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Tribolium castaneum as a Model for High-Throughput RNAi Screening

  • Eileen Knorr
  • Linda Bingsohn
  • Michael R. Kanost
  • Andreas VilcinskasEmail author
Chapter
Part of the Advances in Biochemical Engineering/Biotechnology book series (ABE, volume 136)

Abstract

Coleopteran insects are a highly diverse and successful order, and many beetle species are significant agricultural pests. New biorational strategies for managing populations of beetles and other insect species are needed as pests develop resistance to chemical insecticides and Bt toxins. There is now an opportunity to use genome sequence data to identify genes that are essential for insect growth, development, or survival as new targets for designing control technology. This goal requires a method for high-throughput in vivo screening of thousands of genes to identify candidate genes that, when their expression is disrupted, have a phenotype that may be useful in insect pest control. Tribolium castaneum, the red flour beetle, is a model organism that offers considerable advantages for such screening, including ease of rearing in large numbers, a sequenced genome, and a strong, systemic RNAi response for specific depletion of gene transcripts. The RNAi effect in T. castaneum can be elicited in any tissue and any stage by the injection of dsRNA into the hemocoel, and injection of dsRNA into adult females can even be used to identify phenotypes in offspring. A pilot RNAi screen (iBeetle) is underway. Several T. castaneum genes with promising RNAi phenotypes for further development as mechanisms for plant protection have been identified. These include heat shock protein 90, chitin synthase, the segmentation gene hairy, and a matrix metalloprotease. Candidate genes identified in T. castaneum screens can then be tested in agricultural pest species (in which screening is not feasible), to evaluate their effectiveness for use in potential plant-based RNAi control strategies. Delivery of dsRNA expressed by genetically modified crops to the midgut of phytophagous insects is under investigation as a new tool for very specific protection of plants from insect pest species. The T. castaneum screening platform offers a system for discovery of candidate genes with high potential benefit.

