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Genetic engineering strategies for enhancing tomato resistance to fungal and bacterial pathogens

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Abstract

The classification and detailed overview of the currently known effective strategies used to increase the resistance of tomato (Solanum lycopersicum L., syn. Lycopersicon esculentum Mill.) plants to infectious fungal and bacterial diseases by genetic engineering approaches are presented. Modern data on the mechanisms of the protective effect of heterologous genes on the enhancement of transgenic tomato resistance to fungal and bacterial pathogens are discussed.

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Abbreviations

AMP:

antimicrobial peptides

HR:

hypersensitive response

PGIP:

polygalacturonase-inhibiting proteins

PR proteins:

pathogenesis-related proteins

RIP:

ribosome-inactivating proteins

SAR:

systemic acquired resistance

35S CaMV :

constitutive promoter of 35S RNA of cauliflower mosaic virus

KLP:

knottin-type peptides

References

  1. Food and Agriculture Organization of the United Nations, Rome (Italy): FAO, 2012, http://www/fao.org

  2. Smirnov, A.N. and Kuznetsov, S.A., Late blight of tomato, Zashchita i karantin rastenii, 2006, no. 3, pp. 20–23.

    Google Scholar 

  3. Smirnov, A.N., Oospores of Phytophthora infestans, Mikol. Fitopatol., 2003, vol. 37, pp. 3–21.

    Google Scholar 

  4. Sarowar, S., Kim, Y.J., Kim, E.N., Kim, K.D., Choi, J.Y., Hyung, N.I., and Shin, J.S., Constitutive expression of two pathogenesis-related genes in tomato plants enhanced resistance to oomycete pathogen Phytophthora capsici, Plant Cell, Tissue Organ Cult., 2006, vol. 86, pp. 7–14.

    Article  CAS  Google Scholar 

  5. Jongedijk, E., Tigelaar, H., van Roekel, J.S.C., BresVloemans, S.A., Dekker, I., Elsen, P.J.M., Cornelissen, B.J.C., and Melchers, L.S., Synergistic activity of chitinases and β-1,3-glucanases enhances fungal resistance in transgenic tomato plants, Euphytica, 1995, vol. 85, pp. 173–180.

    Article  CAS  Google Scholar 

  6. Schaefer, S.C., Gasic, K., Cammue, B., Broekaert, W., van Damme, E.J.M., Peumans, W.J., and Korban, S.S., Enhanced resistance to early blight in transgenic tomato lines expressing heterologous plant defense genes, Planta, 2005, vol. 222, pp. 858–866.

    Article  PubMed  CAS  Google Scholar 

  7. Tabaeizadeh, Z., Agharbaouri, Z., Harrak, H., and Poysa, V., Transgenic tomato plants expressing a Lycopersicon chilense chitinase gene demonstrate improved resistance to Verticillium dahlia race 2, Plant Cell Rep., 1999, vol. 19, pp. 197–202.

    Article  CAS  Google Scholar 

  8. Abbas, D.E., Abdallah, N.A., and Madkour, M.M., Production of transgenic tomato plants with enhanced resistance against the fungal pathogen Fusarium oxysporum, Arab. J. Biotechnol., 2009, vol. 12, pp. 73–84.

    Google Scholar 

  9. Girhepuje, P.V. and Shinde, G.B., Transgenic tomato plant expressing a wheat endochitinase gene demonstrated enhanced resistance to Fusarium oxysporum f. sp. lycopersici, Plant Cell, Tissue Organ Cult., 2010, vol. 105, pp. 243–251.

    Article  Google Scholar 

  10. Lee, H.I. and Raikhel, N.V., Prohevein is poorly processed but shows enhanced resistance to a chitin-binding fungus in transgenic plants, Braz. J. Med. Biol. Res., 1995, vol. 28, pp. 743–750.

    PubMed  CAS  Google Scholar 

  11. Lee, O.S., Lee, B., Park, N., Koo, J.C., Kim, Y.H., Prasad, D.T., Karigar, C., Chun, H.J., Jeong, B.R., Kim, D.H., Nam, J., Yun, J.G., Kwak, S.S., Cho, M.J., and Yun, D.J., Pn-AMPs, the hevein-like proteins from Pharbitis nil confers disease resistance against phytopathogenic fungi in tomato, Lycopersicum esculentum, Phytochemistry, 2003, vol. 62, pp. 1073–1079.

