The challenge of RNAi-mediated control of hemipterans.

The post-transcriptional gene silencing mechanism RNA interference (RNAi) has potential as a crop protection strategy against important pest insects. Here we focus on Hemiptera pests, comprising some of the most devastating pest organisms as aphids, whiteflies, psyllids, bedbugs and kissing bugs. At first, a state-of-the-art overview is provided of the progress in RNAi in Hemiptera, as well as on the challenges when developing new RNAi-based pest control strategies against hemipteran pests, such as the delivery of dsRNA and degradation in the insect body. We also discuss the variability in RNAi efficiency as observed between species and experiments, and the factors potentially responsible for this phenomenon.

[1]  G. Smagghe,et al.  Bombyx mori DNA/RNA non-specific nuclease: expression of isoforms in insect culture cells, subcellular localization and functional assays. , 2012, Journal of insect physiology.

[2]  C. Xie,et al.  Silencing of an aphid carboxylesterase gene by use of plant-mediated RNAi impairs Sitobion avenae tolerance of Phoxim insecticides , 2013, Transgenic Research.

[3]  A. Grishok.  RNAi mechanisms in Caenorhabditis elegans , 2005, FEBS letters.

[4]  Daniel G. Anderson,et al.  Action and reaction: the biological response to siRNA and its delivery vehicles. , 2012, Molecular therapy : the journal of the American Society of Gene Therapy.

[5]  T. Daimon,et al.  Importance of juvenile hormone signaling arises with competence of insect larvae to metamorphose. , 2014, Developmental biology.

[6]  G. Reeck,et al.  RNAi Knockdown of a Salivary Transcript Leading to Lethality in the Pea Aphid, Acyrthosiphon pisum , 2006, Journal of insect science.

[7]  Susan J. Brown,et al.  Dissecting Systemic RNA Interference in the Red Flour Beetle Tribolium castaneum: Parameters Affecting the Efficiency of RNAi , 2012, PloS one.

[8]  T. Kaufman,et al.  hunchback is required for suppression of abdominal identity, and for proper germband growth and segmentation in the intermediate germband insect Oncopeltus fasciatus , 2004 .

[9]  K. Pappan,et al.  A protein from the salivary glands of the pea aphid, Acyrthosiphon pisum, is essential in feeding on a host plant , 2008, Proceedings of the National Academy of Sciences.

[10]  Gregor Bucher,et al.  Exploring systemic RNA interference in insects: a genome-wide survey for RNAi genes in Tribolium , 2008, Genome Biology.

[11]  N. Killiny,et al.  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). , 2014, Journal of biotechnology.

[12]  D. Strickman,et al.  Topically Applied AaeIAP1 Double-Stranded RNA Kills Female Adults of Aedes aegypti , 2008, Journal of medical entomology.

[13]  M. F. Potter,et al.  RNA Interference of NADPH-Cytochrome P450 Reductase Results in Reduced Insecticide Resistance in the Bed Bug, Cimex lectularius , 2012, PloS one.

[14]  B. Berkhout,et al.  RNA interference against viruses: strike and counterstrike , 2007, Nature Biotechnology.

[15]  Lili Zhu,et al.  Knockdown of Midgut Genes by dsRNA-Transgenic Plant-Mediated RNA Interference in the Hemipteran Insect Nilaparvata lugens , 2011, PloS one.

[16]  Guy Smagghe,et al.  Mechanisms of dsRNA uptake in insects and potential of RNAi for pest control: a review. , 2010, Journal of insect physiology.

[17]  Guo-Qing Li,et al.  RNAi mediated knockdown of the ryanodine receptor gene decreases chlorantraniliprole susceptibility in Sogatella furcifera. , 2014, Pesticide biochemistry and physiology.

[18]  B. Falk,et al.  Oral Delivery of Double-Stranded RNAs and siRNAs Induces RNAi Effects in the Potato/Tomato Psyllid, Bactericerca cockerelli , 2011, PloS one.

[19]  M. Ghanim,et al.  Tissue-specific gene silencing by RNA interference in the whitefly Bemisia tabaci (Gennadius). , 2007, Insect biochemistry and molecular biology.

[20]  Q. Song,et al.  Molecular basis for insecticide‐enhanced thermotolerance in the brown planthopper Nilaparvata lugens Stål (Hemiptera:Delphacidae) , 2013, Molecular ecology.

