A double-stranded RNA degrading enzyme reduces the efficiency of oral RNA interference in migratory locust

Insect Biochemistry and Molecular Biology

Volumn 86, Issue , 2017, Pages 68-80

  Song, Huifang ^a   Zhang, Jianqin ^a   Li, Daqi ^a,b   Cooper, Anastasia M W ^c   Silver, Kristopher ^c   Li, Tao ^a   Liu, Xiaojian ^a   Ma, Enbo ^a   Zhu, Kun Yan ^c   Zhang, Jianzhen ^a  

^a SHANXI UNIVERSITY   (China)

^b Shanxi Academy of Agricultural Sciences   (China)

^c KANSAS STATE UNIVERSITY   (United States)

Author keywords

dsRNA; dsRNase; Locusta migratoria; Pest management; RNA interference

Indexed keywords

DOUBLE STRANDED RNA; INSECT PROTEIN; RIBONUCLEASE;

AMINO ACID SEQUENCE; ANIMAL; ENZYMOLOGY; LOCUSTA MIGRATORIA; METABOLISM; MOLECULAR GENETICS; RNA INTERFERENCE;

AMINO ACID SEQUENCE; ANIMALS; INSECT PROTEINS; LOCUSTA MIGRATORIA; MOLECULAR SEQUENCE DATA; RIBONUCLEASES; RNA INTERFERENCE; RNA, DOUBLE-STRANDED;

EID: 85020262709     PISSN: 09651748     EISSN: 18790240     Source Type: Journal    
DOI: 10.1016/j.ibmb.2017.05.008     Document Type: Article

References (58)