    Article  CAS  Google Scholar 

  12. Khaliluev, M.R., Mamonov, A.G., Smirnov, A.N., Kharchenko, P.N., and Dolgov, S.V., Expression of genes encoding chitin-binding proteins (PR-4) and hevein-like antimicrobial peptides in transgenic tomato plants enhanced resistanse to Phytophthora infestance, Russ. Agricult. Sci., 2011, no. 4, pp. 297–302.

    Google Scholar 

  13. Ouyang, B., Chen, Y.H., Li, H.X., Qian, C.J., Huang, S.L., and Ye, Z.B., Transformation of tomatoes with osmotin and chitinase genes and their resistance to Fusarium wilt, J. Hortic. Sci. Biotechnol., 2005, vol. 80, pp. 517–522.

    CAS  Google Scholar 

  14. Malehorn, D.E., Borgmeyer, J.R., Smith, C.E., and Shah, D.M., Characterization and expression of an antifungal zeamatin-like protein (Zlp) gene from Zea mays, Plant Physiol., 1994, vol. 106, pp. 1471–1481.

    Article  PubMed  CAS  Google Scholar 

  15. Radhajeyalakshmi, R., Velazhahan, R., Balasubramanian, P., and Doraiswamy, S., Overexpression of thaumatin-like protein in transgenic tomato plants confers enhanced resistance to Alternaria solani, Arch. Phytopathol. Plant Protect., 2005, vol. 38, pp. 257–266.

    Article  CAS  Google Scholar 

  16. Korneeva, I.V., Shestibratov, K.A., Lavrova, N.V., Firsov, A.P., Lebedev, V.G., Kharchenko, P.N., and Dolgov, S.V., Expression of PR-5 protein thaumatin II for improving diseases resistance and fruit quality of tomato, Acta Hortic., 2008, vol. 789, pp. 151–158.

    CAS  Google Scholar 

  17. Korneeva, I.V., Varlamova, N.V., Pushin, A.S., Firsov, A.P., Dolgov, S.V., and Monakhos, G.F., Motamedi, Shalamzari, A., and Dzhalilov, F.S., Transgenic tomato plants expressing PR-5 protein genes demonstrated resistance against Phytophthora infestans and Xanthomonas vesicatoria, Acta Hortic., 2011, vol. 914, pp. 415–418.

    CAS  Google Scholar 

  18. Parashina, E.V., Serdobinskii, L.A., Kalle, E.G., Lavrova, N.V., Avetisov, V.A., Lunin, V.G., and Naroditskii, B.S., Genetic engineering of oilseed rape and tomato plants expressing a radish defensin gene, Russ. J. Plant Physiol., 2000, vol. 47, pp. 417–423.

    CAS  Google Scholar 

  19. Kostov, K., Christova, P., Slavov, S., and Batchvarova, R., Constitutive expression of a radish gene Rs-afp2 in tomato increased the resistance to fungal pathogen, Agric. Environ. Biotechnol., 2009, vol. 23, pp. 1121–1125.

    CAS  Google Scholar 

  20. Zainal, Z., Marouf, E., Ismail, I., and Fei, C.K., Expression of the Capsicum annum (Chili) defensin gene transgenic tomatoes confers enhanced resistance to fungal pathogen, Am. J. Plant Physiol., 2009, vol. 4, pp. 70–79.

    Article  CAS  Google Scholar 

  21. Abdallah, N.A., Shah, D., Abbas, D., and Madkour, M., Stable integration and expression of a plant defensin in tomato confers resistance to Fusarium wilt, GM Crops, 2010, vol. 1, pp. 344–350.

    Article  PubMed  Google Scholar 

  22. Chen, S.-C., Liu, A.-R., and Zou, Z.-R., Overexpression of glucanase gene and defensin gene in transgenic tomato enhances resistance to Ralstonia solanacearum, Russ. J. Plant Physiol., 2006, vol. 53, pp. 671–677.

