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Transgenic tomato plants expressing the Arabidopsis NPR1 gene display enhanced resistance to a spectrum of fungal and bacterial diseases

Abstract

Development of effective disease-resistance to a broad-range of pathogens in crops usually requires tremendous resources and effort when traditional breeding approaches are taken. Genetic engineering of disease-resistance in crops has become popular and valuable in terms of cost and efficacy. Due to long-lasting and broad-spectrum of effectiveness against pathogens, employment of systemic acquired resistance (SAR) for the genetic engineering of crop disease-resistance is of particular interest. In this report, we explored the potential of using SAR-related genes for the genetic engineering of enhanced resistance to multiple diseases in tomato. The Arabidopsis NPR1 (nonexpresser of PR genes) gene was introduced into a tomato cultivar, which possesses heat-tolerance and resistance to tomato mosaic virus (ToMV). The transgenic lines expressing NPR1 were normal as regards overall morphology and horticultural traits for at least four generations. Disease screens against eight important tropical diseases revealed that, in addition to the innate ToMV-resistance, the tested transgenic lines conferred significant level of enhanced resistance to bacterial wilt (BW) and Fusarium wilt (FW), and moderate degree of enhanced resistance to gray leaf spot (GLS) and bacterial spot (BS). Transgenic lines that accumulated higher levels of NPR1 proteins exhibited higher levels and a broader spectrum of enhanced resistance to the diseases, and enhanced disease-resistance was stably inherited. The spectrum and degree of these NPR1-transgenic lines are more significant compared to that of transgenic tomatoes reported to date. These transgenic lines may be further explored as future tomato stocks, aiming at building up resistance to a broader spectrum of diseases.

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References

  1. D Alexander RM Goodman M Gut-Rella C Glascock K Weymann L Friedrich D Maddox P Ahl-Goy T Luntz E Ward J Ryals (1993) ArticleTitleIncreased tolerance to two oomycete pathogens in transgenic tobacco expressing pathogenesis-related protein 1a Proc Natl Acad Sci USA 90 7327–7331

  2. G An (1987) ArticleTitleBinary Ti vectors for plant transformation and promoter analysis Methods Enzymol 153 292–305

  3. PD Bittner-Eddy JL Beynon (2001) ArticleTitleThe Arabidopsis downy mildew resistance gene, RPP13-Nd, functions independently of NDR1 and EDS1 and does not require the accumulation of salicylic acid Mol Plant Microbe Interact 14 416–421

  4. K Broglie I Chet M Holliday R Cressman P Biddle S Knowlton CJ Mauvais R Broglie (1991) ArticleTitleTransgenic plants with enhanced resistance to the fungal pathogen Rhizoctonia solani. Science 254 1194–1197

  5. A Brunetti M Tavazza E Noris R Tavazza P Caciagli G Ancora S Crespi GP Accotto (1997) ArticleTitleHigh expression of truncated viral rep protein confers resistance to tomato yellow leaf curl virus in transgenic tomato plants Mol Plant Microbe Interact 10 571–579

  6. H Cao SA Bowling AS Gordon X Dong (1994) ArticleTitleCharacterization of an Arabidopsis mutant that is nonresponsive to inducers of systemic acquired resistance Plant Cell 6 1583–1592

  7. H Cao J Glazebrook JD Clarke S Volko X Dong (1997) ArticleTitleThe Arabidopsis NPR1 gene that controls systemic acquired resistance encodes a novel protein containing ankyrin repeats Cell 88 57–63

  8. H Cao X Li X Dong (1998) ArticleTitleGeneration of broad-spectrum disease resistance by overexpression of an essential regulatory gene in systemic acquired resistance Proc Natl Acad Sci USA 95 6531–6536

  9. MS Chern HA Fitzgerald RC Yadav PE Canlas X Dong PC Ronald (2001) ArticleTitleEvidence for a disease-resistance pathway in rice similar to the NPR1-mediated signaling pathway in Arabidopsis Plant J 27 101–113