[21]  Guy Smagghe,et al.  Towards the elements of successful insect RNAi. , 2013, Journal of insect physiology.

[22]  J. Pritchard,et al.  A water-specific aquaporin involved in aphid osmoregulation. , 2009, Insect biochemistry and molecular biology.

[23]  F. Mury,et al.  Alpha-Glucosidase Promotes Hemozoin Formation in a Blood-Sucking Bug: An Evolutionary History , 2009, PloS one.

[24]  W. B. Walker,et al.  Saliva of Lygus lineolaris digests double stranded ribonucleic acids. , 2012, Journal of insect physiology.

[25]  Hai-Jun Xu,et al.  Molecular characterization of the flightin gene in the wing-dimorphic planthopper, Nilaparvata lugens, and its evolution in Pancrustacea. , 2013, Insect biochemistry and molecular biology.

[26]  R. Paim,et al.  The role of salivary nitrophorins in the ingestion of blood by the triatomine bug Rhodnius prolixus (Reduviidae: Triatominae). , 2009, Insect biochemistry and molecular biology.

[27]  Haichao Li,et al.  Second-Generation Sequencing Supply an Effective Way to Screen RNAi Targets in Large Scale for Potential Application in Pest Insect Control , 2011, PloS one.

[28]  P. Verma,et al.  Enhanced Whitefly Resistance in Transgenic Tobacco Plants Expressing Double Stranded RNA of v-ATPase A Gene , 2014, PloS one.

[29]  Ronald D. Flannagan,et al.  Characterizing the Mechanism of Action of Double-Stranded RNA Activity against Western Corn Rootworm (Diabrotica virgifera virgifera LeConte) , 2012, PloS one.

[30]  Guo-Qing Li,et al.  RNA Interference Depletion of the Halloween Gene Disembodied Implies its Potential Application for Management of Planthopper Sogatella furcifera and Laodelphax striatellus , 2014, PloS one.

[31]  S. Whyard,et al.  Ingested double-stranded RNAs can act as species-specific insecticides. , 2009, Insect biochemistry and molecular biology.

[32]  X. Belles.  Beyond Drosophila: RNAi in vivo and functional genomics in insects. , 2010, Annual review of entomology.

[33]  F. Zeng,et al.  Feeding-Based RNA Intereference of a Gap Gene Is Lethal to the Pea Aphid, Acyrthosiphon pisum , 2012, PloS one.

[34]  Rik Verdonck,et al.  Identification, functional characterization and phylogenetic analysis of double stranded RNA degrading enzymes present in the gut of the desert locust, Schistocerca gregaria. , 2014, Insect biochemistry and molecular biology.

[35]  T. Kaufman,et al.  Hox gene function and interaction in the milkweed bug Oncopeltus fasciatus (Hemiptera). , 2005, Developmental biology.

[36]  O. Christiaens,et al.  DsRNA degradation in the pea aphid (Acyrthosiphon pisum) associated with lack of response in RNAi feeding and injection assay , 2014, Peptides.

[37]  A. Michel,et al.  Core RNAi Machinery and Sid1, a Component for Systemic RNAi, in the Hemipteran Insect, Aphis glycines , 2013, International journal of molecular sciences.

[38]  M. Allen,et al.  RNA interference‐mediated knockdown of IAP in Lygus lineolaris induces mortality in adult and pre‐adult life stages , 2011 .

[39]  W. B. Walker,et al.  Expression and RNA Interference of Salivary Polygalacturonase Genes in the Tarnished Plant Bug, Lygus lineolaris , 2010, Journal of insect science.

[40]  C. Carlini,et al.  A phospholipase A2 gene is linked to Jack bean urease toxicity in the Chagas' disease vector Rhodnius prolixus. , 2014, Biochimica et biophysica acta.

[41]  D. Deforce,et al.  Differential transcriptome analysis of the common shrimp Crangon crangon: special focus on the nuclear receptors and RNAi-related genes. , 2015, General and comparative endocrinology.

[42]  Claude Rispe,et al.  Gene knockdown by RNAi in the pea aphid Acyrthosiphon pisum , 2007, BMC biotechnology.

