Hostname: page-component-586b7cd67f-2brh9 Total loading time: 0 Render date: 2024-11-27T23:05:51.957Z Has data issue: false hasContentIssue false
  • English
  • Français

The effect of silencing arginine kinase by RNAi on the larval development of Helicoverpa armigera

Published online by Cambridge University Press:  03 July 2015

X.-L. Qi ,
X.-F. Su ,
G.-Q. Lu ,
C.-X. Liu ,
G.-M. Liang  and
H.-M. Cheng
X.-L. Qi
Affiliation:
Biotechnology Research Institute, Chinese Academy of Agricultural Sciences, Beijing 100081, China
X.-F. Su
Affiliation:
Biotechnology Research Institute, Chinese Academy of Agricultural Sciences, Beijing 100081, China
G.-Q. Lu
Affiliation:
Biotechnology Research Institute, Chinese Academy of Agricultural Sciences, Beijing 100081, China
C.-X. Liu
Affiliation:
State Key Laboratory for Biology of Plant Diseases and Insect Pests, Institute of Plant Protection, Chinese Academy of Agricultural Sciences, Beijing 100193, China
G.-M. Liang
Affiliation:
State Key Laboratory for Biology of Plant Diseases and Insect Pests, Institute of Plant Protection, Chinese Academy of Agricultural Sciences, Beijing 100193, China
H.-M. Cheng*
Affiliation:
Biotechnology Research Institute, Chinese Academy of Agricultural Sciences, Beijing 100081, China
*
*Author for correspondence Phone: +86-10-82106125 Fax: +86-10-82106125 E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

Arginine kinase (AK) is an important regulation factor of energy metabolism in invertebrate. An arginine kinase gene, named HaAK, was identified to be differentially expressed between Cry1Ac-susceptible (96S) and Cry1Ac-resistant (Bt-R) Helicoverpa armigera larvae using cDNA-amplification fragment length polymorphism analysis. The full-length open reading frame sequence of HaAK gene with 1068 bp was isolated from H. armigera. Quantitative reverse transcription polymerase chain reaction assay revealed that HaAK gene is specifically expressed in multiple tissues and at larval developmental stages. The peak expression level of HaAK was detected in the midgut of the fifth-instar larvae. Moreover, the expression of HaAK was obviously down-regulated in Bt-R larvae. We further constructed a dsRNA vector directly targeting HaAK and employed RNAi technology to control the larvae. The feeding bioassays showed that minute quantities of dsRNA could greatly increase the larval mortality and delay the larval pupation. Silencing of HaAK significantly retarded the larval development, indicating that HaAK is a potential target for RNA interference-based pest management.