  10. S Chivasa JP Carr (1998) ArticleTitleCyanide restores N gene-mediated resisance to tobacco mosaic virus in transgenic tobacco expressing salicylic acid hydroxylase Plant Cell 10 1489–1498

  11. JD Clarke Y Liu DF Klessig X Dong (1998) ArticleTitleUncoupling PR gene expression from NPR1 and bacterial resistance: characterization of the dominant Arabidopsis cpr6-1 mutant Plant Cell 10 557–569

  12. U Conrath CM Pieterse B Mauch-Mani (2002) ArticleTitlePriming in plant-pathogen interactions Trends Plant Sci 7 210–216

  13. Crill P, Strobel JW, Burgis DS, Bryan HH, John CA, Everett PH, Bartz JA, Hayslip NC and Deen WW (1971) Florida MH-1, Florida’s First Machine Harvest Fresh Market Tomato (p. 12), Circular S-212. Agricultural Experiment Station. University of Florida.

  14. TP Delaney L Friedrich H Kessmann S Uknes B Vernooij E Ward K Weymann J Ryals (1994) ArticleTitleThe molecular biology of systemic acquired resistance Curr Plant Sci Biotechnol Agric 21 339–347

  15. TP Delaney L Friedrich JA Ryals (1995) ArticleTitleArabidopsis signal transduction mutant defective in chemically and biologically induced disease resistance Proc Natl Acad Sci USA 92 6602–6606

  16. C Després C DeLong S Glaze E Liu PR Fobert (2000) ArticleTitleThe Arabidopsis NPR1/NIM1 protein enhances the DNA binding activity of a subgroup of the TGA family of bZIP transcription factors Plant Cell 12 279–290

  17. W Fan X Dong (2002) ArticleTitleIn vivo interaction between NPR1 and transcription factor TGA2 leads to salicylic acid-mediated gene activation in Arabidopsis Plant Cell 14 1377–1389

  18. JJ Fillatti J Kiser R Rose L Comai (1987) ArticleTitleEfficient transfer of a glyphosate tolerance gene into tomato using a binary Agrobacterium tumefaciens vector Bio/Technology 5 726–730

  19. L Friedrich K Lawton R Dietrich M Willits R Cade J Ryals (2001) ArticleTitleNIM1 overexpression in Arabidopsis potentiates plant disease resistance and results in enhanced effectiveness of fungicides Mol Plant Microbe Interact 14 1114–1124

  20. J Glazebrook EE Rogers FM Ausubel (1996) ArticleTitleIsolation of Arabidopsis mutants with enhanced disease susceptibility by direct screening Genetics 143 973–982

  21. A Gubba C Gonsalves MR Stevens DM Tricoli D Gonsalves (2002) ArticleTitleCombining transgenic and natural resistance to obtain broad resistance to tospovirus infection in tomato (Lycopersicon esculentum mill) Mol Breeding 9 13–23

  22. G Jach B Gornhardt J Mundy J Logemann E Pinsdorf R Leah J Schell C Maas (1995) ArticleTitleEnhanced quantitative resistance against fungal disease by combinatorial expression of different barley antifungal proteins in transgenic tobacco Plant J 8 97–109

  23. TL Jinn SH Wu CH Yeh MH Hsieh YC Yeh YM Chen CY Lin (1993) ArticleTitleImmunological kinship of class I low molecular weight heat shock proteins and thermostabilization of soluble proteins in vitro among plants Plant Cell Physiol 34 1055–1062

  24. E Jongedijk H Tigelaar Roekel JS van SA Bres-Vloemans I Dekker PJ Elzen Particlevan den BJ Cornelissen LS Melchers (1995) ArticleTitleSynergistic activity of chitinases and β-1,3-glucanases enhances fungal resistance in transgenic tomato plants Euphytica 85 173–180

  25. P Kachroo K Yoshioka J Shah HK Dooner DF Klessig (2000) ArticleTitleResistance to turnip crinkle virus in Arabidopsis is regulated by two host genes and is salicylic acid dependent but NPR1, ethylene, and jasmonate independent Plant Cell 12 677–690