    Article  CAS  Google Scholar 

  23. Chen, S.C., Liu, A.R., Wang, F.H., and Ahammed, G.J., Combined overexpression of chitinase and defensin genes in transgenic tomato enhances resistance to Botrytis cinerea, Afr. J. Biotechnol., 2009, vol. 8, pp. 5182–5188.

    CAS  Google Scholar 

  24. Chan, Y.L., Prasad, V., Chen, K.H., Liu, P.C., Chan, M.T., and Cheng, C.-P., Transgenic tomato plants expressing an Arabidopsis thionin (Thi2.1) driven by fruit-inactive promoter battle against phytopathogenic attack, Planta, 2005, vol. 221, pp. 386–393.

    Article  PubMed  CAS  Google Scholar 

  25. Li, X., Yang, X., Li, D., Guo, S., and Pei, Y., Enhanced disease resistance in transgenic tomato over-expression antimicrobial proteins LjAMP1 and LjAMP2 from motherwort seeds, Acta Phytophyl. Sinica, 2007, vol. 4, pp. 353–358.

    Google Scholar 

  26. Walz, A., Zingen-Sell, I., Loeffler, M., and Sauer, M., Expression of an oxalate oxidase gene in tomato and severity of disease caused by Botrytis cinerea and Sclerotinia sclerotiorum, Plant Pathol., 2008, vol. 57, pp. 453–458.

    Article  CAS  Google Scholar 

  27. Balaji, V. and Smart, C.D., Over-expression of snakin-2 and extensin-like protein genes restricts pathogen invasiveness and enhanced tolerance to Clavibacter michiganensis subsp. michiganensis in transgenic tomato (Solanum lycopersicum), Transgenic Res., 2012, vol. 21, pp. 23–37.

    Article  PubMed  CAS  Google Scholar 

  28. Broekaert, W.F., Cammue, B.P.A., de Bolle, M.F.C., Thevissen, K., de Samblanx, G.W., Osborn, R.W., and Nielson, D.K., Antimicrobial peptides from plants, Crit. Rev. Plant Sci., 1997, vol. 16, pp. 297–323.

    CAS  Google Scholar 

  29. Selitrennikoff, C.P., Antifungal proteins, Appl. Environ. Microbiol., 2001, vol. 67, pp. 2883–2894.

    Article  PubMed  CAS  Google Scholar 

  30. Edreva, A., Pathogenesis-related protein: research progress in the last 15 years, Gen. Appl. Plant Physiol., 2005, vol. 31, pp. 105–124.

    CAS  Google Scholar 

  31. Van Loon, L.C., Rep, M., and Pieterse, C.M.J., Significance of inducible defense-related proteins in infected plants, Annu. Rev. Phytopathol., 2006, vol. 44, pp. 135–162.

    Article  PubMed  Google Scholar 

  32. Mauch, F. and Staehelin, L.A., Functional implications of the subcellular localization of ethyleneinduced chitinase and β-1,3-glucanase in bean leaves, Plant Cell, 1989, vol. 1, pp. 447–457.

    PubMed  CAS  Google Scholar 

  33. Van Parijs, J., Broeckaert, W.F., Goldstein, I.J., and Peumans, W.J., Hevein: an antifungal protein from rubber-tree latex, Planta, 1991, vol. 183, pp. 258–264.

    Article  Google Scholar 

  34. Liu, J.J., Sturrock, R., and Ekramoddoullah, A.K.M., The superfamily of thaumatin-like proteins: its origin, evolution, and expression towards biological function, Plant Cell Rep., 2009, vol. 5, pp. 419–436.

    Google Scholar 

  35. Thevissen, K., Ghazi, A., de Samblanx, G.W., Brownlee, C., Osborn, R.W., and Broekaert, W.F., Fungal membrane responses induced by plant defensins and thionins, J. Biol. Chem., 1996, vol. 27, pp. 15018–15025.

    Google Scholar 

  36. Egorov, Ts.A. and Odintsova, T.I., Defense peptides of plant immunity, Russ. J. Bioorg. Chem., 2012, vol. 38, pp. 1–9.