Graphical Abstract

Keywords

Tribolium castaneum RNAi Pest control Target genes Transgenic plants 

Abbreviations

RNAi

RNA interference

dsRNA

double stranded RNA

siRNA

short interfering RNAs

Bt

Bacillus thuringiensis

WCR

Western corn rootworm

RKN

Root knot nematode

HSP90

Heat shock protein

MMP

Matrix metalloproteinase

References

  1. 1.
    Alves AP, Lorenzen MD, Beeman RW, Foster JE, Siegfried BD (2010) RNA interference as a method for target-site screening in the western corn rootworm, Diabrotica virgifera virgifera. J Insect Sci 10:1–16CrossRefGoogle Scholar
  2. 2.
    Arakane Y, Specht CA, Kramer KJ, Muthukrishnan S, Beeman RW (2008) Chitin synthases are required for survival, fecundity and egg hatch in the red flour beetle, Tribolium castaneum. Insect Biochem Mol Biol 38:959–962CrossRefGoogle Scholar
  3. 3.
    Aranda M, Marques-Souza H, Bayer T, Tautz D (2008) The role of the segmentation gene hairy in Tribolium. Dev Genes Evol 218:465–477CrossRefGoogle Scholar
  4. 4.
    Araujo RN, Santos A, Pinto FS, Gontijo NF, Lehane MJ, Pereira MH (2006) RNA interference of the salivary gland nitrophorin 2 in the triatomine bug Rhodnius prolixus (Hemiptera: Reduviidae) by dsRNA ingestion or injection. Insect Biochem Mol Biol 36:683–693CrossRefGoogle Scholar
  5. 5.
    Aronstein K, Oppert B, Lorenzen MD (2011) RNAi in agriculturally-important arthropods. In: Grabowski P (ed) RNA processing. InTech, Rijeka, pp 157–180Google Scholar
  6. 6.
    Artymovich KA (2009) Using RNA interference to increase crop yield and decrease pest damage. MMG 445 Basic Biotechnol eJ 5:7–12Google Scholar
  7. 7.
    Ashrafi K, Chang FY, Watts JL, Fraser AG, Kamath RS, Ahringer J, Ruvkun G (2003) Genome-wide RNAi analysis of Caenorhabditis elegans fat regulatory genes. Nature 421:268–272CrossRefGoogle Scholar
  8. 8.
    Bagla P (2010) Hardy cotton-munching pests are latest blow to GM crops. Science 327:1439Google Scholar
  9. 9.
    Baum JA, Bogaert T, Clinton W, Heck GR, Feldmann P, Ilagan O, Johnson S, Plaetinck G, Munyikwa T, Pleau M, Vaughn T, Roberts J (2007) Control of coleopteran insect pests through RNA interference. Nat Biotechnol 25:1322–1326CrossRefGoogle Scholar
  10. 10.
    Bautista MA, Miyata T, Miura K, Tanaka T (2009) RNA interference-mediated knockdown of a cytochrome P450, CYP6BG1, from the diamondback moth, Plutella xylostella, reduces larval resistance to permethrin. Insect Biochem Mol Biol 39:38–46CrossRefGoogle Scholar
  11. 11.
    Bernstein E, Caudy AA, Hammond SM, Hannon GJ (2001) Role for a bidentate ribonuclease in the initiation step of RNA interference. Nature 409:363–366CrossRefGoogle Scholar
  12. 12.
    Bolognesi R, Ramaseshadri P, Anderson J, Bachman P, Clinton W, Flannagan R, Ilagan O, Lawrence C, Levine S, Moar W, Mueller G, Tan J, Uffman J, Wiggins E, Heck G, Segers G (2012) Characterizing the mechanism of action of double-stranded RNA activity against western corn rootworm (Diabrotica virgifera virgifera LeConte). PLoS One 7:e47534CrossRefGoogle Scholar
  13. 13.
    Boutros M, Kiger AA, Armknecht S, Kerr K, Hild M, Koch B, Haas SA, Paro R, Perrimon N, Heidelberg Fly Array Consortium (2004) Cell culture genome-wide RNAi analysis of growth and viability in Drosophila cells. Science 303:832–835Google Scholar
  14. 14.
    Bravo A, del Rincon-Castro MC, Ibarra JE, Soberon M (2011) Towards a healthy control of insect pests: potential use of microbial insecticides. In: Lopez O, Fernandez-Bolanos JG (eds) Green trends in insect control, vol 11. RSC Green Chemistry Books, Holanda, 266–299 Google Scholar
  15. 15.
    Bucher G, Scholten J, Klingler M (2002) Parental RNAi in Tribolium (Coleoptera). Curr Biol 12:R85–R86CrossRefGoogle Scholar
  16. 16.
