes to German cockroach protects dsRNA from degradation and induces RNAi response. Pest Management Science 73:960–966

    CAS  PubMed  Google Scholar 

  • Lu ZJ, Huang YL, Yu HZ, Li NY, Xie YX, Zhang Q, Zeng XD, Hu H, Huang AJ, Yi L, Su HN (2019a) Silencing of the Chitin Synthase Gene Is Lethal to the Asian Citrus Psyllid, Diaphorina citri. International Journal of Molecular Sciences 20(15)

  • Lu ZJ, Zhou CH, Yu HZ, Huang YL, Liu YX, Xie YX, Wang J, Hu W, Huang AJ, Su HN, Yang C (2019b) Potential roles of insect Tropomyosin1-X1 isoform in the process of Candidatus Liberibacter asiaticus infection of Diaphorina citri. Journal of Insect Physiology 114:125–135

    CAS  PubMed  Google Scholar 

  • Lucas K, Raikhel AS (2013) Insect microRNAs: biogenesis, expression profiling and biological functions. Insect Biochemistry and Molecular Biology 43:24–38

    CAS  PubMed  Google Scholar 

  • Matsumoto Y, Hattori M (2016) Gene silencing by parental RNA interference in the Green Rice Leafhopper, Nephotettix cincticeps (Hemiptera: Cicadellidae). Archives of Insect Biochemistry and Physiology 91:152–164

    CAS  PubMed  Google Scholar 

  • Mon H, Kobayashi I, Ohkubo S, Tomita S, Lee J, Sezutsu H, Tamura T, Kusakabe T (2012) Effective RNA interference in cultured silkworm cells mediated by overexpression of Caenorhabditis elegans SID-1. RNA Biology 9:40–46

    CAS  PubMed  Google Scholar 

  • Ni M, Ma W, Wang X, Gao M, Dai Y, Wei X, Zhang L, Peng Y, Chen S, Ding L (2017) Next-generation transgenic cotton: pyramiding RNAi and Bt counters insect resistance. Plant Biotechnology Journal 15:1204–1213

    CAS  PubMed  PubMed Central  Google Scholar 

  • Palli SR (2014) RNA interference in Colorado potato beetle: steps toward development of dsRNA as a commercial insecticide. Current Opinion in Insect Science 6:1–8

    PubMed  PubMed Central  Google Scholar 

  • Pardo S, Martínez AM, Figuero JI, Chavarrieta JM, Viñuela E, Rebollar-Alviter Á, Miranda MA, Valle J, Pineda S (2018) Insecticide resistance of adults and nymphs of Asian citrus psyllid populations from Apatzingán Valley, Mexico. Pest Management Science 74:135–140

    CAS  PubMed  Google Scholar 

  • Price DR, Gatehouse JA (2008) RNAi-mediated crop protection against insects. Trends in Biotechnology 26:393–400

    CAS  PubMed  Google Scholar 

  • 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. Scientific Reports 7:8913

    PubMed  PubMed Central  Google Scholar 

  • Saleh M-C, van Rij RP, Hekele A, Gillis A, Foley E, O’Farrell PH, Andino R (2006) The endocytic pathway mediates cell entry of dsRNA to induce RNAi silencing. Nature Cell Biology 8:793

    CAS  PubMed  PubMed Central  Google Scholar 

  • San Miguel K, Scott JG (2015) The next generation of insecticides: dsRNA is stable as a foliar-applied insecticide. Pest Management Science 72:801–809

    PubMed  Google Scholar 

  • Santos-Ortega Y, Killiny N (2018) Silencing of sucrose hydrolase causes nymph mortality and disturbs adult osmotic homeostasis in Diaphorina citri (Hemiptera: Liviidae). Insect Biochemistry and Molecular Biology 101:131–143

    CAS  PubMed  Google Scholar 

  • Scott JG, Michel K, Bartholomay LC, Siegfried BD, Hunter WB, Smagghe G, Zhu KY, Douglas A (2013) Towards the elements of successful insect RNAi. Journal Insect Physiology 59:1212–1221

    CAS  Google Scholar 

  • Smardon A, Spoerke JM, Stacey SC, Klein ME, Mackin N, Maine EM (2000) EGO-1 is related to RNA-directed RNA polymerase and functions in germ-line development and RNA interference in C. elegans. Current Biology 10:169–178

    CAS  PubMed  Google Scholar 

  • Spit J, Philips A, Wynant N, Santos D, Plaetinck G, Broeck JV (2017) Knockdown of nuclease activity in the gut enhances RNAi efficiency in the Colorado potato beetle, Leptinotarsa decemlineata, but not in the desert locust, Schistocerca gregaria. Insect Biochemistry and Molecular Biology 81:103–116