  26. W Kaniewski V Ilardi L Tomassoli T Mitsky J Layton M Barba (1999) ArticleTitleExtreme resistance to cucumber mosaic virus (CMV) in transgenic tomato expressing one or two viral coat proteins Mol Breeding 5 111–119

  27. HS Kim TP Delaney (2002) ArticleTitleOver-expression of TGA5, which encodes a bZIP transcription factor that interacts with NIM1/NPR1, confers SAR-independent resistance in Arabidopsis thaliana to Peronospora parasitica Plant J 32 151–163

  28. M Kinkema W Fan X Dong (2000) ArticleTitleNuclear localization of NPR1 is required for activation of PR gene expression Plant Cell 12 2339–2350

  29. A Kohler S Schwindling U Conrath (2002) ArticleTitleBenzothiadiazole-induced priming for potentiated responses to pathogen infection, wounding, and infiltration of water into leaves requires the NPR1/NIM1 gene in Arabidopsis Plant Physiol 128 1046–1056

  30. TJ Lee DP Coyne TE Clemente A Mitra (2002) ArticleTitlePartial resistance to bacterial wilt in transgenic tomato plants expressing antibacterial Lactoferrin gene J Amer Soc Hort Sci 127 158–164

  31. L Li JC Steffens (2002) ArticleTitleOverexpression of polyphenol oxidase in transgenic tomato plants results in enhanced bacterial disease resistance Planta 215 239–247

  32. X Li JD Clarke Y Zhang X Dong (2001) ArticleTitleActivation of an EDS1-mediated R-gene pathway in the snc1 mutant leads to constitutive, NPR1-independent pathogen resistance Mol Plant Microbe Interact 14 1131–1139

  33. D Liu KG Raghothama PM Hasegawa RA Bressan (1994) ArticleTitleOsmotin overexpression in potato delays development of disease symptoms Proc Natl Acad Sci USA 91 1888–1892

  34. Y Liu M Schiff R Marathe SP Dinesh-Kumar (2002) ArticleTitleTobacco Rar1, EDS1 and NPR1/NIM1 like genes are required for N-mediated resistance to tobacco mosaic virus Plant J 30 415–429

  35. J Malamy JP Carr DF Klessig I Raskin (1990) ArticleTitleSalicylic acid: a likely endogenous signal in the resistance response of tobacco to viral infection Science 250 1002–1004

  36. JM McDowell A Cuzick C Can J Beynon JL Dangl EB Holub (2000) ArticleTitleDowny mildew (Peronospora parasitica) resistance genes in Arabidopsis vary in functional requirements for NDR1, EDS1, NPR1 and salicylic acid accumulation Plant J 22 523–529

  37. JP Métraux H Signer J Ryals E Ward M Wyss-Benz J Gaudin K Raschdorf E Schmid W Blum B Inverardi (1990) ArticleTitleIncrease in salicylic acid at the onset of systemic acquired resistance in cucumber Science 250 1004–1006

  38. Z Mou W Fan X Dong (2003) ArticleTitleInducers of plant systemic acquired resistance regulate NPR1 function through redox changes Cell 113 935–944

  39. AM Murphy S Chivasa DP Singh JP Carr (1999) ArticleTitleSalicylic acid-induced resistance to viruses and other pathogens: a parting of the ways Trends Plant Sci 4 155–160

  40. AM Murphy A Gilliland CE Wong J West DP Singh JP Carr (2001) ArticleTitleSignal transduction in resistance to plant viruses European Journal of Plant Pathology 107 121–128

  41. CM Pieterse Wees SC van Pelt JA van M Knoester R Laan H Gerrits PJ Weisbeek LC Loon Particlevan (1998) ArticleTitleA novel signaling pathway controlling induced systemic resistance in Arabidopsis Plant Cell 10 1571–1580

  42. GJ Rairdan TP Delaney (2002) ArticleTitleRole of salicylic acid and NIM1/NPR1 in race-specific resistance in Arabidopsis Genetics 161 803–811