    De Maagd RA, Bravo A, Crickmore N (2001) How Bacillus thuringiensis has evolved specific toxins to colonize the insect world. Trends Genet 17:193–199CrossRefGoogle Scholar
  17. 17.
    Dong Y, Friedrich M (2005) Nymphal RNAi: systemic RNAi mediated gene knockdown in juvenile grasshopper. BMC Biotechnol 5:25CrossRefGoogle Scholar
  18. 18.
    Dutt U (2007) Mealy bug infestation in Punjab: Bt cotton falls flat. Environment News Service. http://www.countercurrents.org. 21 Aug
  19. 19.
    Eaton BA, Fetter RD, Davis GW (2002) Dynactin is necessary for synapse stabilization. Neuron 34:729–741CrossRefGoogle Scholar
  20. 20.
    Elbashir SM, Martinez J, Patkaniowska A, Lendeckel W, Tuschl T (2001) Functional anatomy of siRNAs for mediating efficient RNAi in Drosophila melanogaster embryo lysate. EMBO J 20:6877–6888CrossRefGoogle Scholar
  21. 21.
    Escobar MA, Civerolo EL, Summerfelt KR, Dandekar AM (2001) RNAi-mediated oncogene silencing confers resistance to crown gall tumorigenesis. Proc Natl Acad Sci U S A 98:13437–13442CrossRefGoogle Scholar
  22. 22.
    Farhan H, Wendeler MW, Mitrovic S, Fava E, Silberberg Y, Sharan R, Zerial M, Hauri HP (2010) MAPK signaling to the early secretory pathway revealed by ki-nase/phosphatase functional screening. J Cell Biol 189:997–1011CrossRefGoogle Scholar
  23. 23.
    Feinberg EH, Hunter CP (2003) Transport of dsRNA into cells by the transmembrane protein SID-1. Science 301:1545–1547CrossRefGoogle Scholar
  24. 24.
    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 391:806–811CrossRefGoogle Scholar
  25. 25.
    Gassmann AJ (2012) Field-evolved resistance to Bt maize by western corn rootworm: predictions from the laboratory and effects in the field. J Invertebr Pathol 110:287–293CrossRefGoogle Scholar
  26. 26.
    Gatehouse JA (2002) Plant resistance towards insect herbivores: a dynamic interaction. New Phytol 156:145–169CrossRefGoogle Scholar
  27. 27.
    Guo S, Kemphues KJ (1995) Par-1, a gene required for establishing polarity in C. elegans embryos, encodes a putative Ser/Thr kinase that is asymmetrically distributed. Cell 81:611–620CrossRefGoogle Scholar
  28. 28.
    Hammond SM, Bernstein E, Beach D, Hannon GJ (2000) An RNA-directed nuclease mediates post-transcriptional gene silencing in Drosophila cells. Nature 404:293–296CrossRefGoogle Scholar
  29. 29.
    Huang G, Allen R, Davis EL, Baum TJ, Hussey RS (2006) Engineering broad root-knot resistance in transgenic plants by RNAi silencing of a conserved and essential root-knot nematode parasitism gene. Proc Natl Acad Sci U S A 103:14302–14306CrossRefGoogle Scholar
  30. 30.
    Huvenne H, Smagghe G (2010) Mechanisms of dsRNA uptake in insects and potential of RNAi for pest control: a review. J Insect Physiol 56:227–235CrossRefGoogle Scholar
  31. 31.
    James C (2009) Global Status of Commercialized Biotech/GM Crops: 2009 ISAAA Briefs No. 41, International Service for the Acquisition of Agri-Biotech Applications, IthacaGoogle Scholar
  32. 32.
    Kaeberlein M, Powers RW 3rd, Steffen KK, Westman EA, Hu D, Dang N, Kerr EO, Kirkland KT, Fields S, Kennedy BK (2005) Regulation of yeast replicative life span by TOR and Sch9 in response to nutrients. Science 310:1193–1196CrossRefGoogle Scholar
  33. 33.
    Kennerdell JR, Carthew RW (2000) Heritable gene silencing in Drosophila using double-stranded RNA. Nat Biotechnol 18:896–898CrossRefGoogle Scholar
  34. 34.
    Knorr E, Schmidtberg H, Vilcinskas A, Altincicek B (2009) MMPs regulate both development and immunity in the Tribolium model insect. PLoS One 4:e4751CrossRefGoogle Scholar
  35. 35.
    Knorr E, Vilcinskas A (2011) Post-embryonic functions of HSP90 in Tribolium castaneum include the regulation of compound eye development. Dev Genes Evol 221:357–362CrossRefGoogle Scholar
  36. 36.