    CAS  PubMed  Google Scholar 

  • Taning CN, Andrade EC, Hunter WB, Christiaens O, Smagghe G (2016) Asian Citrus Psyllid RNAi Pathway–RNAi evidence. Scientific Reports 6:38082

    CAS  PubMed  PubMed Central  Google Scholar 

  • Terenius O, Papanicolaou A, Garbutt JS, Eleftherianos I, Huvenne H, Kanginakudru S, Albrechtsen M, An C, Aymeric JL, Barthel A, Bebas P, Bitra K, Bravo A, Chevalier F, Collinge DP, Crava CM, de Maagd RA, Duvic B, Erlandson M, Faye I, Felfoldi G, Fujiwara H, Futahashi R, Gandhe AS, Gatehouse HS, Gatehouse LN, Giebultowicz JM, Gomez I, Grimmelikhuijzen CJ, Groot AT, Hauser F, Heckel DG, Hegedus DD, Hrycaj S, Huang L, Hull JJ, Iatrou K, Iga M, Kanost MR, Kotwica J, Li C, Li J, Liu J, Lundmark M, Matsumoto S, Meyering-Vos M, Millichap PJ, Monteiro A, Mrinal N, Niimi T, Nowara D, Ohnishi A, Oostra V, Ozaki K, Papakonstantinou M, Popadic A, Rajam MV, Saenko S, Simpson RM, Soberon M, Strand MR, Tomita S, Toprak U, Wang P, Wee CW, Whyard S, Zhang W, Nagaraju J, French-Constant RH, Herrero S, Gordon K, Swevers L, Smagghe G (2011) RNA interference in Lepidoptera: an overview of successful and unsuccessful studies and implications for experimental design. Journal of Insect Physiology 57:231–245

    CAS  PubMed  Google Scholar 

  • Tian F, Li C, Wang Z, Liu J, Zeng X (2019a) Identification of detoxification genes in imidacloprid-resistant Asian citrus psyllid (Hemiptera: Lividae) and their expression patterns under stress of eight insecticides. Pest Management Science 75:1400–1410

    CAS  PubMed  Google Scholar 

  • Tian F, Wang Z, Li C, Liu J, Zeng X (2019) UDP-Glycosyltransferases are involved in imidacloprid resistance in the Asian citrus psyllid, Diaphorina citri (Hemiptera: Lividae). Pesticide Biochemistry and Physiolology 154:23–31

    CAS  Google Scholar 

  • Tiwari S, Mann RS, Rogers M, Stelinski LL (2011) Insecticide resistance in field populations of Asian citrus psyllid in Florida. Pest Management Science 67:1258–1268

    CAS  PubMed  Google Scholar 

  • Tomoyasu Y, Miller SC, Tomita S, Schoppmeier M, Grossmann D, Bucher G (2008) Exploring systemic RNA interference in insects: a genome-wide survey for RNAi genes in Tribolium. Genome Biology 9:R10

    PubMed  PubMed Central  Google Scholar 

  • Ulvila J, Parikka M, Kleino A, Sormunen R, Ezekowitz RA, Kocks C, Rämet M (2006) Double-stranded RNA is internalized by scavenger receptor-mediated endocytosis in Drosophila S2 cells. Journal of Biological Chemistry 281:14370–14375

    CAS  PubMed  Google Scholar 

  • Upadhyay SK, Chandrashekar K, Thakur N, Verma PC, Borgio JF, Singh PK, Tuli R (2011) RNA interference for the control of whiteflies (Bemisia tabaci) by oral route. Journal of Biosciences 36:153–161

    CAS  PubMed  Google Scholar 

  • van Cleef KW, van Mierlo JT, Miesen P, Overheul GJ, Fros JJ, Schuster S, Marklewitz M, Pijlman GP, Junglen S, van Rij RP (2014) Mosquito and Drosophila entomobirnaviruses suppress dsRNA-and siRNA-induced RNAi. Nucleic Acids Research 42:8732–8744

    PubMed  PubMed Central  Google Scholar 

  • Wang N, Trivedi P (2013) Citrus huanglongbing: a newly relevant disease presents unprecedented challenges. Phytopathology 103:652–665

    PubMed  Google Scholar 

  • Wang N, Pierson EA, Setubal JC, Xu J, Levy JG, Zhang Y, Li J, Rangel LT, Martins J Jr (2017) The Candidatus Liberibacter–Host Interface: Insights into Pathogenesis Mechanisms and Disease Control. Annual Review of Phytopathology 55:451–482

