A virulence factor encoded by a polydnavirus confers tolerance to transgenic tobacco plants against lepidopteran larvae, by impairing nutrient absorption
A virulence factor encoded by a polydnavirus confers tolerance to transgenic tobacco plants against lepidopteran larvae, by impairing nutrient absorption(136 visite) Di Lelio I, Caccia S, Coppola M, Buonanno M, Di Prisco G, Varricchio P, Franzetti E, Corrado G, Monti SM, Rao R, Casartelli M, Pennacchio F
PLOS ONE (ISSN: 1932-6203), 2014 Dec 1; 9(12): N/D-N/D.
Tipo di articolo: Journal Article, Abstract, Conference,
Impact factor: 3.234, Impact factor a 5 anni: 3.702
*** IBB - CNR *** Dipartimento di Agraria, Università di Napoli Federico IIPortici, Italy Istituto di Biostrutture e Bioimmagini (IBB), CNRNapoli, Italy Dipartimento di Scienze e Tecnologie Ambientali, Biologiche e Farmaceutiche, Seconda Università di NapoliCaserta, Italy Dipartimento di Bioscienze, Università degli Studi di MilanoMilano, Italy
Riferimenti:
Casida, J.E., Quistad, G.B., Golden age of insecticide research: Past, present, or future? (1998) Annu Rev Entomol, 43, pp. 1-1
Tomlin, C.D.S., (2009) The Pesticide Manual: AWorld Compendium, 1457p. , Hampshire, UK: Br. CropProt. Counc. 15th ed
Casida, J.E., Durkin, K.A., Neuroactive insecticides: Targets, selectivity, resistance, and secondary effects (2013) Annu Rev Entomol, 58, pp. 99-117
Horowitz, A.R., Ishaaya, I., (2004) Insect Pest Management, p. 344. , Springer-Verlag, Berlin
Norris, R.F., Caswell-Chen, E.P., Kogan, M., (2003) Concepts in Integrated Pest Management, p. 586. , Prentice Hall, Upper Saddle River, New Jersey
Ehler, L.E., Integrated pest management (IPM): Definition, historical development and implementation, and the other IPM (2006) Pest Manag Sci, 62, pp. 787-789
Brewer, M.J., Goodell, P.B., Approaches and incentives to implement integrated pest management that addresses regional and environmental issues (2012) Annu Rev Entomol, 57, pp. 41-59
Bale, J.S., Van Lenteren, J.C., Bigler, F., Biological control and sustainable food production (2008) Philos T R Soc B, 63, pp. 761-776
Roh, J.Y., Choi, J.Y., Li, M.S., Jin, B.R., Je, Y.H., Bacillus thuringiensis as a specific, safe, and effective tool for insect pest control (2007) J Microbiol Biotechnol, 17, pp. 547-559
Sparks, T.C., Crousel, G.D., Durst, G., Natural products as insecticides: The biology, biochemistry and quantitative structure-activity relationships of spinosyns and spinosoids (2001) Pest Manag Sci, 57, pp. 896-905
Kirst, H.A., The spinosyn family of insecticides: Realizing the potential of natural products research (2010) J Antibiot, 63, pp. 101-111
Miresmailli, S., Isman, M., Botanical insecticides inspired by plant-herbivore chemical interactions (2014) Trends Plant Sci, 19, pp. 29-35
Smith, J.J., Herzig, V., King, G.F., Alewood, P.F., The insecticidal potential of venom peptides (2013) Cell Mol Life Sci, 70, pp. 3665-3693
Quicke, D.L.J., (1997) Parasitic Wasps, , London: Chapman & Hall
Whitfield, J.B., Phylogenetic insights into the evolution of parasitism in Hymenoptera (2003) Adv Parasitol, 54, pp. 69-100
Pennacchio, F., Strand, M.R., Evolution of developmental strategies in parasitic Hymenoptera (2006) Annu Rev Entomol, 51, pp. 233-258
Kroemer, J.A., Webb, B.A., Polydnavirus genes and genomes: Emerging gene families and new insights into polydnavirus replication (2004) Annu Rev Entomol, 49, pp. 431-456
Webb, B.A., Strand, M.R., The Biology and Genomics of Polydnaviruses (2005) Comprehensive Molecular Insect Science, 6, pp. 323-360. , (L. I. Gilbert, K. Iatrou, S. S. Gill, Eds). Elsevier, San Diego
Strand, M.R., Polydnavirus gene products that interact with the host immune system (2012) Parasitoid Viruses: Symbionts and Pathogens, pp. 149-161. , Edited by BeckageNE, DrezenJ-M. Elsevier
Maiti, I.B., Dey, N., Dahlman, D.L., Webb, B.A., Antibiosis-type resistance in transgenic plants expressing teratocyte secretory peptide (TSP) gene from hymenopteran endoparasite (Microplitis croceipes) (2003) Plant Biotechnol, 1, pp. 209-219