1. Allen, M.L., Walker, W.B., Saliva of Lygus lineolaris digests double stranded ribonucleic acids. J. Insect Physiol. 58 (2012), 391–396.
2. Andersen, C.L., Jensen, J.L., Ørntoft, T.F., Normalization of real-time quantitative reverse transcription-PCR data: a model-based variance estimation approach to identify genes suited for normalization, applied to bladder and colon cancer data sets. Canc. Res. 64 (2004), 5245–5250.
3. Andrade, C.E., Hunter, W.B., RNA interference – natural gene-based technology for highly specific pest control (HiSPeC). Abdurakhmonov, I.Y., (eds.) RNA Interference. InTech Open, Croatia, 2016, 391–409.
4. Araujo, R.N., Santos, A., Pinto, F.S., Gontijo, N.F., Lehane, M.J., Pereira, M.H., 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 (2006), 683–693.
5. Arimatsu, Y., Furuno, T., Sugimura, Y., Togoh, M., Ishihara, R., Tokizane, M., Kotani, E., Hayashi, Y., Furusawa, T., Purification and properties of double-stranded RNA-degrading nuclease, dsRNase, from the digestive juice of the silkworm, Bombyx mori. J. Insect Biotechnol. Sericol 76 (2007), 57–62.
6. Arimatsu, Y., Kotani, E., Sugimura, Y., Furusawa, T., Molecular characterization of a cDNA encoding extracellular dsRNase and its expression in the silkworm, Bombyx mori. Insect biochem. Mol. Biol. 37 (2007), 176–183.
7. Baum, J.A., Bogaert, T., Clinton, W., Heck, G.R., Feldmann, P., Ilagan, O., Johnson, S., Plaetinck, G., Munyikwa, T., Pleau, M., Vaughn, T., Roberts, J., Control of coleopteran insect pests through RNA interference. Nat. Biotechnol. 25 (2007), 1322–1326.
8. Baum, J.A., Roberts, J.K., Progress towards RNAi-mediated insect pest management. Adv. Insect Physiol. 47 (2014), 249–295.
9. Bettencourt, R., Terenius, O., Faye, I., Hemolin gene silencing by ds-RNA injected into Cecropia pupae is lethal to next generation embryos. Insect Mol. Biol. 11 (2002), 267–271.
10. Britton, H.T.S., Robinson, R.A., Universal buffer solutions and the dissociation constant of veronal. J. Chem. Soc., 1931, 1456–1462.
11. Christiaens, O., Swevers, L., Smagghe, G., DsRNA degradation in the pea aphid (Acyrthosiphon pisum) associated with lack of response in RNAi feeding and injection assay. Peptides 53 (2014), 307–314.
12. Das, S., RNA Interference: an environment friendly approach for targeted pest management. Entomol. Ornithol. Herpetol. Curr. Res. 4 (2015), 3–4.
13. Das, S., Debnath, N., Cui, Y., Unrine, J., Palli, S.R., Chitosan, carbon quantum dot, and silica nanoparticle mediated dsRNA delivery for gene silencing in Aedes aegypti: a comparative analysis. ACS Appl. Mater Inter 7 (2015), 19530–19535.
14. Fire, A., Xu, S.Q., Montgomery, M.K., Kostas, S.A., Driver, S.E., Mello, C.C., Potent and specific genetic interference by double-stranded RNA in Caenorhabditis elegans. Nature 391 (1998), 806–811.
15. Friedhoff, P., Gimadutdinow, O., Pingoud, A., Identification of catalytically relevant amino acids of the extracellular Serratia marcescens endonuclease by alignment-guided mutagenesis. Nucleic Acids Res. 22 (1994), 3280–3287.
16. Friedhoff, P., Kolmes, B., Gimadutdinow, O., Wende, W., Krause, K.L., Pingoud, A., Analysis of the mechanism of the Serratia nuclease using site-directed mutagenesis. Nucleic Acids Res. 24 (1996), 2632–2639.
17. Garbian, Y., Maori, E., Kalev, H., Shafir, S., Sela, I., Bidirectional transfer of RNAi between honey bee and Varroa destructor: varroa gene silencing reduces Varroa population. PLoS Pathog., 8, 2012, e1003035.
18. Garbutt, J.S., Bellés, X., Richards, E.H., Reynolds, S.E., Persistence of double-stranded RNA in insect hemolymph as a potential determiner of RNA interference success: evidence from Manduca sexta and Blattella germanica. J. Insect Physiol. 59 (2013), 171–178.
19. He, B., Chu, Y., Yin, M., Müllen, K., An, C., Shen, J., Fluorescent nanoparticle delivered dsRNA toward genetic control of insect pests. Adv. Mater 25 (2013), 4580–4584.
20. Hunter, W., Ellis, J., Van Engelsdorp, D., Hayes, J., Westervelt, D., Glick, E., Williams, M., Sela, I., Maori, E., Pettis, J., Cox-Foster, D., Paldi, N., Large-scale field application of RNAi technology reducing Israeli acute paralysis virus disease in honey bees (Apis mellifera, Hymenoptera: apidae). PLoS Pathog., 6, 2010, e1001160.
21. Jin, S., Singh, N.D., Li, L., Zhang, X., Daniell, H., Engineered chloroplast dsRNA silences cytochrome p450 monooxygenase, V-ATPase and chitin synthase genes in the insect gut and disrupts Helicoverpa armigera larval development and pupation. Plant Biotechnol. J. 13 (2015), 435–446.