    Kruger M, van Rensburg JBJ, van den Berg J (2009) Perspective on the development of stem borer resistance to Bt maize and refuge compliance at the Vaalharts irrigation scheme in South Africa. Crop Prot 28:684–689CrossRefGoogle Scholar
  37. 37.
    Li X, Zhang M, Zhang H (2011) RNA interference of four genes in adult Bactrocera dorsalis by feeding their dsRNAs. PLoS One 6:e17788CrossRefGoogle Scholar
  38. 38.
    Luo Y, Wang X, Yu D, Kang L (2012) The SID-1 double-stranded RNA transporter is not required for systemic RNAi in the migratory locust. RNA Biol 9:663–671CrossRefGoogle Scholar
  39. 39.
    Luttrell RG, Ali I, Allen KC, Young SY III, Szalanski A, Williams K, Lorenz G, Parker CD Jr, Blanco C (2004) Resistance to Bt in Arkansas populations of cotton boll-worm. In: Richter DA (ed) Proceedings of the 2004 beltwide cotton conferences, National Cotton Council of America, San Antonio, TX, Memphis, TNGoogle Scholar
  40. 40.
    Lynch JA, Desplan C (2006) A method for parental RNA interference in the wasp Nasonia vitripennis. Nat Protoc 1:486–494CrossRefGoogle Scholar
  41. 41.
    Lynch JA, Panfilio KA, da Fonseca RN (2009) As Tribolium matures as a model insect, Coleopteran community congregates in cologne. Dev Genes Evol 219:531–533CrossRefGoogle Scholar
  42. 42.
    Lynch JA, Roth S (2011) The evolution of dorsal-ventral patterning mechanisms in insects. Genes Dev 25:107–118CrossRefGoogle Scholar
  43. 43.
    Mao YB, Cai WJ, Wang JW, Hong GJ, Tao XY, Wang LJ, Huang YP, Chen XY (2007) Silencing a cotton bollworm P450 monooxygenase gene by plant-mediated RNAi impairs larval tolerance of gossypol. Nat Biotechnol 25:1307–1313CrossRefGoogle Scholar
  44. 44.
    Martinez J, Patkaniowska A, Urlaub H, Lührmann R, Tuschl T (2002) Single-stranded antisense siRNAs guide target RNA cleavage in RNAi. Cell 110:563–574CrossRefGoogle Scholar
  45. 45.
    Mendelsohn M, Kough J, Vaituzis Z, Matthews K (2003) Are Bt crops safe? Nat Biotechnol 21:1003–1009CrossRefGoogle Scholar
  46. 46.
    Miller SC, Miyata K, Brown SJ, Tomoyasu Y (2012) Dissecting systemic RNA interference in the red flour beetle Tribolium castaneum: parameters affecting the efficiency of RNAi. PLoS One 7:e47431CrossRefGoogle Scholar
  47. 47.
    Morris K, Lorenzen MD, Hiromasa Y, Tomich JM, Oppert C, Elpidina EN, Vinokurov K, Jurat-Fuentes JL, Fabrick J, Oppert B (2009) Tribolium castaneum larval gut transcriptome and proteome: a resource for the study of the coleopteran gut. J Proteome Res 8:3889–3898CrossRefGoogle Scholar
  48. 48.
    Morton DG, Hoose WA, Kemphues KJ (2012) A genome-wide RNAi screen for enhancers of par mutants reveals new contributors to early embryonic polarity in Caenorhabditis elegans. Genetics 192:929–942CrossRefGoogle Scholar
  49. 49.
    Napoli C, Lemieux C, Jorgensen R (1990) Introduction of a chimeric chalcone synthase gene into petunia results in reversible co-suppression of homologous genes in trans. Plant Cell 2:279–289CrossRefGoogle Scholar
  50. 50.
    Newmark PA, Reddien PW, Cebrià F, Sánchez Alvarado A (2003) Ingestion of bacterially expressed double-stranded RNA inhibits gene expression in planarians. Proc Natl Acad Sci U S A 30(100 Suppl 1):11861–11865CrossRefGoogle Scholar
  51. 51.
    Noh MY, Beeman RW, Arakane Y (2012) RNAi-based functional genomics in Tribolium castaneum and possible application for controlling insect pests. Entomol Res 42:1–10CrossRefGoogle Scholar
  52. 52.
    Phillips TW, Throne JE (2010) Biorational approaches to managing stored-product insects. Ann Rev Entomol 55:375–397CrossRefGoogle Scholar
  53. 53.
    Pisa V, Cozzolino M, Gargiulo S, Ottone C, Piccioni F, Monti M, Gigliotti S, Talamo F, Graziani F, Pucci P, Verrotti AC (2009) The molecular chaperone Hsp90 is a component of the cap-binding complex and interacts with the translational re-pressor cup during Drosophila oogenesis. Gene 432:67–74CrossRefGoogle Scholar
