Transgenic expression of gallerimycin, a novel antifungal insect defensin from the greater wax moth Galleria mellonella, confers resistance to pathogenic fungi in tobacco

References

Altschul, S.F., Madden, T.L., Schaffer, A.A., Zhang, J., Zhang, Z., Miller, W., and Lipman, D.J. (1997). Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res.25, 3389–3402.10.1093/nar/25.17.3389Search in Google Scholar

Ausubel, F.M., Brent, R., Kingston, R.E., Moore, D.D., Seidman, J.G., Smith, J.A., and Struhl, K. (1987). Current Protocols in Molecular Biology (New York, USA: John Wiley and Sons).Search in Google Scholar

Banzet, N., Latorse, M.P., Bulet, P., Francois, E., Derpierre, C., and Dubald, M. (2002). Expression of insect cystein-rich antifungal peptides in transgenic tobacco enhances resistance to a fungal disease. Plant Sci.162, 995–1006.10.1016/S0168-9452(02)00053-5Search in Google Scholar

Brooks, B.R., Bruccoleri, R.E., Olafson, B.D., States, D.J., Swaminathan, S., and Karplus, M. (1983). CHARMM: a program for macromolecular energy, minimization, and dynamics calculations. J. Comp. Chem.4, 187–217.10.1002/jcc.540040211Search in Google Scholar

Carlsson, A., Nystrom, T., de Cock, H., and Bennich, H. (1998). Attacin – an insect immune protein – binds LPS and triggers the specific inhibition of bacterial outer-membrane protein synthesis. Microbiology144, 2179–2188.10.1099/00221287-144-8-2179Search in Google Scholar

Cavallarin, L., Andreu, D., and San Segundo, B. (1998). Cecropin A-derived peptides are potent inhibitors of fungal plant pathogens. Mol. Plant-Microbe Interact.11, 218–227.10.1094/MPMI.1998.11.3.218Search in Google Scholar

Christensen, B., Fink, J., Merrifield, R.B., and Mauzerall, D. (1988). Channel-forming properties of cecropins and related model compounds incorporated into planar lipid membranes. Proc. Natl. Acad. Sci. USA85, 5072–5076.10.1073/pnas.85.14.5072Search in Google Scholar

Ekengren, S. and Hultmark, D. (1999). Drosophila cecropin as an antifungal agent. Insect. Biochem. Mol. Biol.29, 965–972.10.1016/S0965-1748(99)00071-5Search in Google Scholar

Fehlbaum, P., Bulet, P., Michaut, L., Lagueux, M., Broekaert, W.F., Hetru, C., and Hoffmann, J.A. (1994). Insect immunity. Septic injury of Drosophila induces the synthesis of a potent antifungal peptide with sequence homology to plant antifungal peptides. J. Biol. Chem.269, 33159–33163.Search in Google Scholar

Galis, I., Bilyeu, K.D., Godinho, M.J.G., and Jameson, P.E. (2005). Expression of three Arabidopsis cytokinin oxidase/dehydrogenase promoter::GUS chimeric constructs in tobacco: response to developmental and biotic factors. Plant Growth Regul.45, 173–182.10.1007/s10725-005-2547-5Search in Google Scholar

Gao, A.G., Hakimi, S.M., Mittanck, C.A., Wu, Y., Woerner, B.M., Stark, D.M., Shah, D.M., Liang, J., and Rommens, C.M. (2000). Fungal pathogen protection in potato by expression of a plant defensin peptide. Nat. Biotechnol.18, 1307–1310.10.1038/82436Search in Google Scholar

Garcia, M.L., Gao, Y.D., McManus, O.B., and Kaczorowski, G.J. (2001). Potassium channels: from scorpion venoms to high-resolution structure. Toxicon39, 739–748.10.1016/S0041-0101(00)00214-2Search in Google Scholar

