Toxin delivery by the coat protein of an aphid-vectored plant virus provides plant resistance to aphids

Nature Biotechnology

Volumn 32, Issue 1, 2014, Pages 102-105

  Bonning, Bryony C ^a   Pal, Narinder ^a   Liu, Sijun ^a   Wang, Zhaohui ^a   Sivakumar, S ^a   Dixon, Philip M ^b   King, Glenn F ^c   Miller, W Allen ^a  

^a IOWA STATE UNIVERSITY   (United States)

^b Iowa State University   (United States)

^c UNIVERSITY OF QUEENSLAND   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

ACYRTHOSIPHON PISUM; CHEMICAL INSECTICIDES; COAT PROTEINS; FUSION PROTEINS; PEST MANAGEMENT; PLANT RESISTANCE; PLANT VIRUS; TRANSGENIC ARABIDOPSIS;

AMINO ACIDS; PLANTS (BOTANY); TOXIC MATERIALS; VIRUSES;

RECOMBINANT PROTEINS;

COAT PROTEIN; GLUTATHIONE TRANSFERASE; GREEN FLUORESCENT PROTEIN; HYBRID PROTEIN; NEUROTOXIN;

APHID; ARABIDOPSIS; ARTICLE; CONTROLLED STUDY; HEMIPTERA; HEMOLYMPH; HOST RESISTANCE; LUTEOVIRUS; MEMBRANE; MUTATION; MYZUS PERSICAE; NONHUMAN; PEA APHID; PLANT VIRUS; PRIORITY JOURNAL; RHOPALOSIPHUM PADI; SOYBEAN APHID; VIRION;

ANIMALS; APHIDS; ARABIDOPSIS; CAPSID PROTEINS; DISEASE RESISTANCE; INSECTICIDES; LUTEOVIRUS; NEUROTOXINS; RECOMBINANT FUSION PROTEINS;

EID: 84892168590     PISSN: 10870156     EISSN: 15461696     Source Type: Journal    
DOI: 10.1038/nbt.2753     Document Type: Article

References (37)