22. Li, D.Q., Zhang, J.Q., Wang, Y., Liu, X.J., Ma, E.B., Sun, Y., Li, S., Zhu, K.Y., Zhang, J.Z., Two chitinase 5 genes from locusta migratoria: molecular characteristics and functional differentiation. Insect biochem. Mol. Biol. 58 (2015), 46–54.
23. Li, Y.L., Song, H.F., Zhang, X.Y., Li, D.Q., Zhang, T.T., Ma, E.B., Zhang, J.Z., Heterologous expression and characterization of two chitinase 5 enzymes from the migratory locust Locusta migratoria. Insect Sci. 23 (2016), 406–416.
24. Lim, Z.X., Robinson, K.E., Jain, R.G., Chandra, G.S., Asokan, R., Asgari, S., Mitter, N., Diet-delivered RNAi in Helicoverpa armigera - progresses and challenges. J. Insect Physiol. 85 (2016), 86–93.
25. Liu, J., Swevers, L., Iatrou, K., Huvenne, H., Smagghe, G., Bombyx mori DNA/RNA non-specific nuclease: expression of isoforms in insect culture cells, subcellular localization and functional assays. J. Insect. Physiol. 58 (2012), 1166–1176.
26. Lomer, C.J., Bateman, R.P., Johnson, D.L., Langewald, J., Thomas, M., Biological control of locusts and grasshoppers. Annu. Rev. Entomol. 46 (2001), 667–702.
27. Luo, Y., Wang, X., Wang, X., Yu, D., Chen, B., Kang, L., Differential responses of migratory locusts to systemic RNA interference via double-stranded RNA injection and feeding. Insect Mol. Biol. 22 (2013), 574–583.
28. Machado, V., Rodriguez-Garcia, M.J., Sanchez-Garcia, F.J., Galian, J., RNA Interference: a new strategy in the evolutionary arms race between human control strategies and insect pests. Folia Biol. 62 (2014), 335–343.
29. Mao, Y.B., Cai, W.J., Wang, J.W., Hong, G.J., Tao, X.Y., Wang, L.J., Huang, Y.P., Chen, X.Y., Silencing a cotton bollworm P450 monooxygenase gene by plant-mediated RNAi impairs larval tolerance of gossypol. Nat. Biotechnol. 25 (2007), 1307–1313.
30. Martín, D., Maestro, O., Cruz, J., Mané-Padrós, D., Bellés, X., RNAi studies reveal a conserved role for RXR in molting in the cockroach Blattella germanica. J. Insect Physiol. 52 (2006), 410–416.
31. Miller, M.D., Tanner, J., Alpaugh, M., Benedik, M.J., Krause, K.L., 2.1 Å structure of serratia endonuclease suggests a mechanism for binding to double-stranded DNA. Nat. Struct. Biol. 1 (1994), 461–468.
32. Nicholas, K.B., Nicholas, H.B., GeneDoc: a Tool for Editing and Annotating Multiple Sequence Alignments. 1997, Published online by the National Resource for Biomedical Supercomputing, Pittsburgh, PA www.psc.edu/biomed/genedoc.
33. Pitino, M., Coleman, A.D., Maffei, M.E., Ridout, C.J., Hogenhout, S.A., Silencingof aphid genes by dsRNA feeding from plants. PLoS One, 6, 2011, e25709.
34. Ren, D., Cai, Z., Song, J., Wu, Z., Zhou, S., DsRNA uptake and persistence account for tissue-dependent susceptibility to RNA interference in the migratory locust, Locusta migratoria. Insect Mol. Biol. 23 (2014), 175–184.
35. Rodrigues, T.B., Figueira, A., Management of insect pest by RNAi–a new tool for crop protection. Abdurakhmonov, I.Y., (eds.) RNA Interference. InTech Open, Croatia, 2016, 371–390.
36. Revuelta, L., Piulachs, M.D., Bellés, X., Castañera, P., Ortego, F., Díaz-Ruíz, J.R., Hernández-Crespo, P., Tenllado, F., RNAi of ace1 and ace2 in Blattella germanica reveals their differential contribution to acetylcholinesterase activity and sensitivity to insecticides. Insect biochem. Mol. Biol. 39 (2009), 913–919.
37. Sanitt, P., Apiratikul, N., Niyomtham, N., Yingyongnarongkul, B.E., Assavalapsakul, W., Panyim, S., Udomkit, A., Cholesterol-based cationic liposome increases dsRNA protection of yellow head virus infection in Penaeus vannamei. J. Biotechnol. 228 (2016), 95–102.
38. Scott, J.G., Michel, K., Bartholomay, L.C., Siegfried, B.D., Hunter, W.B., Smagghe, G., Zhu, K.Y., Douglas, A.E., Towards the elements of successful insect RNAi. J. Insect Physiol. 59 (2013), 1212–1221.
39. Song, T.Q., Yang, M.L., Wang, Y.L., Liu, Q., Wang, H.M., Zhang, J., Li, T., The cuticular protein LmTwdl1 is involved in the molt development of the migratory locust. Insect Sci. 23 (2016), 520–530.
40. Spit, J., Philips, A., Wynant, N., Santos, D., Plaetinck, G., Broeck, V.J., 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 biochem. Mol. Biol. 81 (2017), 103–116.
41. Taning, C.N.T., Christiaens, O., Berkvens, N., Casteels, H., Maes, M., Smagghe, G., Oral RNAi to control Drosophila suzukii: laboratory testing against larval and adult stages. J. Pest Sci. 89 (2016), 803–814.