Keywords

Helicoverpa armigeraarginine kinasegenes expressionRNA interferencepest control
Type
Research Papers
Information
Bulletin of Entomological Research , Volume 105 , Issue 5 , October 2015 , pp. 555 - 565
Check for updates
Copyright
Copyright © Cambridge University Press 2015 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Adeyemi, O.S. & Whiteley, C.G. (2014) Interaction of metal nanoparticles with recombinant arginine kinase from Trypanosoma brucei: thermodynamic and spectrofluorimetric evaluation. Biochimica et Biophysica Acta 1840, 701–706.Google Scholar
Ahmad, S., Ansari, M.S. & Muslim, M. (2015) Toxic effects of neem based insecticides on the fitness of Helicoverpa armigera (Hübner). Crop Protection 68, 72–78.Google Scholar
Amann, R.I., Krumholz, L. & Stahl, D.A. (1990) Fluorescent-oligonucleotide probing of whole cells for determinative, phylogenetic, and environmental studies in microbiology. Journal of Bacteriology 172, 762–770.Google Scholar
Apone, F., Ruggiero, A., Tortora, A., Tito, A., Grimaldi, M.R., Arciello, S., Andrenacci, D., Lelio, I.D. & Colucci, G. (2014) Targeting the diuretic hormone receptor to control the cotton leafworm, Spodoptera littoralis . Journal of Insect Science 14, 1–16.Google Scholar
Arockiaraj, J., Vanaraja, P., Easwvaran, S., Singh, A., Alinejaid, T., Othman, R.Y. & Bhassu, S. (2011) Gene profiling and characterization of arginine kinase-1 (MrAK-1) from freshwater giant prawn (Macrobrachium rosenbergii). Fish Shellfish Immunology 31, 81–89.Google Scholar
Belles, X. (2010) Beyond Drosophila: RNAi in vivo and functional genomics in insects. Annual Review of Entomology 55, 111–128.CrossRefGoogle ScholarPubMed
Bradford, M.M. (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein–dye binding. Analytical Biochemistry 72, 248–254.Google Scholar
Cao, G., Feng, H., Guo, F., Wu, K., Li, X., Liang, G. & Desneux, N. (2014) Quantitative analysis of fitness costs associated with the development of resistance to the Bt toxin Cry1Ac in Helicoverpa armigera . Scientific Reports 4, 5629.Google Scholar
Chen, J., Zhang, D., Yao, Q., Zhang, J., Dong, X., Tian, H., Chen, J. & Zhang, W. (2010) Feeding-based RNA interference of a trehalose phosphate synthase gene in the brown planthopper, Nilaparvata lugens . Insect Molecular Biology 19, 777–786.CrossRefGoogle ScholarPubMed
Chen, W. & Xu, W.H. (2014) Wnt/β-catenin signaling regulates Helicoverpa armigera pupal development by up-regulating c-Myc and AP-4. Insect Biochemistry and Molecular Biology 53, 44–53.Google Scholar
Chomczynski, P. & Sacchi, N. (1987) Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Analytical Biochemistry 162, 156–159.CrossRefGoogle ScholarPubMed
Christianson, A.M., King, D.L., Hatzivassiliou, E., Casas, J.E., Hallenbeck, P.L., Nikodem, V.M., Mitsialis, S.A. & Kafatos, F.C. (1992) DNA binding and heteromerization of the Drosophila transcription factor chorion factor 1/ultraspiracle. Proceedings of The National Academy of Sciences of the United States of America 89, 11503–11507.Google Scholar
Citelli, M., Lara, F.A., Vaz, I.d.S. Jr. & Oliveira, P.L. (2007) Oxidative stress impairs heme detoxification in the midgut of the cattle tick, Rhipicephalus (Boophilus) microplus . Molecular and Biochemical Parasitology 151, 81–88.Google Scholar
Dawson, N.J. & Storey, K.B. (2011) Regulation of tail muscle arginine kinase by reversible phosphorylation in an anoxia-tolerant crayfish. Journal of Comparative Physiology B 181, 851–859.Google Scholar
Ellington, W.R. (2001) Evolution and physiological roles of phosphagen systems. Annual Review of Physiology 63, 289–325.Google Scholar
Fernandes, M., Xiao, H. & Lis, J.T. (1994) Fine structure analyses of the Drosophila and Saccharomyces heat shock factor–heat shock element interactions. Nucleic Acids Research 22, 167–173.Google Scholar
Gassmann, A.J., Carrière, Y. & Tabashnik, B.E. (2008) Fitness costs of insect resistance to Bacillus thuringiensis . Annual Review of Entomology 54, 147–163.Google Scholar
Guo, H., Lu, G., Su, X., Liang, G., Liu, C. & Cheng, H. (2014) Up-regulated death-associated LIM-only protein contributes to fitness costs of Bacillus thuringiensis Cry1Ac resistance in Helicoverpa armigera . Journal of Insect Physiology 60, 145–152.Google Scholar
Guo, Q., Chen, B. & Wang, X. (2004) Evidence for proximal cysteine and lysine residues at or near the active site of arginine kinase of Stichopus japonicus . Biochemistry (Mosc) 69, 1336–1343.Google Scholar
Hacker, U., Kaufmann, E., Hartmann, C., Jurgens, G., Knochel, W. & Jackle, H. (1995) The Drosophila fork head domain protein crocodile is required for the establishment of head structures. EMBO Journal 14, 5306–5317.CrossRefGoogle ScholarPubMed