Hammond-Kosack, K.E. and Parker, J.E. (2003). Deciphering plant-pathogen communication: fresh perspectives for molecular resistance breeding. Curr. Opin. Biotechnol.14, 177–193.10.1016/S0958-1669(03)00035-1Search in Google Scholar

Hightower, R., Baden, C., Penzes, E., and Dunsmuir, P. (1994). The expression of cecropin peptide in transgenic tobacco does not confer resistance to Pseudomonas syringae pv. tabaci. Plant Cell Rep. 13, 295–299.10.1007/BF00233324Search in Google Scholar PubMed

Horsh, R., Fry, J., Hoffman, H., Eicholts, D., Rogers, S., and Fraley, R. (1985). Simple and general method for transferring genes into plants. Science277, 1229–1231.10.1126/science.227.4691.1229Search in Google Scholar PubMed

Huang, Y., Nordeen, R.O., Di, M., Owens, L.D., and McBeath, J.H. (1997). Expression of an engineered cecropin gene cassette in transgenic tobacco plants confers disease resistance to Pseudomonas syringae pv tabaci. Phytopathology87, 494–499.10.1094/PHYTO.1997.87.5.494Search in Google Scholar PubMed

Hultmark, D., Engstrom, A., Andersson, K., Steiner, H., Bennich, H., and Boman, H.G. (1983). Insect immunity. Attacins, a family of antibacterial proteins from Hyalophora cecropia. EMBO J.2, 571–576.Search in Google Scholar

Imani, J., Berting, A., Nitsche, S., Schäfer, S., Gerlich, W.H., and Neumann, K.-H. (2002). The integration of a major hepatitis B virus gene into cell-cycle synchronized carrot cell suspension cultures and its expression in regenerated carrot plants. Plant Cell Tissue Organ Cult.71, 157–164.10.1023/A:1019903216459Search in Google Scholar

Jameson, P.E. (2000). Cytokinins and auxins in plant-pathogen interactions – an overview. Plant Growth Regul.32, 369–380.10.1023/A:1010733617543Search in Google Scholar

Jaynes, J.M., Xanthopoulos, K.G., Destefano-Beltran, L., and Dodds, J.H. (1987). Increasing bacterial disease resistance in plants utilizing antibacterial genes from insects. Bioessays6, 263–270.10.1002/bies.950060605Search in Google Scholar

Jefferson, R.A., Kavanagh, T.A., and Bevan, M.W. (1987). GUS fusions: β-glucuronidase as a sensitive and versatile gene fusion marker in higher plants. EMBO J.6, 3901–3907.10.1002/j.1460-2075.1987.tb02730.xSearch in Google Scholar PubMed PubMed Central

Jouirou, B., Mosbah, A., Visan, V., Grissmer, S., M'Barek, S., Fajloun, Z., Van Rietschoten, J., Devaux, C., Rochat, H., Lippens, G., et al. (2004). Cobatoxin 1 from Centruroides noxius scorpion venom: chemical synthesis, three-dimensional structure in solution, pharmacology and docking on K⁺ channels. Biochem. J.377, 37–49.10.1042/bj20030977Search in Google Scholar PubMed PubMed Central

Ko, K., Norelli, J.L., Reynoird, J.P., Boresjza, W.E., Brown, S.K., and Aldwinckle, H.S. (2000). Effect of untranslated leader sequence of AMV RNA 4 and signal peptide of pathogenesis-related protein 1b on attacin gene expression, and resistance to fire blight in transgenic apple. Biotechnol. Lett.22, 373–381.10.1023/A:1005672601625Search in Google Scholar

Koncz, C. and Schell, J. (1986). The promoter of TL-DNA gene 5 controls the tissue-specific expression of chimeric genes carried by a novel type of Agrobacterium binary vector. Mol. Gen. Genet.204, 383–396.10.1007/BF00331014Search in Google Scholar

Kraulis, P.J. (1991). MolScript: a program to produce both detailed and schematic plots of protein structures. J. Appl. Crystallogr.24, 946–950.10.1107/S0021889891004399Search in Google Scholar