    Article  CAS  Google Scholar 

  37. Cammue, B.P.A., de Bolle, M.F.C., Terras, F.R.G., Proost, P., van Damme, J., Rees, S.B., Vanderleyden, J., and Broekaert, W.F., Isolation and characterization of a novel class of plant antimicrobial peptides from Mirabilis jalapa L. seeds, J. Biol. Chem., 1992, vol. 267, pp. 2228–2233.

    PubMed  CAS  Google Scholar 

  38. Berrocal-Lobo, M., Segura, A., Moreno, M., Lopez, G., Garcia-Olmedo, F., and Molina, A., Snakin-2, an antimicrobial peptide from potato whose gene is locally induced by wounding and responds to pathogen infection, Plant Physiol., 2002, vol. 128, pp. 951–961.

    Article  PubMed  CAS  Google Scholar 

  39. Alan, A.R., Blowers, A., and Earle, E.D., Expression of a magainin-type antimicrobial peptide gene (MSI-99) in tomato enhances resistance to bacterial speck disease, Plant Cell Rep., 2004, vol. 22, pp. 388–396.

    Article  PubMed  CAS  Google Scholar 

  40. Jan, P.S., Huang, H.Y., and Chen, H.M., Expression of a synthesized gene encoding cationic peptide cecropin B in transgenic tomato plants protects against bacterial diseases, Appl. Environ. Microbiol., 2010, vol. 76, pp. 769–775.

    Article  PubMed  CAS  Google Scholar 

  41. Lönnerdal, B. and Iyer, S., Lactoferrin: molecular structure and biological function, Annu. Rev. Nutr., 1995, vol. 15, pp. 93–110.

    Article  PubMed  Google Scholar 

  42. Lee, T.J., Coyne, D.P., Clemente, T.E., and Mitra, A., Partial resistance to bacterial wilt in transgenic tomato plants expressing antibacterial lactoferrin gene, J. Am. Soc. Hortic. Sci., 2002, vol. 127, pp. 158–164.

    CAS  Google Scholar 

  43. Zhang, X.H., Guo, D.J., Zhang, L.M., Li, W.B., and Sun, Y.R., The research on expression of rabbit defensin (NP-1) gene in transgenic tomato, Acta Genet. Sinica, 2000, vol. 27, pp. 953–958.

    CAS  Google Scholar 

  44. Shah, M.R., Mukherjee, P.K., and Eapen, S., Expression of a fungal endochitinase gene in transgenic tomato and tobacco results in enhanced tolerance to fungal pathogens, Physiol. Mol. Biol. Plants, 2010, vol. 16, pp. 39–51.

    Article  PubMed  CAS  Google Scholar 

  45. Grayer, R.J. and Kokubun, T., Plant-fungal interactions: the search for phytoalexins and other antifungal compounds from higher plants, Phytochemistry, 2001, vol. 56, pp. 253–263.

    Article  PubMed  CAS  Google Scholar 

  46. Thomzik, J.E., Stenzel, K., Stöcker, R., Schreier, P.H., Hain, R., and Stahl, D.J., Synthesis of a grapevine phytoalexin in transgenic tomatoes (Lycopersicon esculentum Mill.) conditions resistance against Phytophthora infestans, Physiol. Mol. Plant Pathol., 1997, vol. 51, pp. 265–278.

    Article  CAS  Google Scholar 

  47. Kartel’, N.A., Shpakovskii, G.V., Spivak, S.G., Brichkova, G.G., Yarmolinskii, D.G., Berdichevets, I.N., and Maneshina, T.V., Recombinant plasmid pGBP450f and a method for obtaining transgenic plants with high productivity and resistance to fungal phytopathogens,RF Patent no. 2237717, Byull. Izobret., 2004, no. 10.

    Google Scholar 

  48. Spivak, S.G., Berdichevets, I.N., Litvinovskaya, R.P., Drach, S.V., Kartel’, N.A., and Shpakovskii, G.V., Some peculiarities of steroid metabolism in transgenic Nicotiana tabacum plants bearing the CYP11A1 cDNA of cytochrome P450SCC from the bovine adrenal cortex, Russ. J. Bioorg. Chem., 2010, vol. 36, pp. 224–232.