  43. JB Rasmussen R Hammerschmidt MN Zook (1991) ArticleTitleSystemic induction of salicylic acid accumulation in cucumber after inoculation with Pseudomonas syringae pv syringae. Plant Physiol 97 1342–1347

  44. MM Robison S Shah B Tamot KP Pauls BA Moffatt BR Glick (2001) ArticleTitleReduced symptoms of Verticillium wilt in transgenic tomato expressing a bacterial ACC deaminase Mol Plant Pathology 2 135–145

  45. CM Rommens GM Kishore (2000) ArticleTitleExploiting the full potential of disease-resistance genes for agricultural use Curr Opin Biotechnol 11 120–125

  46. J Ryals K Weymann K Lawton L Friedrich D Ellis HY Steiner J Johnson TP Delaney T Jesse P Vos S Uknes (1997) ArticleTitleThe Arabidopsis NIM1 protein shows homology to the mammalian transcription factor inhibitor IκB Plant Cell 9 425–439

  47. JA Ryals UH Neuenschwander MG Willits A Molina HY Steiner MD Hunt (1996) ArticleTitleSystemic acquired resistance Plant Cell 8 1809–1819

  48. MA Saghai-Maroof KM Soliman RA Jorgensen RW Allard (1984) ArticleTitleRibosomal DNA spacer-length polymorphisms in barley: mendelian inheritance, chromosomal location, and population dynamics Proc Natl Acad Sci USA 81 8014–8018

  49. JM Salmeron B Vernooij (1998) ArticleTitleTrnasgenic approaches to microbial disease resistance in crop plants Curr Opin Plant Biology 1 347–352

  50. J Sambrook DW Russell (2001) Molecular Cloning. A Laboratory Manual EditionNumber3 Cold Spring Harbor Laboratory Press Cold Spring Harbor, New York

  51. DM Shah (1997) ArticleTitleGenetic engineering for fungal and bacterial disease Curr Opin Biotechnol 8 208–214

  52. J Shah F Tsui DF Klessig (1997) ArticleTitleCharacterization of a salicylic acid-insensitive mutant (sai1) of Arabidopsis thaliana, identified in a selective screen utilizing the SA-inducible expression of the tms2 gene Mol Plant Microbe Interact 10 69–78

  53. SL Shih JT Wang BT Chiang SK Green (1995) ArticleTitleDistribution of tomato leaf curl virus in Taiwan and its host range Plant protection Bulletin, R.O.C. 37 445

  54. Y Shirano P Kachroo J Shah DF Klessig (2002) ArticleTitleA gain-of-function mutation in an Arabidopsis toll interleukin1 receptor-nucleotide binding site-leucine-rich repeat type R gene triggers defense responses and results in enhanced disease resistance Plant Cell 14 3149–3162

  55. SH Spoel A Koornneef SM Claessens JP Korzelius Pelt JA van MJ Mueller AJ Buchala JP Metraux R Brown K Kazan LC Loon Particlevan X Dong CM Pieterse (2003) ArticleTitleNPR1 modulates cross-talk between salicylate- and jasmonate-dependent defense pathways through a novel function in the cytosol Plant Cell 15 760–770

  56. JR Stommel ME Tousignant T Wai R Pasini M. KJ (1998) ArticleTitleViral satellite RNA expression in transgenic tomato confers field tolerance to cucumber mosaic virus Plant Disease 82 391–396

  57. MH Stuiver JH Custers (2001) ArticleTitleEngineering disease resistance in plants Nature 411 865–868

  58. R Subramaniam D Desveaux C Spickler SW Michnick N Brisson (2001) ArticleTitleDirect visualization of protein interactions in plant cells Nature Biotechnol 19 769–772

  59. Z Tabaeizadeh Z Agharbaoui H Harrak V Poysa (1999) ArticleTitleTransgenic tomato plants expressing a Lycopersicon chilense chitinase gene demonstrate improved resistance to Verticillium dahliae race 2 Plant Cell Rep 19 197–202