  54. 54.
    Pitino M, Coleman AD, Maffei ME, Ridout CJ, Hogenhout SA (2011) Silencing of aphid genes by dsRNA feeding from plants. PLoS One 6:e25709CrossRefGoogle Scholar
  55. 55.
    Price DR, Gatehouse JA (2008) RNAi-mediated crop protection against insects. Trends Biotechnol 26:393–400CrossRefGoogle Scholar
  56. 56.
    Qaim M, de Janvry A (2003) Genetically modified crops, corporate pricing strategies, and farmers’ adoption: the case of Bt cotton in Argentina. Am J Agr Econ 85:814–828CrossRefGoogle Scholar
  57. 57.
    Rajagopal R, Sivakumar S, Agrawal N, Malhotra P, Bhatnagar RK (2002) Silencing of midgut aminopeptidase N of Spodoptera litura by double-stranded RNA establishes its role as Bacillus thuringiensis toxin receptor. Biol Chem 277:46849–46851CrossRefGoogle Scholar
  58. 58.
    Rangasamy M, Siegfried BD (2012) Validation of RNA interference in western corn rootworm Diabrotica virgifera virgifera LeConte (Coleoptera: Chrysomelidae) adults. Pest Manag Sci 68:587–591CrossRefGoogle Scholar
  59. 59.
    Ramaseshadri P, Segers G, Flannagan R, Wiggins E, Clinton W, Ilagan O, McNulty B, Clark T, Bolognesi R (2013) Physiological and cellular responses caused by RNAi-mediated suppression of Snf7 orthologue in western corn rootworm (Diabrotica virgifera virgifera) larvae. PLoS One 8(1):e54270CrossRefGoogle Scholar
  60. 60.
    Rice ME (2004) Transgenic rootworm corn: assessing potential agronomic, economic, and environmental benefits. Plant Health Prog. doi: 10.1094/PHP-2004-0301-01-RV Google Scholar
  61. 61.
    Richter K, Buchner J (2001) Hsp90: chaperoning signal transduction. J Cell Physiol 188:281–290CrossRefGoogle Scholar
  62. 62.
    Roignant JY, Carré C, Mugat B, Szymczak D, Lepesant JA, Antoniewski C (2003) Absence of transitive and systemic pathways allows cell-specific and isoform-specific RNAi in Drosophila. RNA 9:299–308CrossRefGoogle Scholar
  63. 63.
    Rutherford SL, Lindquist S (1998) Hsp90 as a capacitor for morphological evolution. Nature 396:336–342CrossRefGoogle Scholar
  64. 64.
    Saj A, Arziman Z, Stempfle D, van Belle W, Sauder U, Horn T, Dürrenberger M, Paro R, Boutros M, Merdes G (2010) A combined ex vivo and in vivo RNAi screen for notch regulators in Drosophila reveals an extensive notch interaction network. Dev Cell 18:862–876CrossRefGoogle Scholar
  65. 65.
    Sander K (1975) Pattern specification in the insect embryo. Ciba Found Symp 0:241–263Google Scholar
  66. 66.
    Sander K (1976) Specification of the basic body pattern in insect embryogenesis. Adv Insect Physiol 12:125–238CrossRefGoogle Scholar
  67. 67.
    Schwarz DS, Hutvágner G, Du T, Xu Z, Aronin N, Zamore PD (2003) Asymmetry in the assembly of the RNAi enzyme complex. Cell 115:199–208CrossRefGoogle Scholar
  68. 68.
    Shimizu T, Yoshii M, Wei T, Hirochika H, Omura T (2009) Silencing by RNAi of the gene for Pns12, a viroplasm matrix protein of rice dwarf virus, results in strong resistance of transgenic rice plants to the virus. Plant Biotechnol J 7:24–32CrossRefGoogle Scholar
  69. 69.
    Sijen T, Plasterk RH (2003) Transposon silencing in the Caenorhabditis elegans germ line by natural RNAi. Nature 426:310–314CrossRefGoogle Scholar
  70. 70.
    Simón-Mateo C, García JA (2011) Antiviral strategies in plants based on RNA silencing. Biochim Biophys Acta 1809:722–731CrossRefGoogle Scholar
  71. 71.
    Sokoloff A (1972) The biology of Tribolium with special emphasis on genetic aspects 1. Oxford University Press, LondonGoogle Scholar
  72. 72.
    Sokoloff A (1974) The biology of Tribolium with special emphasis on genetic aspects 2. Oxford University Press, LondonGoogle Scholar
  73. 73.
    Sokoloff A (1977) The biology of Tribolium with special emphasis on genetic aspects 3. Oxford University Press, LondonGoogle Scholar