Kylsten, P., Samakovlis, C., and Hultmark, D. (1990). The cecropin locus in Drosophila: a compact gene cluster involved in the response to infection. EMBO J.9, 217–224.10.1002/j.1460-2075.1990.tb08098.xSearch in Google Scholar PubMed PubMed Central

Lamberty, M., Ades, S., Uttenweiler Joseph, S., Brookhart, G., Bushey, D., Hoffmann, J.A., and Bulet, P. (1999). Insect immunity. Isolation from the lepidopteran Heliothis virescens of a novel insect defensin with potent antifungal activity. J. Biol. Chem.274, 9320–9326.10.1074/jbc.274.14.9320Search in Google Scholar PubMed

Langridge, W.H.R., Fitzgerald, K.J., Koncz, C., Schell, J., and Szalay, A.A. (1989). Dual promoter of Agrobacterium tumefaciens mannopine synthase genes is regulated by plant growth hormones. Proc. Natl. Acad. Sci. USA80, 3214–3223.10.1073/pnas.86.9.3219Search in Google Scholar PubMed PubMed Central

Li, W., Yuan, R.C., Burns, J.K., Timmer, L.W., and Chung, K.R. (2003a). Genes for hormone biosynthesis and regulation are highly expressed in citrus flowers infected with the fungus Colletotrichum acutatum, causal agent of postbloom fruit drop. J. Am. Soc. Hortic. Sci.128, 578–583.10.21273/JASHS.128.4.0578Search in Google Scholar

Li, X.Q., Gasic, K., Cammue, B., Broekaert, W., and Korban, S.S. (2003b). Transgenic rose lines harboring an antimicrobial protein gene, Ace-AMP1, demonstrate enhanced resistance to powdery mildew (Sphaerotheca pannosa). Planta218, 226–232.10.1007/s00425-003-1093-5Search in Google Scholar PubMed

Lockey, T.D. and Ourth, D.D. (1996). Formation of pores in Escherichia coli cell membranes by a cecropin isolated from hemolymph of Heliothis virescens larvae. Eur. J. Biochem.236, 263–271.10.1111/j.1432-1033.1996.00263.xSearch in Google Scholar PubMed

MacKerell, A.D., Bashford, D., Bellott, M., Dunbrack, R.L., Evanseck, J.D., Field, M.J., Fischer, S., Gao, J., Guo, H., Ha, S., et al. (1998). All-atom empirical potential for molecular modeling and dynamics studies of proteins. J. Phys. Chem. B102, 3586–3616.10.1021/jp973084fSearch in Google Scholar PubMed

Maksimov, I.V., Ganiev, R.M., Khairullin, R.M., and Shakirova, F.M. (2003). Hormonal balance in the wheat sprouts infected Tilletia caries. Mikol. Fitopatol.37, 64–71.Search in Google Scholar

Mandahar, C.L. and Garg, I.D. (1976). Cytokinin activity of powdery mildew (Erysiphe cichoracearum) infected leaves of Abelmoschus esculentus. Phytopathol. Z.85, 86–89.10.1111/j.1439-0434.1976.tb04803.xSearch in Google Scholar

Maor, R. and Shirasu, K. (2005). The arms race continues: battle strategies between plants and fungal pathogens. Curr. Opin. Microbiol.8, 399–404.10.1016/j.mib.2005.06.008Search in Google Scholar

Maor, R., Haskin, S., Levi-Kedmi, H., and Sharon, A. (2004). In planta production of indole-3-acetic acid by Colletotrichum gloeosporioides f. sp aeschynomene. Appl. Environ. Microb.70, 1852–1854.10.1128/AEM.70.3.1852-1854.2004Search in Google Scholar

Marti-Renom, M.A., Stuart, A.C., Fiser, A., Sánchez, R., Melo, F., and Sali, A. (2000). Comparative protein structure modeling of genes and genomes. Annu. Rev. Biophys. Biomol. Struct.29, 291–325.10.1146/annurev.biophys.29.1.291Search in Google Scholar