Jamal, F., Singh, D. & Pandey, P.K. (2014) Negative effects of a nonhost proteinase inhibitor of ~19.8 kDa from Madhuca indica seeds on developmental physiology of Helicoverpa armigera (Hubner). Biomed Research International, doi: 10.1155/2014/202398.CrossRefGoogle ScholarPubMed
Kranthi, K., Jadhav, D., Kranthi, S., Wanjari, R., Ali, S. & Russell, D. (2002) Insecticide resistance in five major insect pests of cotton in India. Crop Protection 21, 449–460.Google Scholar
Kulathunga, D.G., Wickramasinghe, S., Rajapakse, R.P., Yatawara, L., Jayaweera, W.R. & Agatsuma, T. (2012) Immunolocalization of arginine kinase (AK) in Toxocara canis, Toxocara vitulorum, and Ascaris lumbricoides . Parasitology Research 111, 663–671.CrossRefGoogle Scholar
Lauzon, C.R., Potter, S.E. & Prokopy, R.J. (2003) Degradation and detoxification of the dihydrochalcone phloridzin by Enterobacter agglomerans, a bacterium associated with the apple pest, Rhagoletis pomonella (Walsh)(Diptera: Tephritidae). Environmental Entomology 32, 953–962.Google Scholar
Li, F., Wu, Q.Y. & Wang, X.Y. (2013) The amino acid residue L113 is involved in arginine kinase activity and structural stability. International Journal of Biological Macromolecules 52, 198–205.Google Scholar
Liang, G., Tan, W. & Guo, Y. (2000) Studies on the resistance screening and cross-resistance of cotton bollworm to Bacillus thuringiensis (Berliner). Scientia Agricultura Sinica 33, 46–53.Google Scholar
Liang, G., Chen, W. & Liu, T. (2003) Effects of three neem-based insecticides on diamondback moth (Lepidoptera: Plutellidae). Crop Protection 22, 333–340.Google Scholar
Liang, G.M., Wu, K.M., Yu, H.K., Li, K.K., Feng, X. & Guo, Y.Y. (2008) Changes of inheritance mode and fitness in Helicoverpa armigera (Hubner) (Lepidoptera: Noctuidae) along with its resistance evolution to Cry1Ac toxin. Journal of Invertebrate Pathology 97, 142–149.CrossRefGoogle ScholarPubMed
Lipskaya, T.Y. (2001) The physiological role of the creatine kinase system: evolution of views. Biochemistry (Mosc) 66, 115–129.Google Scholar
Liu, F., Wang, X.D., Zhao, Y.Y., Li, Y.J., Liu, Y.C. & Sun, J. (2015) Silencing the HaAK gene by transgenic plant-mediated RNAi impairs larval growth of Helicoverpa armigera . International Journal of Biological Sciences 11, 67–74.Google Scholar
Macdonald, P.M. & Struhl, G. (1988) cis-acting sequences responsible for anterior localization of bicoid mRNA in Drosophila embryos. Nature 336, 595–598.Google Scholar
Mao, Y., Cai, W., Wang, J., Hong, G., Tao, X., Wang, L., Huang, Y. & Chen, X. (2007) Silencing a cotton bollworm P450 monooxygenase gene by plant-mediated RNAi impairs larval tolerance of gossypol. Nature Biotechnology 25, 1307–1313.Google Scholar
Pereira, C.A. (2014) Arginine kinase: a potential pharmacological target in trypanosomiasis. Infect Disord Drug Targets 14, 30–36.Google Scholar
Pereira, C.A., Alonso, G.D., Paveto, M.C., Flawiá, M.M. & Torres, H.N. (1999) L-Arginine uptake and L-phosphoarginine synthesis in Trypanosoma cruzi . Journal of Eukaryotic Microbiology 46, 566–570.Google Scholar
Perkins, K.K., Dailey, G.M. & Tjian, R. (1988) In vitro analysis of the Antennapedia P2 promoter: identification of a new Drosophila transcription factor. Genes Development 2, 1615–1626.CrossRefGoogle ScholarPubMed
Pinkel, D., Straume, T. & Gray, J. (1986) Cytogenetic analysis using quantitative, high-sensitivity, fluorescence hybridization. Proceedings of the National Academy of Sciences of the United States of America 83, 2934–2938.CrossRefGoogle ScholarPubMed
Quan, G.X., Kanda, T. & Tamura, T. (2002) Induction of the white egg 3 mutant phenotype by injection of the double-stranded RNA of the silkworm white gene. Insect Molecular Biology 11, 217–222.Google Scholar
Read, D. & Manley, J.L. (1992) Alternatively spliced transcripts of the Drosophila tramtrack gene encode zinc finger proteins with distinct DNA binding specificities. EMBO Journal 11, 1035–1044.CrossRefGoogle ScholarPubMed
Regulski, M., McGinnis, N., Chadwick, R. & McGinnis, W. (1987) Developmental and molecular analysis of deformed; a homeotic gene controlling Drosophila head development. EMBO Journal 6, 767–777.Google Scholar
Seals, J.D. & Grossman, S.H. (1988) Purification and characterization of arginine kinase from the sea cucumber Caudina arenicola . Comparative Biochemistry and Physiology Part B: Comparative Biochemistry 89, 701–707.Google Scholar