  74. 74.
    Steeves RM, Todd TC, Essig JS, Trick HN (2006) Transgenic soybeans expressing siRNAs specific to a major sperm protein gene suppress Heterodera glycines re-production. Funct Plant Biol 33:991–999CrossRefGoogle Scholar
  75. 75.
    Storer NP, Babcock JM, Schlenz M, Meade T, Thompson GD, Bing JW, Huckaba RM (2010) Discovery and characterization of field resistance to Bt maize: Spodoptera frugiperda (Lepidoptera: Noctuidae) in Puerto Rico. J Econ Entomol 103:1031–1038CrossRefGoogle Scholar
  76. 76.
    Tabara H, Grishok A, Mello CC (1998) RNAi in C. elegans: soaking in the genome sequence. Science 282:430–431CrossRefGoogle Scholar
  77. 77.
    Tabashnik BE, Cushing NL, Finson N, Johnson MW (1990) Field development of resistance to Bacillus thuringiensis in diamondback moth (Lepidoptera: Plutellidae). J Econ Entomol 83:1671–1676CrossRefGoogle Scholar
  78. 78.
    Tabashnik BE, Gassmann AJ, Crowder DW, Carriere Y (2008) Field evolved resistance to Bt toxins. Nature Biotechnol 26:1074–1076CrossRefGoogle Scholar
  79. 79.
    Tabashnik BE, Gassmann AJ, Crowder DW, Carriére Y (2008) Insect resistance to Bt crops: evidence versus theory. Nat Biotechnol 26:199–202CrossRefGoogle Scholar
  80. 80.
    Tabashnik BE, Van Rensburg JB, Carrière Y (2009) Field-evolved insect resistance to Bt crops: definition, theory, and data. J Econ Entomol 102:2011–2025CrossRefGoogle Scholar
  81. 81.
    Tabashnik BE, Wu K, Wu Y (2012) Early detection of field-evolved resistance to Bt cotton in China: cotton bollworm and pink bollworm. J Invertebr Pathol 110:301–306CrossRefGoogle Scholar
  82. 82.
    Tautz D (2004) Segmentation. Dev Cell 7:301–312CrossRefGoogle Scholar
  83. 83.
    Throne JE, Hallman JA, Johnson JA, Follett PA (2003) Post-harvest entomology research in the United States Department of Agriculture-Agricultural Research Service. Pest Manag Sci 59:69–628CrossRefGoogle Scholar
  84. 84.
    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 express-ing dsRNA of a non-midgut gene. PLoS One 4:e6225CrossRefGoogle Scholar
  85. 85.
    Timmons L, Fire A (1998) Specific interference by ingested dsRNA. Nature 395:854CrossRefGoogle Scholar
  86. 86.
    Tomoyasu Y, Denell RE (2004) Larval RNAi in Tribolium (Coleoptera) for analyzing adult development. Dev Genes Evol 214:575–578CrossRefGoogle Scholar
  87. 87.
    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 Biol 9:R10CrossRefGoogle Scholar
  88. 88.
    Tribolium Genome Sequencing Consortium (2008) The genome of the model beetle and pest Tribolium castaneum. Nature 452:949–955Google Scholar
  89. 89.
    Turner CT, Davy MW, MacDiarmid RM, Plummer KM, Birch NP, Newcomb RD (2006) RNA interference in the light brown apple moth, Epiphyas postvittana (Walker) induced by double-stranded RNA feeding. Insect Mol Biol 15:383–391CrossRefGoogle Scholar
  90. 90.
    van den Berg A, Mols J, Han J (2008) RISC-target interaction: cleavage and translational suppression. Biochim Biophys Acta 1779:668–677CrossRefGoogle Scholar
  91. 91.
    van Rensburg JBJ (2007) First report of field resistance by stem borer Busseola fusca (Fuller) to Bt-transgenic maize. S Afr J Plant Soil 27:147–151CrossRefGoogle Scholar
  92. 92.
    Virla EG, Casuso M, Frias EA (2010) A preliminary study on the effects of a transgenic corn event on the non target pest Dalbulus Maiid (Hemitera: Cicadeliidae). Crop Prot 29:635–638CrossRefGoogle Scholar
  93. 93.
    Walshe DP, Lehane SM, Lehane MJ, Haines LR (2009) Prolonged gene knockdown in the tsetse fly Glossina by feeding double stranded RNA. Insect Mol Biol 18:11–19CrossRefGoogle Scholar
  94. 94.
    Wang XH, Aliyari R, Li WX, Li HW, Kim K, Carthew R, Atkinson P, Ding SW (2006) RNA interference directs innate immunity against viruses in adult Drosophila. Science 312:452–454CrossRefGoogle Scholar