    CAS  PubMed  Google Scholar 

  • Whangbo JS, Hunter CP (2008) Environmental RNA interference. Trends in Genetics 24:297–305

    CAS  PubMed  Google Scholar 

  • Whitten M, Dyson P (2017) Gene silencing in non-model insects: Overcoming hurdles using symbiotic bacteria for trauma-free sustainable delivery of RNA interference. BioEssays 39:1600247

    Google Scholar 

  • Whitten MM, Facey PD, Del Sol R, Fernández-Martínez LT, Evans MC, Mitchell JJ, Bodger OG, Dyson PJ (2016) Symbiont-mediated RNA interference in insects. Proceedings of the Royal Society Biological Sciences Series B 283:20160042

  • Xiao D, Gao X, Xu J, Liang X, Li Q, Yao J, Zhu KY (2015) Clathrin-dependent endocytosis plays a predominant role in cellular uptake of double-stranded RNA in the red flour beetle. Insect Biochemistry and Molecular Biology 60:68–77

    CAS  PubMed  Google Scholar 

  • Yao J, Rotenberg D, Afsharifar A, Barandoc-Alviar K, Whitfield AE (2013) Development of RNAi methods for Peregrinus maidis, the corn planthopper. PLoS One 8:e70243

    CAS  PubMed  PubMed Central  Google Scholar 

  • Yu X, Killiny N (2018a) Effect of parental RNA interference of a transformer-2 homolog on female reproduction and offspring sex determination in Asian citrus psyllid. Physiological Entomology 43:42–50

    CAS  Google Scholar 

  • Yu X, Killiny N (2018b) Effect of silencing a boule homologue on the survival and reproduction of Asian citrus psyllid Diaphorina citri. Physiological Entomology 43:268–275

    CAS  Google Scholar 

  • Yu X, Killiny N (2018c) RNA interference of two glutathione S-transferase genes, Diaphorina citri DcGSTe2 and DcGSTd1, increases the susceptibility of Asian citrus psyllid (Hemiptera: Liviidae) to the pesticides fenpropathrin and thiamethoxam. Pest Management Science 74:638–647

    CAS  PubMed  Google Scholar 

  • Yu X, Wang G, Huang S, Ma Y, Xia L (2014) Engineering plants for aphid resistance: current status and future perspectives. Theoretical and Applied Genetics 127:2065–2083

    CAS  PubMed  Google Scholar 

  • Yu X-D, Jones HD, Sun Y-W, Wang G-P, Xia L-Q (2016a) 12 Cross-species Silencing: Plant-mediated RNAi for Insect Control. In: Jones HD (ed) Biotechnology of Major Cereals. CAB International, Wallingford, pp 151–164

    Google Scholar 

  • Yu XD, Liu ZC, Huang SL, Chen ZQ, Sun YW, Duan PF, Ma YZ, Xia LQ (2016b) RNAi-mediated Plant Protection against Aphids. Pest Management Science 72:1090–1098

    CAS  PubMed  Google Scholar 

  • Yu X, Gowda S, Killiny N (2017) Double stranded RNA delivery through soaking, mediates silencing of the muscle protein 20 and increases mortality to the Asian citrus psyllid, Diaphorina citri. Pest Management Science 73:1846–1853

    CAS  PubMed  Google Scholar 

  • Yu HZ, Li NY, Li B, Toufeeq S, Xie YX, Huang YL, Du YM, Zeng XD, Zhu B, Lu ZJ (2020) Immune Functional Analysis of Chitin Deacetylase 3 from the Asian Citrus Psyllid Diaphorina citri. International Journal of Molecular Sciences 21(1)

  • Zhang X, Zhang J, Zhu KY (2010) Chitosan/double-stranded RNA nanoparticle-mediated RNA interference to silence chitin synthase genes through larval feeding in the African malaria mosquito (Anopheles gambiae). Insect Molecular Biology 19:683–693

    PubMed  Google Scholar 

  • Zhang J, Khan SA, Hasse C, Ruf S, Heckel DG, Bock R (2015) Pest control. Full crop protection from an insect pest by expression of long double-stranded RNAs in plastids. Science 347:991–994

    CAS  PubMed  Google Scholar 

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Acknowledgements

The authors thank our lab members for their helpful discussion and suggestions. Some works mentioned in this paper are funded by the National Natural Science Foundation of China (Grant no. 31601379), and the grant no. 201500955-04 from SCRI-NIFA, USDA.

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Yu, X., Killiny, N. RNA interference-mediated control of Asian citrus psyllid, the vector of the huanglongbing bacterial pathogen. Trop. plant pathol. 45, 298–305 (2020). https://doi.org/10.1007/s40858-020-00356-7

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