Planta

, Volume 233, Issue 5, pp 895–910 | Cite as

Nicotiana tabacum overexpressing γ-ECS exhibits biotic stress tolerance likely through NPR1-dependent salicylic acid-mediated pathway

  • Srijani Ghanta
  • Dipto Bhattacharyya
  • Ragini Sinha
  • Anindita Banerjee
  • Sharmila Chattopadhyay
Original Article

Abstract

The elaborate networks and the crosstalk of established signaling molecules like salicylic acid (SA), jasmonic acid (JA), ethylene (ET), abscisic acid (ABA), reactive oxygen species (ROS) and glutathione (GSH) play key role in plant defense response. To obtain further insight into the mechanism through which GSH is involved in this crosstalk to mitigate biotic stress, transgenic Nicotiana tabacum overexpressing Lycopersicon esculentum gamma-glutamylcysteine synthetase (LeECS) gene (NtGB lines) were generated with enhanced level of GSH in comparison with wild-type plants exhibiting resistance to pathogenesis as well. The expression levels of non-expressor of pathogenesis-related genes 1 (NPR1)-dependent genes like pathogenesis-related gene 1 (NtPR1), mitogen-activated protein kinase kinase (NtMAPKK), glutamine synthetase (NtGLS) were significantly enhanced alongwith NtNPR1. However, the expression levels of NPR1-independent genes like NtPR2, NtPR5 and short-chain dehydrogenase/reductase family protein (NtSDRLP) were either insignificant or were downregulated. Additionally, increase in expression of thioredoxin (NtTRXh), S-nitrosoglutathione reductase 1 (NtGSNOR1) and suppression of isochorismate synthase 1 (NtICS1) was noted. Comprehensive analysis of GSH-fed tobacco BY2 cell line in a time-dependent manner reciprocated the in planta results. Better tolerance of NtGB lines against biotrophic Pseudomonas syringae pv. tabaci was noted as compared to necrotrophic Alternaria alternata. Through two-dimensional gel electrophoresis (2-DE) and image analysis, 48 differentially expressed spots were identified and through identification as well as functional categorization, ten proteins were found to be SA-related. Collectively, our results suggest GSH to be a member in cross-communication with other signaling molecules in mitigating biotic stress likely through NPR1-dependent SA-mediated pathway.

Keywords

Biotic stress Glutathione Nicotiana tabacum NPR1 Salicylic acid Transgenic plants 

Abbreviations

ET

Ethylene

GSH

Glutathione

JA

Jasmonic acid

NPR1

Non-expressor of pathogenesis-related genes 1

PR

Pathogenesis-related protein gene

ROS

Reactive oxygen species

SA

Salicylic acid

Supplementary material

425_2011_1349_MOESM1_ESM.doc (618 kb)
Supplementary material 1 (DOC 618 kb)