    Article  CAS  Google Scholar 

  49. Flor, H.H., Host-parasite interactions in flax rust-its genetics and other implications, Phytopathology, 1955, vol. 45, pp. 680–685.

    Google Scholar 

  50. Toyoda, K., Collins, N.C., Takahashi, A., and Shirasu, K., Resistance and susceptibility of plants to fungal pathogens, Transgenic Res., 2002, vol. 11, pp. 567–582.

    Article  PubMed  CAS  Google Scholar 

  51. Van Ooijen, G., van den Burg, H.A., Cornelissen, B.J.C., and Takken, F.L.W., Structure and function of resistance proteins in solanaceous plants, Annu. Rev. Phytopathol., 2007, vol. 45, pp. 43–72.

    Article  PubMed  Google Scholar 

  52. Liu, J., Liu, X., Dai, L., and Wang, G., Recent progress in elucidating the structure, function and evolution of disease resistance genes in plants, J. Genet. Genom., 2007, vol. 34, pp. 765–776.

    Article  Google Scholar 

  53. Honee, G., Melchers, L.S., Vleeshouwers, V.G.A.A., van Roekel, J.S.C., and de Wit, P.J.G.M., Production of the AVR9 elicitor from the fungal pathogen Cladosporium fulfum in transgenic tobacco and tomato plants, Plant Mol. Biol., 1995, vol. 29, pp. 909–920.

    Article  PubMed  CAS  Google Scholar 

  54. Martin, G.B., Brommonschenkel, S.H., Chunwongse, J., Frary, A., Ganal, M.W., Spivey, R., Wu, T., Earle, E.D., and Tanksley, S.D., Map-based cloning of a protein kinase gene conferring disease resistance in tomato, Science, 1993, vol. 262, pp. 1432–1436.

    Article  PubMed  CAS  Google Scholar 

  55. Koc, N.K., Kayim, M., Yetisir, H., Sari, N., Unlu, Yuceer, S., and Arici, S.E., The improvement of resistance to bacterial speck in transgenic tomato plants by Agrobacterium tumefaciens mediated transformation, Russ. J. Plant Physiol., 2007, vol. 54, pp. 89–96.

    Article  CAS  Google Scholar 

  56. Tai, T.H., Dahlbeck, D., Clark, E.T., Gajiwala, P., Pasion, R., Whalen, M.C., Stall, R.E., and Staskawicz, B.J., Expression of the Bs2 pepper gene confers resistance to bacterial spot disease in tomato, Proc. Natl. Acad. Sci. USA, 1999, vol. 96, pp. 14 153–14 158.

    Article  CAS  Google Scholar 

  57. Afroz, A., Chaudhry, Z., Rashid, U., Ali, G.M., Nazir, F., Iqbal, J., and Khan, M.R., Enhanced resistance against bacterial wilt in transgenic tomato (Lycopersicon esculentum) lines expressing the Xa21 gene, Plant Cell, Tissue Organ Cult., 2011, vol. 104, pp. 227–237.

    Article  CAS  Google Scholar 

  58. De Lorenzo, G., D’Ovidio, R., and Cervone, F., The role of polygalacturonase-inhibiting proteins (PGIPs) in defense against pathogenic fungi, Annu. Rev. Phytopathol., 2001, vol. 39, pp. 313–335.

    Article  PubMed  Google Scholar 

  59. Glinka, E.M., Protsenko, M.A., Bulantseva, E.A., and Sal’kova, E.G., Effect of proteinaceous polygalacturonase inhibitors from apple seed tissue on an enzyme isolated from phytopathogenic fungi, Prikl. Biokhim. Mikrobiol., 2001, vol. 37, pp. 607–611.

    PubMed  CAS  Google Scholar 

  60. Desiderio, A., Aracri, B., Leckie, F., Mattei, B., Salvi, G., Tigelaar, H., van Roekel, J.S.C., Baulcombe, D.C., Melchers, L.S., de Lorenzo, G., and Cervone, F., Polygalacturonase-inhibiting proteins (PGIPs) with different specificities are expressed in Phaseolus vulgaris, Mol. Plant-Microbe Interact., 1997, vol. 10, pp. 852–860.