Gill, T.A., Fath-Goodin, A., Maiti, I.B., Webb, B.A., Potential uses of cys-motif and other polydnavirus genes in biotechnology (2006) Adv Virus Res, 68, pp. 393-426
Pennacchio, F., Giordana, B., Rao, R., Applications of parasitoid virus and venom research in agriculture (2012) Parasitoid Viruses: Symbionts and Pathogens, pp. 269-283. , Edited by BeckageNE, DrezenJ-M. Elsevier
Falabella, P., Riviello, L., Caccialupi, P., Rossodivita, T., Valente, M.T., A gammaglutamyltranspeptidase of Aphidius ervi venom induces apoptosis in the ovaries of host aphids (2007) Insect Biochem Mol Biol, 37, pp. 453-465
Duchi, S., Cavaliere, V., Fagnocchi, L., Grimaldi, M.R., Falabella, P., The impact on microtubule network of a bracovirus IkB-like Protein (2010) Cell Mol Life Sci, 67, pp. 1699-1712
Valzania, L., Romani, P., Tian, L., Li, S., Cavaliere, V., A polydnavirus ANK protein acts as virulence factor by disrupting the function of prothoracic gland steroidogenic cells (2014) PLoS ONE, 9 (4), p. e95104
Danna, K.J., Production of cellulases in plants for biomass conversion (2001) Regulation of Phytochemicals by Molecular Techniques, pp. 206-223. , Eds, JA Saunders, , BF Matthews
John Romeo, Elsevier publisher
Tortiglione, C., Fogliano, V., Ferracane, R., Fanti, P., Pennacchio, F., An insect peptide engineered into the tomato prosystemin gene is released in tobacco transgenic plants and exerts biological activity (2003) Plant Mol Biol, 53, pp. 891-902
Corrado, G., Scarpetta, M., Alioto, D., Di Maro, A., Polito, L., Inducible antiviral activity and rapid production of the Ribosome-Inactivating Protein I from Phytolacca heterotepala in tobacco (2008) Plant Science, 174, pp. 467-474
Fulton, T.M., Chunwongse, J., Tanksley, S.D., Microprep protocol for extraction of DNA from tomato and other herbaceous plants (1995) Plant Mol Biol Rep, 13, pp. 207-209
Shewmaker, C.K., Ridge, N.P., Pokalsky, A.R., Rose, R.E., Hiatt, W.R., Nucleotide sequence of an EF-1 alpha genomic clone from tomato (1190) Nucleic Acids Res, 14, p. 4276
Bradford, M.M., A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding (1976) Anal Biochem, 72, pp. 248-254
Di Lelio, I., Varricchio, P., Di Prisco, G., Marinelli, A., Lasco, V., Functional analysis of an immune gene of Spodoptera littoralis by RNAi (2014) J Insect Physiol, 64, pp. 90-97
Tornatore, L., Marasco, D., Dathan, N., Vitale, R.M., Benedetti, E., Gadd45 beta forms a homodimeric complex that binds tightly to MKK7 (2008) J Mol Biol, 378, pp. 97-111
Giordana, B., Sacchi, V.F., Hanozet, G.M., Intestinal amino acid absorption in lepidopteran larvae (1982) Biochim Biophys Acta, 692, pp. 81-88
Hilpert, K., Hansen, G., Wessner, H., Küttner, G., Welfle, K., Anti c-myc antibody 9E10: Epitope key position and variability characterized using peptide spot synthesis on cellulose (2001) Protein Eng, 14, pp. 803-806
Toyooka, K., Okamoto, T., Minamikawa, T., Mass transport of proform of aKDEL-tailed cysteine proteinase (SH-EP) to protein storage vacuoles by endoplasmic retriculum-derived vesicle is involved in protein mobilization in germinating seeds (2000) J Cell Biol, 148, pp. 453-464
Dorak, T., (2006) Real-time PCR, , Edited by Taylor and Francis Group
Whitmore, L., Wallace, B.A., DICHROWEB: An online server for protein secondary structure analyses from circular dichroism spectroscopic data (2004) Nucleic Acids Res, 32, pp. 668-673
Schmitz, K.S., (1990) Dynamic Light Scattering by Macromolecules, , Academic Press, Boston
Parenti, P., Giordana, B., Sacchi, V.F., Hanozet, G.M., Guerritore, A., Metabolic activity related to the potassium pump in the midgut of Bombyx mori larvae (1985) J Exp Biol, 116, pp. 69-78
Casartelli, M., Leonardi, M.G., Fiandra, L., Parenti, P., Giordana, B., Multiple transport pathways for dibasic amino acids in the larval midgut of the silkworm Bombyx mori (2001) Insect Biochem Mol Biol, 31, pp. 621-632