1. Sanahuja, G., Banakar, R., Twyman, R.M., Capell, T. & Christou, P. Bacillus thuringiensis: a century of research, development and commercial applications. Plant Biotechnol. J. 9, 283-300 (2011).
2. Stokstad, E. & Grullon, G. Infographic: pesticide planet. Science 341, 730-731 (2013).
3. Chougule, N.P. & Bonning, B.C. Toxins for transgenic resistance to hemipteran pests. Toxins 4, 405-429 (2012).
4. Li, H., Chougule, N.P. & Bonning, B.C. Interaction of the Bacillus thuringiensis delta endotoxins Cry1Ac and Cry3Aa with the gut of the pea aphid, Acyrthosiphon pisum (Harris). J. Invertebr. Pathol. 107, 69-78 (2011).
5. Lu, Y. et al. Mirid bug outbreaks in multiple crops correlated with wide-scale adoption of Bt cotton in China. Science 328, 1151-1154 (2010).
6. Li, G. et al. Effects of transgenic Bt cotton on the population density, oviposition behavior, development, and reproduction of a nontarget pest, Adelphocoris suturalis (Hemiptera: Miridae). Environ. Entomol. 39, 1378-1387 (2010).
7. Schmidt, N.R. & Bonning, B.C. in Molecular Biology and Genetics of Lepidoptera (eds. M. Goldsmith & F. Marc) 307-319 (Taylor and Francis, Baton Rouge, FL, 2010).
8. King, G.F. & Hardy, M.C. Spider-venom peptides: structure, pharmacology, and potential for control of insect pests. Annu. Rev. Entomol. 58, 475-496 (2013).
9. Reavy, B. & Mayo, M.A. Persistent transmission of luteoviruses by aphids. Adv. Bot. Res. 36, 21-46 (2002).
10. Gray, S. & Gildow, F.E. Luteovirus-aphid interactions. Annu. Rev. Phytopathol. 41, 539-566 (2003).
11. Liu, S., Sivakumar, S., Wang, Z., Bonning, B.C. & Miller, W.A. The readthrough domain of Pea enation mosaic virus coat protein is not essential for virus stability in the hemolymph of the pea aphid. Arch. Virol. 154, 469-479 (2009).
12. Fletcher, J.I. et al. The structure of a novel insecticidal neurotoxin, ?-atracotoxin-HV1, from the venom of an Australian funnel web spider. Nat. Struct. Biol. 4, 559-566 (1997).
13. Pal, N., Yamamoto, T., King, G.F., Waine, C. & Bonning, B.C. Aphicidal efficacy of scorpion-and spider-derived neurotoxins. Toxicon 70, 114-122 (2013).
14. Sivakumar, S. et al. Baculovirus-expressed virus-like particles of Pea enation mosaic virus vary in size and encapsidate baculovirus mRNAs. Virus Res. 139, 54-63 (2009).
15. Lamb, J.W. et al. Assembly of virus-like particles in insect cells infected with a baculovirus containing a modified coat protein gene of potato leafroll luteovirus. J. Gen. Virol. 77, 1349-1358 (1996).
16. Locke, M. & Russell, V.W. in Microscopic Anatomy of Invertebrates, vol. 11B (eds. F.W. Harrison & M. Locke) 687-709 (Wiley-Liss Inc., New York, 1998).
17. Crossley, A.C. in Comprehensive Insect Physiology, Biochemistry, and Pharmacology (eds. G.A. Kerkut & L.I. Gilbert) 487-515 (Pergamon Press, New York, 1985).
18. Wang, X. et al. Structure-function studies of ?-atracotoxin, a potent antagonist of insect voltage-gated calcium channels. Eur. J. Biochem. 264, 488-494 (1999).
19. Tedford, H.W., Fletcher, J.I. & King, G.F. Functional significance of the beta hairpin in the insecticidal neurotoxin ?-atracotoxin-Hv1a. J. Biol. Chem. 276, 26568-26576 (2001).
20. Jeffers, L.A. & Michael Roe, R. The movement of proteins across the insect and tick digestive system. J. Insect Physiol. 54, 319-332 (2008).
21. Maiti, I.B., Oey, N., Dahlman, D.L. & Webb, B.A. Antibiosis-type resistance in transgenic plants expressing a teratocyte secretory peptide (TSP) gene from a hymenopteran endoparasite (Microplitis croceipes). Plant Biotechnol. J. 1, 209-219 (2003).
22. Tortiglione, C. et al. The expression in tobacco plants of Aedes aegypti Trypsin Modulating Oostatic Factor (Aea-TMOF) alters growth and development of the tobacco budworm, Heliothis virescens. Mol. Breed. 9, 159-169 (2002).
23. Gray, S.M. & Banerjee, N. Mechanisms of arthropod transmission of plant and animal viruses. Microbiol. Mol. Biol. Rev. 63, 128-148 (1999).
24. Fitches, E.C., Pyati, P., King, G.F. & Gatehouse, J.A. Fusion to snowdrop lectin magnifies the oral activity of insecticidal ?-hexatoxin-Hv1a peptide by enabling its delivery to the central nervous system. PLoS ONE 7, e39389 (2012).
25. Fitches, E.C. et al. Insecticidal activity of scorpion toxin (ButaIT) and snowdrop lectin (GNA) containing fusion proteins towards pest species of different orders. Pest Manag. Sci. 66, 74-83 (2010).
26. Bonning, B.C. & Chougule, N.P. Delivery of intrahemocoelic peptides for insect pest management. Trends Biotechnol. (in the press) (2013).
27. Pennacchio, F., Giordana, B. & Rao, R. in Parasitoid Viruses: Symbionts and Pathogens (eds. N.E. Beckage & J.M. Drezen) 269-283 (Academic Press, San Diego, 2012).
28. Demler, S.A., Rucker-Feeney, D.G., Skaf, J.S. & deZoeten, G.A. Expression and suppression of circulative aphid transmission in pea enation mosaic virus. J. Gen. Virol. 78, 511-523 (1997).
29. Fukatsu, T., Tsuchida, T., Nikoh, N. & Koga, R. Spiroplasma symbiont of the pea aphid, Acyrthosiphon pisum (Insecta: Homoptera). Appl. Environ. Microbiol. 67, 1284-1291 (2001).
30. Tedford, H.W. et al. Scanning mutagenesis of ?-atracotoxin-Hv1a reveals a spatially restricted epitope that confers selective activity against insect calcium channels. J. Biol. Chem. 279, 44133-44140 (2004).
31. Febvay, G., Delobel, B. & Rahbe, Y. Influence of the amino-acid balance on the improvement of an artificial diet for a biotype of Acyrthosiphon pisum (Homoptera, Aphididae). Can. J. Zool. 66, 2449-2453 (1988).
32. Liu, S., Bonning, B.C. & Miller, W.A. A simple wax-embedding method for isolation of aphid hemolymph for detection of luteoviruses in the hemocoel. J. Virol. Methods 132, 174-180 (2006).
33. Clough, S.J. & Bent, A.F. Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J. 16, 735-743 (1998).
34. Collins, T.J. ImageJ for microscopy. Biotechniques 43, S25-S30 (2007).
35. Hughes, P.R., Van Beek, N.A.M. & Wood, H.A. A modified droplet feeding method for rapid assay of Bacillus thuringiensis and baculoviruses in noctuid larvae. J. Invertebr. Pathol. 48, 187-192 (1986).
36. SAS Institute. SAS/STAT(R) 9.3 User's Guide (SAS Institute Inc., Cary NC, 2013).
37. LeOra-Software POLO-PC. A User's Guide to Probit and Logit Analysis (LeOra Software, Berkeley, California, 1987).