    Article  PubMed  CAS  Google Scholar 

  61. Powell, A.L.T., van Kan, J., Ten, Have, A., Visser, J., Greve, L.C., Bennett, A.B., and Labavitch, L.M., Transgenic expression of pear PGIP in tomato limits fungal colonization, Mol. Plant-Microbe Interact., 2000, vol. 13, pp. 942–950.

    Article  PubMed  CAS  Google Scholar 

  62. Kesarwani, M., Azam, M., Natarajan, K., Mehta, A., and Datta, A., Oxalate decarboxylase from Collybia velutipes: molecular cloning and its overexpression to confer resistance to fungal infection in transgenic tobacco and tomato, J. Biol. Chem., 2000, vol. 275, pp. 7230–7238.

    Article  PubMed  CAS  Google Scholar 

  63. Maksimov, I.V., Cherepanova, E.A., and Khairullin, R.M., “Chitin-specific” peroxidases in plants, Biochemistry (Moscow), 2003, vol. 68, pp. 111–115).

    Article  CAS  Google Scholar 

  64. Peberdy, J.F., Presidential address: fungi without coatsprotoplast as tool for mycological research, Mycol. Res., 1989, vol. 93, pp. 1–20.

    Article  Google Scholar 

  65. Medeghini, Bonatti, P., Lorenzini, G., Baroni, Fornasiero, R., Nali, C., and Sgarbi, E., Cytochemical detection of cell wall bound peroxidase in rust infected broad bean leaves, J. Phytopathol., 1994, vol. 140, pp. 319–325.

    Article  Google Scholar 

  66. Bradley, D.J., Kjellbom, P., and Lamb, C.J., Elicitor- and wound-induced oxidative cross-linking of a proline-rich plant cell wall structural protein: a novel, rapid plant defense response, Cell, 1992, vol. 70, pp. 21–

    Article  PubMed  CAS  Google Scholar 

  67. De Leeuw, G.T.N., Deposition of lignin, suberin and callose in relation to the restriction of infection by Botrytis cinerea in ghost spots of tomato fruits, J. Phytopathol., 1985, vol. 112, pp. 143–152.

    Article  Google Scholar 

  68. Reuveni, R. and Ferreira, J.F., The relationship between peroxidase activity and the resistance of tomatoes (Lycopersicum esculentum) to Verticillium dahlia, J. Phytopathol., 1985, vol. 112, pp. 193–197.

    Article  CAS  Google Scholar 

  69. Lagrimini, L.M., Vaughn, J., Erb, W.A., and Miller, S.A., Peroxidase overproduction in tomato: wound-induced polyphenol deposition and disease resistance, HortScience, 1993, vol. 28, pp. 218–221.

    CAS  Google Scholar 

  70. McDowell, J.M. and Dangl, J.L., Signal transduction in the plant immune response, Trends Biochem. Sci., 2000, vol. 25, pp. 79–82.

    Article  PubMed  CAS  Google Scholar 

  71. Oldroyd, G.E.D. and Staskawicz, B.J., Genetically engineered broad-spectrum disease resistance in tomato, Proc. Natl. Acad. Sci. USA, 1998, vol. 95, pp. 10300–10305.

    Article  PubMed  CAS  Google Scholar 

  72. Zhou, J.M., Trifa, Y., Silva, H., Pontier, D., Lam, E., Shah, J., and Klessig, D.F., NPR1 differentially interacts with members of the TGA/OBF family of transcription factors that bind an element of the PR-1 gene required for induction by salicylic acid, Mol. Plant-Microbe Interact., 2000, vol. 13, pp. 191–202.

    Article  PubMed  CAS  Google Scholar 

  73. Lin, W.C., Lu, C.F., Wu, J.W., Cheng, M.L., Lin, Y.M., Yang, N.S., Black, L., Green, S.K., Wang, J.F., and Cheng, C.P., Transgenic tomato plants expressing the Arabidopsis NPR1 gene display enhanced resistance to a spectrum of fungal and bacterial diseases, Transgenic Res., 2004, vol. 13, pp. 567–581.