Leonardi, M.G., Casartelli, M., Parenti, P., Giordana, B., Evidence for a low-affinity, high-capacity uniport for amino acids in Bombyx mori larval midgut (1998) Am J Physiol, 274, pp. R1372-R1375
Leonardi, M.G., Caccia, S., Gonzalez-Cabrera, J., Ferré, J., Giordana, B., Leucine transport is affected by Bacillus thuringiensis Cry1 toxins in brush border membrane vesicles from Ostrinia nubilalis Hb (Lepidoptera: Pyralidae) and Sesamia nonagrioides Lefebvre (Lepidoptera: Noctuidae) midgut (2007) J Membrane Biol, 214, pp. 157-164
Thoetkiattikul, H., Beck, M.H., Strand, M.R., Inhibitor kappaB-like proteins from a polydnavirus inhibit NF-kappaB activation and suppress the insect immune response (2005) Proc Natl Acad Sci USA, 32, pp. 11426-11431
Bitra, K., Suderman, R.J., Strand, M.R., Polydnavirus Ank proteins bind NF-kB homodimers and inhibit processing of Relish (2012) PLoS Pathog, 8 (5), p. e1002722. , 2012
Li, J., Mahajan, J., Tsai, M.-D., Ankyrin repeat: A unique motif mediating protein-protein interactions (2006) Biochemistry, 45, pp. 15168-15178
Campioni, S., Mossuto, M.F., Torrassa, S., Calloni, G., De Laureto, P.P., Conformational properties of the aggregation precursor state of HypF-N (2008) J Mol Biol, 379, pp. 554-567
Caccia, S., Van Damme, E.J., De Vos, W.H., Smagghe, G., Mechanism of entomotoxicity of the plant lectin from Hippeastrum hybrid (Amaryllis) in Spodoptera littoralis larvae (2012) J Insect Physiol, 58, pp. 1177-1183
Li, H.M., Sun, L., Mittapalli, O., Muir, W.M., Xie, J., Transcriptional signatures in response to wheat germ agglutinin and starvation in Drosophila melanogaster larval midgut (2009) Insect Mol Biol, 18, pp. 21-31
Vandenborre, G., Smagghe, G., Van Damme, E.J.M., Plant lectins as defense proteins against phytophagous insects (2011) Phytochemistry, 72, pp. 1538-1550
Casida, J. E., Quistad, G. B., Golden age of insecticide research: Past, present, or future? (1998) Annu Rev Entomol, 43, pp. 1-1
Tomlin, C. D. S., (2009) The Pesticide Manual: AWorld Compendium, 1457p. , Hampshire, UK: Br. CropProt. Counc. 15th ed
Casida, J. E., Durkin, K. A., Neuroactive insecticides: Targets, selectivity, resistance, and secondary effects (2013) Annu Rev Entomol, 58, pp. 99-117
Horowitz, A. R., Ishaaya, I., (2004) Insect Pest Management, p. 344. , Springer-Verlag, Berlin
Norris, R. F., Caswell-Chen, E. P., Kogan, M., (2003) Concepts in Integrated Pest Management, p. 586. , Prentice Hall, Upper Saddle River, New Jersey
Ehler, L. E., Integrated pest management (IPM): Definition, historical development and implementation, and the other IPM (2006) Pest Manag Sci, 62, pp. 787-789
Brewer, M. J., Goodell, P. B., Approaches and incentives to implement integrated pest management that addresses regional and environmental issues (2012) Annu Rev Entomol, 57, pp. 41-59
Bale, J. S., Van Lenteren, J. C., Bigler, F., Biological control and sustainable food production (2008) Philos T R Soc B, 63, pp. 761-776
Roh, J. Y., Choi, J. Y., Li, M. S., Jin, B. R., Je, Y. H., Bacillus thuringiensis as a specific, safe, and effective tool for insect pest control (2007) J Microbiol Biotechnol, 17, pp. 547-559
Sparks, T. C., Crousel, G. D., Durst, G., Natural products as insecticides: The biology, biochemistry and quantitative structure-activity relationships of spinosyns and spinosoids (2001) Pest Manag Sci, 57, pp. 896-905
Kirst, H. A., The spinosyn family of insecticides: Realizing the potential of natural products research (2010) J Antibiot, 63, pp. 101-111
Smith, J. J., Herzig, V., King, G. F., Alewood, P. F., The insecticidal potential of venom peptides (2013) Cell Mol Life Sci, 70, pp. 3665-3693
Quicke, D. L. J., (1997) Parasitic Wasps, , London: Chapman & Hall
Whitfield, J. B., Phylogenetic insights into the evolution of parasitism in Hymenoptera (2003) Adv Parasitol, 54, pp. 69-100
Kroemer, J. A., Webb, B. A., Polydnavirus genes and genomes: Emerging gene families and new insights into polydnavirus replication (2004) Annu Rev Entomol, 49, pp. 431-456