  60. TH Tai D Dahlbeck ET Clark P Gajiwala R Pasion MC Whalen RE Stall BJ Staskawicz (1999) ArticleTitleExpression of the Bs2 pepper gene confers resistance to bacterial spot disease in tomato Proc Natl Acad Sci USA 96 14153–14158

  61. X Tang M Xie YJ Kim J Zhou DF Klessig GB Martin (1999) ArticleTitleOverexpression of Pto activates defense responses and confers broad resistance Plant Cell 11 15–30

  62. H Vanacker H Lu DN Rate JT Greenberg (2001) ArticleTitleA role for salicylic acid and NPR1 in regulating cell growth in Arabidopsis Plant J 28 209–216

  63. JF Wang P Hanson JA Barnes (1998) Worldwide evaluation of an international set of resistance sources to bacterial wilt in tomato C Allen J Elphinstone (Eds) Bacterial Wilt Disease. Molecular and Ecological Aspects Springer-Verlag Press Berlin 269–275

  64. Wang JF and Lin CH (2004) Colonization capacity of Ralstonia solanacearum tomato strains differing in aggressiveness on tomatoes and weeds. In: Allen C, Prior P and Hayward AC (eds). Bacterial Wilt: The Disease and the Ralstonia solanacearum Species Complex APS Press, St Paul (in press).

  65. JF Wang J Olivier P Thoquet B Mangin L Sauviac NH Grimsley (2000) ArticleTitleResistance of tomato line Hawaii7996 to Ralstonia solanacearum Pss4 in Taiwan is controlled mainly by a major strain-specific locus Mol Plant Microbe Interact 13 6–13

  66. ER Ward SJ Uknes SC Williams SS Dincher DL Wiederhold DC Alexander P Ahl-Goy JP Metraux JA Ryals (1991) ArticleTitleCoordinate gene activity in response to agents that induce systemic acquired resistance Plant Cell 3 1085–1094

  67. S Whitham S McCormick B Baker (1996) ArticleTitleThe N gene of tobacco confers resistance to tobacco mosaic virus in transgenic tomato Proc Natl Acad Sci USA 93 8776–8781

  68. CE Wong RA Carson JP Carr (2002) ArticleTitleChemically induced virus resistance in Arabidopsis thaliana is independent of pathogenesis-related protein expression and the NPR1 gene Mol Plant Microbe Interact 15 75–81

  69. D Yu C Chen Z Chen (2001) ArticleTitleEvidence for an important role of WRKY DNA binding proteins in the regulation of NPR1 gene expression Plant Cell 13 1527–1539

  70. C Zhang AD Shapiro (2002) ArticleTitleTwo pathways act in an additive rather than obligatorily synergistic fashion to induce systemic acquired resistance and PR gene expression BMC Plant Biol 2 9

  71. Y Zhang W Fan M Kinkema X Li X Dong (1999) ArticleTitleInteraction of NPR1 with basic leucine zipper protein transcription factors that bind sequences required for salicylic acid induction of the PR-1 gene Proc Natl Acad Sci USA 96 6523–6528

  72. JM Zhou Y Trifa H Silva D Pontier E Lam J Shah DF Klessig (2000) ArticleTitleNPR1 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 13 191–202

  73. Q Zhu EA Maher S Masoud RA Dixon C Lamb (1994) ArticleTitleEnhanced protection against fungal attack by constitutive co-expression of chitinase and glucanase genes in transgenic tobacco Bio/Technology 12 807–812

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Correspondence to Chiu-Ping Cheng.

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Lin, W., Lu, C., Wu, J. et al. Transgenic tomato plants expressing the Arabidopsis NPR1 gene display enhanced resistance to a spectrum of fungal and bacterial diseases. Transgenic Res 13, 567–581 (2004). https://doi.org/10.1007/s11248-004-2375-9

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Keywords

  • Arabidopsis NPR1
  • disease resistance
  • PR genes
  • tomato