  95. 95.
    Waterhouse PM, Wang MB, Lough T (2001) Gene silencing as an adaptive defence against viruses. Nature 411:834–842CrossRefGoogle Scholar
  96. 96.
    Wendler F, Gillingham AK, Sinka R, Rosa-Ferreira C, Gordon DE, Franch-Marro X, Peden AA, Vincent JP, Munro S (2010) A genome-wide RNA interference screen identifies two novel components of the metazoan secretory pathway. EMBO J 29:304–314CrossRefGoogle Scholar
  97. 97.
    Whyard S, Singh AD, Wong S (2009) Ingested double-stranded RNAs can act as species-specific insecticides. Insect Biochem Mol Biol 39:824–832CrossRefGoogle Scholar
  98. 98.
    Winston WM, Sutherlin M, Wright AJ, Feinberg EH, Hunter CP (2007) Caenorhabditis elegans SID-2 is required for environmental RNA interference. Proc Natl Acad Sci U S A 104:10565–10570CrossRefGoogle Scholar
  99. 99.
    Winston WM, Molodowitch C, Hunter CP (2002) Systemic RNAi in C. elegans requires the putative transmembrane protein SID-1. Science 295:2456–2459Google Scholar
  100. 100.
    Wittstock U, Agerbirk N, Stauber EJ, Olsen CE, Hippler M, Mitchell-Olds T, Gershenzon J, Vogel H (2004) Successful herbivore attack due to metabolic diversion of a plant chemical defense. Proc Natl Acad Sci U S A 101:4859–4864CrossRefGoogle Scholar
  101. 101.
    Xu J, Shu J, Zhang Q (2010) Expression of the Tribolium castaneum (Coleoptera: Tenebrionidae) hsp83 gene and its relation to oogenesis during ovarian maturation. J Genet Genomics 37:513–522CrossRefGoogle Scholar
  102. 102.
    Xue XY, MaoYB Tao XY et al (2012) New approaches to agricultural insect pest control based on RNA interference. Adv Insect Physiol 42:73–117CrossRefGoogle Scholar
  103. 103.
    Yadav BC, Veluthambi K, Subramaniam K (2006) Host-generated double stranded RNA induces RNAi in plant-parasitic nematodes and protects the host from infection. Mol Biochem Parasitol 148:219–222CrossRefGoogle Scholar
  104. 104.
    Yu N, Christiaens O, Liu J, Niu J, Cappelle K, Caccia S, Huvenne H, Smagghe G (2013) Delivery of dsRNA for RNAi in insects: an overview and future directions. J Insect Sci 20:4–14CrossRefGoogle Scholar
  105. 105.
    Zamore PD, Tuschl T, Sharp PA, Bartel DP (2000) RNAi: double-stranded RNA directs the ATP-dependent cleavage of mRNA at 21–23 nucleotide intervals. Cell 101:25–33CrossRefGoogle Scholar
  106. 106.
    Zha W, Peng X, Chen R, Du B, Zhu L, He G (2011) Knockdown of midgut genes by dsRNA-transgenic plant-mediated RNA interference in the hemipteran insect Nilaparvata lugens. PLoS One 6:e20504CrossRefGoogle Scholar
  107. 107.
    Zhang H, Li H-C, Miao X-X (2013) Feasibility, limitation and possible solutions of RNAi-based technology for insect pest control. J Insect Sci 20:61–68Google Scholar
  108. 108.
    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 Mol Biol 19:683–693CrossRefGoogle Scholar
  109. 109.
    Zhao YY, Yang G, Wang-Pruski G, You MS (2008) Phyllotreta striolata (Coleoptera: Chrysomelidae): arginine kinase cloning and RNAi-based pest control. Eur J Entomol 105:815–822CrossRefGoogle Scholar
  110. 110.
    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 38:805–815CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2013

Authors and Affiliations

  • Eileen Knorr
    • 1
  • Linda Bingsohn
    • 2
  • Michael R. Kanost
    • 3
  • Andreas Vilcinskas
    • 1
    • 2
    Email author
  1. 1.Institute of Phytopathology and Applied ZoologyJustus-Liebig-University of GiessenGiessenGermany
  2. 2.Department of BioresourcesFraunhofer Institute of Molecular Biology and Applied EcologyGiessenGermany
  3. 3.Department of Biochemistry and Molecular BiophysicsKansas State UniversityManhattanUSA

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