[43]  G. Smagghe,et al.  The possible impact of persistent virus infection on the function of the RNAi machinery in insects: a hypothesis , 2013, Front. Physiol..

[44]  K. Lu,et al.  Molecular characterization and gene functional analysis of Dicer‐2 gene from Nilaparvata lugens (Hemiptera: Geometroidea) , 2013, Insect science.

[45]  Zhaojun Han,et al.  Cloning and Phylogenetic Analysis of Sid-1-Like Genes from Aphids , 2008, Journal of insect science.

[46]  B. Falk,et al.  RNA Interference towards the Potato Psyllid, Bactericera cockerelli, Is Induced in Plants Infected with Recombinant Tobacco mosaic virus (TMV) , 2013, PloS one.

[47]  Jianzhen Zhang,et al.  Chitosan/double‐stranded RNA nanoparticle‐mediated RNA interference to silence chitin synthase genes through larval feeding in the African malaria mosquito (Anopheles gambiae) , 2010, Insect molecular biology.

[48]  G. Smagghe,et al.  Transcriptional response of BmToll9-1 and RNAi machinery genes to exogenous dsRNA in the midgut of Bombyx mori. , 2013, Journal of insect physiology.

[49]  R. Andino,et al.  Cricket Paralysis Virus (CrPV) antagonizes Argonaute 2 to modulate antiviral defense in Drosophila , 2010, Nature Structural &Molecular Biology.

[50]  N. Killiny,et al.  Silencing Abnormal Wing Disc Gene of the Asian Citrus Psyllid, Diaphorina citri Disrupts Adult Wing Development and Increases Nymph Mortality , 2013, PloS one.

[51]  P. O’Farrell,et al.  The endocytic pathway mediates cell entry of dsRNA to induce RNAi silencing , 2006, Nature Cell Biology.

[52]  A. Tanaka,et al.  Brasiliensin: A novel intestinal thrombin inhibitor from Triatoma brasiliensis (Hemiptera: Reduviidae) with an important role in blood intake , 2007, International journal for parasitology.

[53]  Geert Plaetinck,et al.  Control of coleopteran insect pests through RNA interference , 2007, Nature Biotechnology.

[54]  M. Maffei,et al.  Silencing of Aphid Genes by dsRNA Feeding from Plants , 2011, PloS one.

[55]  P. Verma,et al.  RNA interference for the control of whiteflies (Bemisia tabaci) by oral route , 2011, Journal of Biosciences.

[56]  Zhangwu Zhao,et al.  Influence of catalase gene silencing on the survivability of Sitobion avenae. , 2014, Archives of insect biochemistry and physiology.

[57]  Xinda Lin,et al.  Characterization of the Distal-less gene homologue, NlDll, in the brown planthopper, Nilaparvata lugens (Stål). , 2014, Gene.

[58]  June Hyung Lee,et al.  Dual modes of RNA-silencing suppression by Flock House virus protein B2 , 2005, Nature Structural &Molecular Biology.

[59]  R. Paim,et al.  Long-term effects and parental RNAi in the blood feeder Rhodnius prolixus (Hemiptera; Reduviidae). , 2013, Insect biochemistry and molecular biology.

[60]  S. Fexova,et al.  Juvenile hormone signaling during reproduction and development of the linden bug, Pyrrhocoris apterus. , 2014, Insect biochemistry and molecular biology.

[61]  K. Lu,et al.  Dicer1 is crucial for the oocyte maturation of telotrophic ovary in Nilaparvata lugens (STÅL) (Hemiptera: Geometroidea). , 2013, Archives of insect biochemistry and physiology.

[62]  Isabel Gómez,et al.  RNA interference in Lepidoptera: an overview of successful and unsuccessful studies and implications for experimental design. , 2011, Journal of insect physiology.

[63]  F. Zeng,et al.  Plant-mediated RNAi of a gap gene-enhanced tobacco tolerance against the Myzus persicae , 2013, Transgenic Research.

[64]  T. Wenseleers,et al.  Reproduction of honeybee workers is regulated by epidermal growth factor receptor signaling. , 2014, General and comparative endocrinology.

[65]  T. Kaufman,et al.  Functional analyses in the hemipteran Oncopeltus fasciatus reveal conserved and derived aspects of appendage patterning in insects. , 2004, Developmental biology.