Mills, D., Hammerschlag, F.A., Nordeen, R.O., and Owens, L.D. (1994). Evidence for the breakdown of cecropin B by proteinases in the intercellular fluid of peach leaves. Plant Sci.104, 17–22.10.1016/0168-9452(94)90186-4Search in Google Scholar

Moffat, A.S. (2001). Finding new ways to fight plant diseases. Science292, 2270–2273.10.1126/science.292.5525.2270Search in Google Scholar

Murashige, T. and Skoog, F. (1962). A revised medium for rapid growth and bioassay with tobacco tissue culture. Physiol. Plantarum15, 473–497.10.1111/j.1399-3054.1962.tb08052.xSearch in Google Scholar

Nakai, K. and Kanehisa, M. (1991). Expert system for predicting protein localization sites in Gram-negative bacteria. Proteins11, 95–110.10.1002/prot.340110203Search in Google Scholar

Oerke, E.C., Dehne, H.W., Sch;auonbeck, F., and Weber, A. (1994). Crop production and crop protection: estimated losses in major food and cash crops (Amsterdam, The Netherlands: Elsevier).Search in Google Scholar

Osusky, M., Zhou, G., Osuska, L., Hancock, R.E., Kay, W.W., and Misra, S. (2000). Transgenic plants expressing cationic peptide chimeras exhibit broad-spectrum resistance to phytopathogens. Nat. Biotechnol.18, 1162–1166.10.1038/81145Search in Google Scholar

Owens, L.D. and Heutte, T.M. (1997). A single amino acid substitution in the antimicrobial defense protein cecropin B is associated with diminished degradation by leaf intercellular fluid. Mol. Plant-Microbe Interact.10, 525–528.10.1094/MPMI.1997.10.4.525Search in Google Scholar

Pearson, W.R. (1990). Rapid and sensitive sequence comparison with FASTP and FASTA. Methods Enzymol.183, 63–98.10.1016/0076-6879(90)83007-VSearch in Google Scholar

Reynoird, J.P., Mourgues, F., Norelli, J., Aldwinckle, H.S., Brisset, M.N., and Chevreau, E. (1999). First evidence for improved resistance to fire blight in transgenic pear expressing the attacin E gene from Hyalophora cecropia. Plant Sci.149, 23–31.10.1016/S0168-9452(99)00139-9Search in Google Scholar

Rozen, S. and Skaletsky, H. (2000). Primer3 on the WWW for General Users and for Biologist Programmers (Totowa, NJ, USA: Humana Press).Search in Google Scholar

Sali, A. and Blundell, T.L. (1993). Comparative protein modelling by satisfaction of spatial restraints. J. Mol. Biol.234, 779–815.10.1006/jmbi.1993.1626Search in Google Scholar

Samakovlis, C., Kimbrell, D.A., Kylsten, P., Engstrom, A., and Hultmark, D. (1990). The immune response in Drosophila: pattern of cecropin expression and biological activity. EMBO J.9, 2969–2976.10.1002/j.1460-2075.1990.tb07489.xSearch in Google Scholar

Sambrook, J., Fritsch, E.F., and Maniatis, T. (1989). Molecular Cloning: A Laboratory Manual, 2nd Edition (Cold Spring Harbor, NY, USA: Cold Spring Harbor Laboratory Press).Search in Google Scholar

Schuhmann, B., Seitz, V., Vilcinskas, A., and Podsiadlowski, L. (2003). Cloning and expression of gallerimycin, an antifungal peptide expressed in immune response of greater wax moth larvae, Galleria mellonella. Arch. Insect Biochem. Physiol.53, 125–133.10.1002/arch.10091Search in Google Scholar

Seitz, V., Clermont, A., Wedde, M., Hummel, M., Vilcinskas, A., Schlatterer, K., and Podsiadlowski, L. (2003). Identification of immunorelevant genes from greater wax moth (Galleria mellonella) by a subtractive hybridization approach. Dev. Comp. Immunol.27, 207–215.10.1016/S0145-305X(02)00097-6Search in Google Scholar