Soberon, M., Gill, S. & Bravo, A. (2009) Signaling versus punching hole: how do Bacillus thuringiensis toxins kill insect midgut cells? Cellular and Molecular Life Sciences 66, 1337–1349.Google Scholar
Stanojevic, D., Hoey, T. & Levine, M. (1989) Sequence-specific DNA-binding activities of the gap proteins encoded by hunchback and Kruppel in Drosophila . Nature 341, 331–335.CrossRefGoogle Scholar
Tabashnik, B.E. (1994) Evolution of resistance to Bacillus thuringiensis . Annual Review of Entomology 39, 47–79.Google Scholar
Tabashnik, B.E., Brévault, T. & Carrière, Y. (2013) Insect resistance to Bt crops: lessons from the first billion acres. Nature Biotechnology 31, 510–521.CrossRefGoogle ScholarPubMed
Tay, W.T., Soria, M.F., Walsh, T., Thomazoni, D., Silvie, P., Behere, G.T., Anderson, C. & Downes, S. (2013) A brave new world for an old world pest: Helicoverpa armigera (Lepidoptera: Noctuidae) in Brazil. PLoS ONE 8, e80134.Google Scholar
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, e6225.Google Scholar
Timmons, L. & Fire, A. (1998) Specific interference by ingested dsRNA. Nature 395, 854 Google Scholar
Timmons, L., Court, D.L. & Fire, A. (2001) Ingestion of bacterially expressed dsRNAs can produce specific and potent genetic interference in Caenorhabditis elegans . Gene 263, 103–112.CrossRefGoogle ScholarPubMed
Uda, K. & Suzuki, T. (2004) Role of amino acid residues on the GS region of Stichopus arginine kinase and Danio creatine kinase. Protein Journal 23, 53–64.Google Scholar
Van Doren, M., Bailey, A.M., Esnayra, J., Ede, K. & Posakony, J.W. (1994) Negative regulation of proneural gene activity: hairy is a direct transcriptional repressor of achaete. Genes Development 8, 2729–2742.Google Scholar
Voncken, F., Gao, F., Wadforth, C., Harley, M. & Colasante, C. (2013) The phosphoarginine energy-buffering system of Trypanosoma brucei involves multiple arginine kinase isoforms with different subcellular locations. PLoS ONE 8, e65908.Google Scholar
von Kalm, L., Crossgrove, K., Von Seggern, D., Guild, G.M. & Beckendorf, S.K. (1994) The broad-complex directly controls a tissue-specific response to the steroid hormone ecdysone at the onset of Drosophila metamorphosis . EMBO Journal 13, 3505–3516.Google Scholar
Wang, W.D., Wang, J.S., Shi, Y.L., Zhang, X.C., Pan, J.C. & Zou, G.L. (2013) Mutation of residue arginine 330 of arginine kinase results in the generation of the oxidized form more susceptible. International Journal of Biological Macromolecules 54, 238–243.Google Scholar
Wu, Q.Y., Guo, H.Y., Geng, H.L., Ru, B.M., Cao, J., Chen, C., Zeng, L.Y., Wang, X.Y., Li, F. & Xu, K.L. (2014) T273 plays an important role in the activity and structural stability of arginine kinase. International Journal of Biological Macromolecules 63, 21–28.Google Scholar
Xiong, Y., Zeng, H., Zhang, Y., Xu, D. & Qiu, D. (2013) Silencing the HaHR3 gene by transgenic plant-mediated RNAi to disrupt Helicoverpa armigera development. International Journal of Biological Macromolecules 9, 370–381.Google Scholar
Xu, Z.B., Zou, X.P., Zhang, N., Feng, Q.L. & Zheng, S.C. (2014) Detoxification of insecticides, allechemicals and heavy metals by glutathione S-transferase SlGSTE1 in the gut of Spodoptera litura . Insect Science 00, 1–9, doi: 10.1111/1744-7917.12142.Google Scholar
Yang, J. & Han, Z.j. (2014) Efficiency of different methods for dsRNA delivery in cotton bollworm (Helicoverpa armigera). Journal of Integrative Agriculture 13, 115–123.Google Scholar
Yao, C.L., Ji, P.F., Kong, P., Wang, Z.Y. & Xiang, J.H. (2009) Arginine kinase from Litopenaeus vannamei: cloning, expression and catalytic properties. Fish Shellfish Immunology 26, 553–558.Google Scholar
Yu, S., Liu, H. & Luo, L. (2007) Analysis of relative gene expression using different real-time quantitative PCR. Acta Agronomica Sinica 33, 1214–1218.Google Scholar
Zhang, S., Cheng, H., Gao, Y., Wang, G., Liang, G. & Wu, K. (2009) Mutation of an aminopeptidase N gene is associated with Helicoverpa armigera resistance to Bacillus thuringiensis Cry1Ac toxin. Insect Biochemistry and Molecular Biology 39, 421–429.Google Scholar
Zhao, X.F., Wang, J.X., Xu, X.L., Li, Z.M. & Kang, C.J. (2004) Molecular cloning and expression patterns of the molt-regulating transcription factor HHR3 from Helicoverpa armigera . Insect Molecular Biology 13, 407–412.Google Scholar
Zhao, Y., Yang, G., Wang-Pruski, G. & You, M. (2008) Phyllotreta striolata (Coleoptera: Chrysomelidae): Arginine kinase cloning and RNAi-based pest control. European Journal of Entomology 105, 815–812.Google Scholar
Supplementary material: Image

Qi supplementary material S1

Figure

Download Qi supplementary material S1(Image)
Image 756.9 KB