Webb, B. A., Strand, M. R., The Biology and Genomics of Polydnaviruses (2005) Comprehensive Molecular Insect Science, 6, pp. 323-360. , (L. I. Gilbert, K. Iatrou, S. S. Gill, Eds). Elsevier, San Diego
Strand, M. R., Polydnavirus gene products that interact with the host immune system (2012) Parasitoid Viruses: Symbionts and Pathogens, pp. 149-161. , Edited by BeckageNE, DrezenJ-M. Elsevier
Maiti, I. B., Dey, N., Dahlman, D. L., Webb, B. A., Antibiosis-type resistance in transgenic plants expressing teratocyte secretory peptide (TSP) gene from hymenopteran endoparasite (Microplitis croceipes) (2003) Plant Biotechnol, 1, pp. 209-219
Gill, T. A., Fath-Goodin, A., Maiti, I. B., Webb, B. A., Potential uses of cys-motif and other polydnavirus genes in biotechnology (2006) Adv Virus Res, 68, pp. 393-426
Danna, K. J., Production of cellulases in plants for biomass conversion (2001) Regulation of Phytochemicals by Molecular Techniques, pp. 206-223. , Eds, JA Saunders, , BF Matthews
Fulton, T. M., Chunwongse, J., Tanksley, S. D., Microprep protocol for extraction of DNA from tomato and other herbaceous plants (1995) Plant Mol Biol Rep, 13, pp. 207-209
Shewmaker, C. K., Ridge, N. P., Pokalsky, A. R., Rose, R. E., Hiatt, W. R., Nucleotide sequence of an EF-1 alpha genomic clone from tomato (1190) Nucleic Acids Res, 14, p. 4276
Bradford, M. M., A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding (1976) Anal Biochem, 72, pp. 248-254
Schmitz, K. S., (1990) Dynamic Light Scattering by Macromolecules, , Academic Press, Boston
Leonardi, M. G., Casartelli, M., Parenti, P., Giordana, B., Evidence for a low-affinity, high-capacity uniport for amino acids in Bombyx mori larval midgut (1998) Am J Physiol, 274, pp. R1372-R1375
Leonardi, M. G., Caccia, S., Gonzalez-Cabrera, J., Ferr, J., Giordana, B., Leucine transport is affected by Bacillus thuringiensis Cry1 toxins in brush border membrane vesicles from Ostrinia nubilalis Hb (Lepidoptera: Pyralidae) and Sesamia nonagrioides Lefebvre (Lepidoptera: Noctuidae) midgut (2007) J Membrane Biol, 214, pp. 157-164
Li, H. M., Sun, L., Mittapalli, O., Muir, W. M., Xie, J., Transcriptional signatures in response to wheat germ agglutinin and starvation in Drosophila melanogaster larval midgut (2009) Insect Mol Biol, 18, pp. 21-31
The biological control of insect pests is based on the use of natural enemies. However, the growing information on the molecular mechanisms underpinning the interactions between insects and their natural antagonists can be exploited to develop "bio-inspired" pest control strategies, mimicking suppression mechanisms shaped by long co-evolutionary processes. Here we focus on a virulence factor encoded by the polydnavirus associated with the braconid wasp Toxoneuron nigriceps (TnBV), an endophagous parasitoid of noctuid moth larvae. This virulence factor (TnBVANK1) is a member of the viral ankyrin (ANK) protein family, and appears to be involved both in immunosuppression and endocrine alterations of the host. Transgenic tobacco plants expressing TnBVANK1 showed insecticide activity and caused developmental delay in Spodoptera littoralis larvae feeding on them. This effect was more evident in a transgenic line showing a higher number of transcripts of the viral gene. However, this effect was not associated with evidence of translocation into the haemocoel of the entire protein, where the receptors of TnBVANK1 are putatively located. Indeed, immunolocalization experiments evidenced the accumulation of this viral protein in the midgut, where it formed a thick layer coating the brush border of epithelial cells. In vitro transport experiments demonstrated that the presence of recombinant TnBVANK1 exerted a dose- dependent negative impact on amino acid transport. These results open new perspectives for insect control and stimulate additional research efforts to pursue the development of novel bioinsecticides, encoded by parasitoid-derived genes. However, future work will have to carefully evaluate any effect that these molecules may have on beneficial insects and on non-target organisms.
ibb.cnr.it