Sharma, A., Sharma, R., Imamura, M., Yamakawa, M., and Machii, H. (2000). Transgenic expression of cecropin B, an antibacterial peptide from Bombyx mori, confers enhanced resistance to bacterial leaf blight in rice. FEBS Lett.484, 7–11.10.1016/S0014-5793(00)02106-2Search in Google Scholar

Steiner, H., Hultmark, D., Engstrom, A., Bennich, H., and Boman, H.G. (1981). Sequence and specificity of two antibacterial proteins involved in insect immunity. Nature292, 246–248.10.1038/292246a0Search in Google Scholar

Steiner, H., Andreu, D., and Merrifield, R.B. (1988). Binding and action of cecropin and cecropin analogues: antibacterial peptides from insects. Biochim. Biophys. Acta939, 260–266.10.1016/0005-2736(88)90069-7Search in Google Scholar

Thevissen, K., Ghazi, A., DeSamblanx, G.W., Brownlee, C., Osborn, R.W., and Broekaert, W.F. (1996). Fungal membrane responses induced by plant defensins and thionins. J. Biol. Chem.271, 15018–15025.10.1074/jbc.271.25.15018Search in Google Scholar PubMed

Thevissen, K., Warnecke, D.C., Francois, I.E., Leipelt, M., Heinz, E., Ott, C., Zahringer, U., Thomma, B.P., Ferket, K.K., and Cammue, B.P. (2004). Defensins from insects and plants interact with fungal glucosylceramides. J. Biol. Chem.279, 3900–3905.10.1074/jbc.M311165200Search in Google Scholar PubMed

Thompson, J.D., Higgins, D.G., and Gibson, T.J. (1994). Clustal-W – improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res.22, 4673–4680.10.1093/nar/22.22.4673Search in Google Scholar PubMed PubMed Central

Velten, J. and Schell, J. (1985). Selection-expression plasmid vectors for use in genetic transformation of higher plants. Nucleic Acids Res.13, 6981–6998.10.1093/nar/13.19.6981Search in Google Scholar PubMed PubMed Central

Vilcinskas, A. and Gross, J. (2005). Drugs from bugs: the use of insects as a valuable source of transgenes with potential in modern plant protection strategies. J. Pest Sci.78, 187–191.10.1007/s10340-005-0114-5Search in Google Scholar

Vilcinskas, A. and Matha, V. (1997). Antimycotic activity of lysozyme and its contribution to antifungal humoral defence reactions in Galleria mellonella. Anim. Biol.6, 19–29.Search in Google Scholar

Vizarova, G. (1979). Changes in the level of endogenous cytokinins of barley during the development of powdery mildew Erysiphe graminis hordei. Phytopathol. Z.95, 329–341.10.1111/j.1439-0434.1979.tb01608.xSearch in Google Scholar

Volkoff, A.N., Rocher, J., d'Alencon, E., Bouton, M., Landais, I., Quesada-Moraga, E., Vey, A., Fournier, P., Mita, K., and Devauchelle, G. (2003). Characterization and transcriptional profiles of three Spodoptera frugiperda genes encoding cysteine-rich peptides. A new class of defensin-like genes from lepidopteran insects? Gene319, 43–53.Search in Google Scholar

Yevtushenko, D.P., Romero, R., Forward, B.S., Hancock, R.E., Kay, W.W., and Misra, S. (2005). Pathogen-induced expression of a cecropin A-melittin antimicrobial peptide gene confers antifungal resistance in transgenic tobacco. J. Exp. Bot.56, 1685–1695.10.1093/jxb/eri165Search in Google Scholar PubMed

Zasloff, M. (2002). Antimicrobial peptides of multicellular organisms. Nature415, 389–395.10.1038/415389aSearch in Google Scholar PubMed