42. Terenius, O., Papanicolaou, A., Garbutt, J.S., Eleftherianos, I., Huvenne, H., Kanginakudru, S., Albrechtsen, M., An, C., Aymeric, J.L., Barthel, A., Bebas, P., Bitra, K., Bravo, A., Chevalier, F., Colling, D.P., Crava, C.M., de Maagd, R.A., Duvic, B., Erlandson, M., Faye, I., Felföldi, G., Fujiwara, H., Futahashi, R., Gandhe, A.S., Gatehouse, H.S., Gatehouse, L.N., Giebultowicz, J.M., Gómez, I., Grimmelikhuijzen, C.J.P., Groot, A.T., Hauser, F., Heckel, D.G., Hegedus, D.D., Hrycaj, S., Huang, L., Hull, J.J., Iatrou, K., Iga, M., Kanost, M.R., Kotwica, J., Li, C., Li, J., Liu, J., Lundmark, M., Matsumoto, S., Meyering-Vos, M., Millichap, P.J., Monteiro, A., Mrinal, N., Niimi, T., Nowara, D., Ohnishi, A., Oostra, V., Ozaki, K., Papakonstantinou, M., Popadi, A., Rajam, M.V., Saenko, S., Simpson, R.M., Soberón, M., Strand, M.R., Tomita, S., Toprak, U., Wang, P., Wee, C.W., Whyard, S., Zhang, W., Nagaraju, J., ffrench-Constant, R.H., Hererro, S., Gordon, K., Swevers, L., Smagghe, G., RNA interference in Lepidoptera: an overview of successful and unsuccessful studies and implications for experimental design. J. Insect Physiol. 57 (2011), 231–245.
43. Tian, H.G., Peng, H., Yao, Q., Chen, H.X., Xie, Q., Tang, B., Zhang, W.Q., Developmental control of a lepidopteran pest Spodoptera exigua by ingestion of bacteria expressing dsRNA of a non-midgut gene. PLoS One, 4, 2009, e6225.
44. Vandesompele, J., Preter, K.D., Pattyn, F., Poppe, B., Roy, N.V., Paepe, A.D., Speleman, F., Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biol. 3 (2002), 0034.1–0034.11.
45. Wang, X., Fang, X., Yang, P., Jiang, X., Jiang, F., Zhao, D., Li, B., Cui, F., Wei, J., Ma, C., Wang, Y., He, J., Luo, Y., Wang, Z., Guo, X., Guo, W., Wang, X., Zhang, Y., Yang, M., Hao, S., Chen, B., Ma, Z., Yu, D., Xiong, Z., Zhu, Y., Fan, D., Han, L., Wang, B., Chen, Y., Wang, J., Yang, L., Zhao, W., Feng, Y., Chen, G., Lian, J., Li, Q., Huang, Z., Yao, X., Lv, N., Zhang, G., Li, Y., Wang, J., Wang, J., Zhu, B., Kang, L., The locust genome provides insight into swarm formation and long-distance flight. Nat. Commun., 5, 2014, 3957.
46. Wang, K., Peng, Y., Pu, J., Fu, W., Wang, J., Han, Z., Variation in RNAi efficacy among insect species is attributable to dsRNA degradation in vivo. Insect biochem. Mol. Biol. 77 (2016), 1–9.
47. Wang, Y.B., Zhang, H., Li, H.C., Miao, X.X., Second-generation sequencing supply an effective way to screen RNAi targets in large scale for potential application in pest insect control. PLoS One, 6, 2011, e18644.
48. Wynant, N., Santos, D., Verdonck, R., Spit, J., Wielendaele, V.P., Broeck, J.V., Identification, functional characterization and phylogenetic analysis of double stranded RNA degrading enzymes present in the gut of the desert locust, Schistocerca gregaria. Insect biochem. Mol. Biol. 46 (2014), 1–8.
49. Wynant, N., Duressa, T.F., Santos, D., Duppen, J.V., Proost, P., Huybrechts, R., Broeck, J.V., Lipophorins can adhere to dsRNA, bacteria and fungi present in the hemolymph of the desert locust: a role as general scavenger for pathogens in the open body cavity. J. Insect Physiol. 64 (2014), 7–13.
50. Yang, J., Han, Z., Efficiency of different methods for dsRNA delivery in cotton bollworm (Helicoverpa armigera). J. Integr. Agr. 13 (2014), 115–123.
51. Yang, M.L., Wang, Y.L., Jiang, F., Song, T.Q., Wang, H.M., Liu, Q., Zhang, J., Zhang, J.Z., Kang, L., MiR-71 and miR-263 jointly regulate target genes chitin synthase and chitinase to control locust molting. PLoS Genet., 12, 2016, e1006257.
52. Yu, N., Christiaens, O., Liu, J., Niu, J., Cappelle, K., Caccia, S., Huvenne, H., Smagghe, G., Delivery of dsRNA for RNAi in insects: an overview and future directions. Insect Sci. 20 (2013), 4–14.
53. Zhang, J., Khan, S.A., Hasse, C., Ruf, S., Full crop protection from an insect pest by expression of long double-stranded RNAs in plastids. Science 347 (2015), 991–994.
54. Zhang, J.Z., Liu, X.J., Zhang, J.Q., Li, D.Q., Sun, Y., Guo, Y.P., Ma, E.B., Zhu, K.Y., Silencing of two alternative splicing-derived mRNA variants of chitin synthase 1 gene by RNAi is lethal to the oriental migratory locust, Locusta migratoria manilensis (Meyen). Insect biochem. Mol. Biol. 40 (2010), 824–833.
55. Zhang, X., Zhang, J., Zhu, K.Y., 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 (2010), 683–693.
56. Zhou, X.G., Wheeler, M.M., Oi, F.M., Scharf, M.E., RNA interference in the termite Reticulitermes flavipes through ingestion of double-stranded RNA. Insect biochem. Mol. Biol. 38 (2008), 805–815.
57. Zhu, F., Xu, J., Palli, R., Ferguson, J., Palli, S.R., Ingested RNA interference for managing the populations of the Colorado potato beetle, Leptinotarsa decemlineata. Pest Manag. Sci. 67 (2011), 175–182.
58. Zhu, K.Y., RNA interference: a powerful tool in entomological research and a novel approach for insect pest management. Insect Sci. 20 (2013), 1–3.