References

  1. Ball L, Accotto GP, Bechtold U, Creissen G, Funck D, Jimenez A, Kular B, Leyland N, Mejia-Carranza J, Reynolds H, Karpins S, Mullineaux PM (2004) Evidence for a direct link between glutathione biosynthesis and stress defense gene expression in Arabidopsis. Plant Cell 16:2448–2462PubMedCentralPubMedCrossRefGoogle Scholar
  2. Banerjee A, Chattopadhyay S (2010) Effect of over-expression of Linum usitatissimum PINORESINOL LARICIRESINOL REDUCTASE (LuPLR) gene in transgenic Phyllanthus amarus. Plant Cell Tissue Organ Cult 103:315–323CrossRefGoogle Scholar
  3. Beak D, Pathange P, Chung JS, Jiang J, Gao L, Oikawa A, Hirai MY, Saito K, Pare PW, Shi H (2010) A stress-inducible sulphotransferase sulphonates salicylic acid and confers pathogen resistance in Arabidopsis. Plant Cell Environ 33:1383–1392Google Scholar
  4. Bjellqvist B, Hughes GJ, Pasquali C, Paquet N, Ravier F, Sanchez JC, Frutiger S, Hochstrasser D (1993) The focusing positions of polypeptides in immobilized pH gradients can be predicted from their amino acid sequences. Electrophoresis 14:1023–1031PubMedCrossRefGoogle Scholar
  5. Blanco F, Salinas P, Cecchini NM, Jordana X, Van Hummelen P, Alvarez ME, Holuigue L (2009) Early genomic responses to salicylic acid in Arabidopsis. Plant Mol Biol 70:79–102PubMedCrossRefGoogle Scholar
  6. Bolter C, Brammall RA, Cohen R, Lazarovits G (1993) Glutathione alterations in melon and tomato roots following treatment with chemicals which induce disease resistance to Fusarium wilt. Physiol Mol Plant Pathol 42:321–336CrossRefGoogle Scholar
  7. Bowling SA, Clarke JD, Liu Y, Klessig DF, Dong X (1997) The cpr5 mutant of Arabidopsis expresses both NPR1-dependent and NPR1-independent resistance. Plant Cell 9:1573–1584PubMedCentralPubMedGoogle Scholar
  8. Bradford M (1976) A rapid and sensitive method for the quantification of microgram quantities of protein utilizing the principle of protein–dye binding. Anal Biochem 72:248–254PubMedCrossRefGoogle Scholar
  9. Bradley DJ, Kjellbom P, Lamb CJ (1992) Elicitor- and wound-induced oxidative cross-linking of a proline-rich plant cell wall protein: a novel, rapid defense response. Cell 70:21–30PubMedCrossRefGoogle Scholar
  10. Cao H, Bowling SA, Gordon AS, Dong X (1994) Characterization of an Arabidopsis mutant that is nonresponsive to inducers of systemic acquired resistance. Plant Cell 6:1583–1592PubMedCentralPubMedGoogle Scholar
  11. Cao H, Glazebrook J, Clarke JD, Volko S, Dong X (1997) The Arabidopsis NPR1 gene that controls systemic acquired resistance encodes a novel protein containing ankyrin repeats. Cell 88:57–63PubMedCrossRefGoogle Scholar
  12. Chen Z, Silva H, Klessig DF (1993) Active oxygen species in the induction of plant systemic acquired resistance by salicylic acid. Science 262:1883–1886PubMedCrossRefGoogle Scholar
  13. Clarke JD, Liu Y, Klessig DF, Dong X (1998) Uncoupling PR gene expression from NPR1 and bacterial resistance: characterization of the dominant Arabidopsis cpr6-1 mutant. Plant Cell 10:557–569PubMedCentralPubMedGoogle Scholar
  14. Creissen G, Firmin J, Fryer M, Kular B, Leyland N, Reynolds H, Pastori G, Wellburn F, Baker N, Wellburn A, Mullineaux P (1999) Elevated glutathione biosynthetic capacity in the chloroplasts of transgenic tobacco plants paradoxically causes increased oxidative stress. Plant Cell 11:1277–1291PubMedCentralPubMedGoogle Scholar
  15. De Vos M, Van Zaanen W, Koornneef A, Korzelius JP, Dicke M, Van Loon LC, Pieterse CMJ (2006) Herbivore-induced resistance against microbial pathogens in Arabidopsis. Plant Physiol 142:352–363PubMedCentralPubMedCrossRefGoogle Scholar
  16. Delaney T, Friedrich L, Ryals J (1995) Arabidopsis signal transduction mutant defective in chemically and biologically induced disease resistance. Proc Natl Acad Sci USA 92:6602–6606PubMedCrossRefGoogle Scholar
  17. Després C, Chubak C, Rochon A, Clark R, Bethune T, Desveaux D, Fobert PR (2003) The Arabidopsis NPR1 disease resistance protein is a novel cofactor that confers redox regulation of DNA binding activity to the basic domain/leucine zipper transcription factor TGA1. Plant Cell 15:2181–2191PubMedCentralPubMedCrossRefGoogle Scholar