    Article  PubMed  CAS  Google Scholar 

  74. He, P., Warren, R.F., Zhao, T., Shan, L., Zhu, L., Tang, X., and Zhou, J.-M., Overexpression of Pti5 in tomato potentiates pathogen-induced defense gene expression and enhanced diseases resistance to Pseudomonas syringae pv. tomato, Mol. Plant-Microbe Interact., 2001, vol. 14, pp. 1453–1457.

    Article  PubMed  CAS  Google Scholar 

  75. Scheer, J.M. and Ryan, C.A., The systemin receptor SR160 Lycopersicon peruvianum is a member of the LRR receptor kinase family, Proc. Natl. Acad. Sci. USA, 2002, vol. 99, pp. 9585–9590.

    Article  PubMed  CAS  Google Scholar 

  76. Jones, R.W., Ospina-Giraldo, M., and Clemente, T., Prosystemin — antimicrobial-peptide fusion reduces tomato late blight lesion expansion, Mol. Breed., 2004, vol. 14, pp. 83–89.

    Article  CAS  Google Scholar 

  77. Mehdy, M.C., Active oxygen species in plant defense against pathogens, Plant Physiol., 1994, vol. 105, pp. 467–472.

    PubMed  CAS  Google Scholar 

  78. Huang, H.E., Liu, C.A., Lee, M.J., Kuo, C.G., Chen, H.M., Ger, M.J., Tsai, Y.C., Chen, Y.R., Lin, M.K., and Feng, T.Y., Resistance enhancement of transgenic tomato to bacterial pathogens by the heterologous expression of sweet pepper ferredoxin-I protein, Phytopathology, 2007, vol. 97, pp. 900–906.

    Article  PubMed  CAS  Google Scholar 

  79. Seong, E.S., Cho, H.S., Choi, D., Joung, Y.H., Lim, C.K., Hur, J.H., and Wang, M.H., Tomato plants overexpressing CaKR1 enhanced tolerance to salt and oxidative stress, Biochem. Biophys. Res. Commun., 2007, vol. 363, pp. 983–988.

    Article  PubMed  CAS  Google Scholar 

  80. Wu, G., Shortt, B.J., Lawrence, E.B., Leon, J., Fitzsimmons, K.C., Levine, E.B., Raskin, I., and Shah, D.M., Activation of host defense mechanisms by elevated production of H2O2 in transgenic plants, Plant Physiol., 1997, vol. 115, pp. 427–435.

    PubMed  CAS  Google Scholar 

  81. Kerdnaimongkol, K. and Woodson, W.R., Inhibition of catalase by antisense RNA increases susceptibility to oxidative stress and chilling injury in tomato plants, J. Am. Soc. Hortic. Sci., 1999, vol. 124, pp. 330–336.

    CAS  Google Scholar 

  82. Mayer, A.M., Polyphenol oxidases in plants and fungi: going places? A review, Phytochemistry, 2006, vol. 67, pp. 2318–2331.

    Article  PubMed  CAS  Google Scholar 

  83. Thipyapong, P., Hunt, M.D., and Steffens, J.C., Antisense down-regulation of polyphenol oxidase results in enhanced disease susceptibility, Planta, 2004, vol. 220, pp. 105–107.

    Article  PubMed  CAS  Google Scholar 

  84. Li, L. and Steffens, J.C., Overexpression of polyphenol oxidase in transgenic tomato plants results in enhanced bacterial disease resistance, Planta, 2002, vol. 215, pp. 239–247.

    Article  PubMed  CAS  Google Scholar 

  85. Groeneveld, R.A., Ansink, E., van de Wiel, C.C.M., and Wesseler, J., Benefits and costs of biologically contained genetically modified tomatoes and eggplants in Italy and Spain, Sustainability, 2011, vol. 3, pp. 1265–1281.

    Article  Google Scholar 

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Correspondence to G. V. Shpakovskii.

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Original Russian Text © M.R. Khaliluev, G.V. Shpakovskii, 2013, published in Fiziologiya Rastenii, 2013, Vol. 60, No. 6, pp. 763–775.

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Khaliluev, M.R., Shpakovskii, G.V. Genetic engineering strategies for enhancing tomato resistance to fungal and bacterial pathogens. Russ J Plant Physiol 60, 721–732 (2013). https://doi.org/10.1134/S1021443713050087

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