  18. Dron M, Clouse SD, Dixon RA, Lawton MA, Lamb CJ (1988) Glutathione and fungal elicitor regulation of a plant defense gene promoter in electroporated protoplasts. Proc Natl Acad Sci USA 85:6738–6742PubMedCrossRefGoogle Scholar
  19. Du L, Ali GS, Simons KA, Hou J, Yang T, Reddy ASN, Poovaiah BW (2009) Ca2+/calmodulin regulates salicylic-acid-mediated plant immunity. Nature 457:1154–1158PubMedCrossRefGoogle Scholar
  20. El-Zahaby HM, Gullner G, Kiraly Z (1995) Effects of powdery mildew infection of barley on the ascorbate–glutathione cycle and other antioxidants in different host–pathogen interactions. Phytopathol 85:1225–1230CrossRefGoogle Scholar
  21. Foyer CH, Lopez-Delgado H, Dat JF, Schott IM (1997) Hydrogen peroxide- and glutathione-associated mechanisms of acclamatory stress tolerance and signalling. Physiol Plant 100:241–254CrossRefGoogle Scholar
  22. Freeman JL, Garcia D, Kim D, Hopf A, Salt DE (2005) Constitutively elevated salicylic acid signals glutathione-mediated nickel tolerance in Thlaspi nickel hyperaccumulators. Plant Physiol 137:1082–1091PubMedCentralPubMedCrossRefGoogle Scholar
  23. Gasteiger E, Hoogland C, Gattiker A, Duvaud S, Wilkins MR, Appel RD, Bairoch A (2005) Protein identification and analysis tools on the expasy server. In: Walker JM (ed) The proteomics protocols handbook. Humana Press, pp 571–607Google Scholar
  24. Glazebrook J (2001) Genes controlling expression of defense responses in Arabidopsis: 2001 status. Curr Opin Plant Biol 4:301–308PubMedCrossRefGoogle Scholar
  25. Glazebrook J (2005) Contrasting mechanisms of defense against biotrophic and necrotrophic pathogens. Annu Rev Phytopathol 43:205–227PubMedCrossRefGoogle Scholar
  26. Glazebrook J, Ausubel FM (1994) Isolation of phytoalexin-deficient mutants of Arabidopsis thaliana and characterization of their interactions with bacterial pathogens. Proc Natl Acad Sci USA 91:8955–8959PubMedCrossRefGoogle Scholar
  27. Glazebrook J, Rogers EE, Ausubel FM (1996) Isolation of Arabidopsis mutants with enhanced disease susceptibility by direct screening. Genetics 143:973–982PubMedGoogle Scholar
  28. Glazebrook J, Zook M, Merrit F, Kagan I, Rogers EE, Crute IR, Holub EB, Hammerschmidt R, Ausubel FM (1997) Phytoalexin-deficient mutants of Arabidopsis reveal that PAD4 encodes a regulatory factor and that four PAD genes contribute to downy mildew resistance. Genetics 146:381–392PubMedGoogle Scholar
  29. Gomez LD, Noctor G, Knight MR, Foyer CH (2004) Regulation of calcium signaling and gene expression by glutathione. J Exp Bot 55:1851–1859PubMedCrossRefGoogle Scholar
  30. Görlach J, Volrath S, Knauf-Beiter G, Hengy G, Beckhove U, Kogel KH, Oostendorp M, Staub T, Ward E, Kessmann H, Ryals J (1996) Benzothiadiazole, a novel class of inducers of systemic acquired resistance, activates gene expression and disease resistance in wheat. Plant Cell 8:629–643PubMedCentralPubMedGoogle Scholar
  31. Grant M, Jones J (2009) Hormone (dis)harmony moulds plant health and disease. Science 324:750–752PubMedCrossRefGoogle Scholar
  32. Gullner G, Komives T, Rennenberg H (2001) Enhanced tolerance of transgenic poplar plants overexpressing γ-glutamylcysteine synthetase towards chloroacetanilide herbicides. J Exp Bot 52:971–979PubMedCrossRefGoogle Scholar
  33. Hell R, Bergmann L (1990) γ-Glutamylcysteine synthetase in higher plants: catalytic properties and subcellular localization. Planta 180:603–612PubMedCrossRefGoogle Scholar
  34. Herschbach C, van der Zalm E, Schneider A, Jouanin L, De Kok LJ, Rennenberg H (2000) Regulation of sulfur nutrition in wild-type and transgenic poplar over-expressing γ-glutamylcysteine synthetase in the cytosol as affected by atmospheric H2S. Plant Physiol 124:461–473PubMedCentralPubMedCrossRefGoogle Scholar
  35. Isaacson T, Damasceno CMB, Saravanan RS, He Y, Catalá C, Saladié M, Rose JKC (2006) Sample extraction techniques for enhanced proteomic analysis of plant tissues. Nat Protoc 1:769–774PubMedCrossRefGoogle Scholar
  36. Ishikawa K, Yoshimura K, Harada K, Fukusaki E, Ogawa T, Tamoi M, Shigeoka S (2010) AtNUDX6, an ADP-ribose/NADH pyrophosphohydrolase in Arabidopsis, positively regulates NPR1-dependent salicylic acid signalling. Plant Physiol 152:2000–2012PubMedCentralPubMedCrossRefGoogle Scholar
  37. Jang EK, Min KH, Kim SH, Nam SH, Zhang S, Kim YC, Cho BH, Yang KY (2009) Mitogen-activated protein kinase cascade in the signaling for polyamine biosynthesis in tobacco. Plant Cell Physiol 50:658–664PubMedCrossRefGoogle Scholar
  38. Kanehisa M, Goto S (2000) KEGG: kyoto encyclopedia of genes and genomes. Nucleic Acids Res 28:27–30PubMedCentralPubMedCrossRefGoogle Scholar
  39. Kocsy G, Szalai G, Vagujfalvi A, Stehli L, Orosz G, Galiba G (2000) Genetic study of glutathione accumulation during cold hardening in wheat. Planta 210:295–301PubMedCrossRefGoogle Scholar
  40. Kumar A, Chakraborty A, Ghanta S, Chattopadhyay S (2009) Agrobacterium-mediated genetic transformation of mint with E. coli glutathione synthetase gene. Plant Cell Tissue Organ Cult 96:117–126CrossRefGoogle Scholar
  41. Laudert D, Weiler EW (1998) Allene oxide synthase: a major control point in Arabidopsis thaliana octadecanoid signalling. Plant J 15:675–684PubMedCrossRefGoogle Scholar
  42. Lawton KA, Potter SL, Uknes S, Ryals J (1994) Acquired resistance signal transduction in Arabidopsis is ethylene independent. Plant Cell 6:581–590PubMedCentralPubMedGoogle Scholar
  43. Leon-Reyes A, Van der Does D, De Lange ES, Delker C, Wasternack C, Van Wees SCM, Ritsema T, Pieterse CMJ (2010) Salicylate-mediated suppression of jasmonate-responsive gene expression in Arabidopsis is targeted downstream of the jasmonate biosynthesis pathway. Planta 232:1423–1432PubMedCentralPubMedCrossRefGoogle Scholar
  44. Liedschulte V, Wachter A, Zhigang A, Rausch T (2010) Exploiting plants for glutathione (GSH) production: uncoupling GSH synthesis from cellular controls results in unprecedented GSH accumulation. Plant Biotechnol J 8:1–14CrossRefGoogle Scholar
  45. Liu Y, Zhang S, Klessig DF (2000) Molecular cloning and characterization of a tobacco MAP kinase kinase that interacts with SIPK. Mol Plant Microbe Interact 13:118–124PubMedCrossRefGoogle Scholar
  46. Loake G, Grant M (2007) Salicylic acid in plant defence—the players and protagonists. Curr Opin Plant Biol 10:466–472PubMedCrossRefGoogle Scholar
  47. Matton DP, Constabel P, Brisson N (1990) Alcohol dehydrogenase gene expression in potato following elicitor and stress treatment. Plant Mol Biol 14:775–783PubMedCrossRefGoogle Scholar
  48. May MJ, Hammond-Kosack KE, Jones JDG (1996) Involvement of reactive oxygen species, glutathione metabolism, and lipid peroxidation in the Cf-gene-dependent defense response of tomato cotyledons induced by race-specific elicitors of Cladosporium fulvum. Plant Physiol 110:1367–1379PubMedCentralPubMedGoogle Scholar
  49. May MJ, Vernoux T, Leaver C, Van Montagu M, Inzé D (1998) Glutathione homeostasis in plants: implications for environmental sensing and plant development. J Exp Bot 49:649–667Google Scholar
  50. Mhamdi A, Hager J, Chaouch S, Queval G, Han Y, Taconnat L, Saindrenan P, Gouia H, Issakidis-Bourguet E, Renou JP, Noctor G (2010) Arabidopsis GLUTATHIONE REDUCTASE 1 plays a crucial role in leaf responses to intracellular H2O2 and in ensuring appropriate gene expression through both salicylic acid and jasmonic acid signaling pathways. Plant Physiol 153:1144–1160PubMedCentralPubMedCrossRefGoogle Scholar
  51. Mou Z, Fan W, Dong X (2003) Inducers of plant systemic acquired resistance regulate NPR1 function through redox changes. Cell 27:935–944CrossRefGoogle Scholar
  52. Mur LAJ, Kenton P, Atzorn R, Miersch O, Wasternack C (2006) The outcomes of concentration-specific interactions between salicylate and jasmonate signaling include synergy, antagonism, and oxidative stress leading to cell death. Plant Physiol 140:249–262PubMedCentralPubMedCrossRefGoogle Scholar
  53. Murashige T, Skoog F (1962) A revised medium for rapid growth and bioassays with tobacco tissue cultures. Physiol Plant 15:473–497CrossRefGoogle Scholar
  54. Nawrath C, Métraux JP (1999) Salicylic acid induction–deficient mutants of Arabidopsis express PR-2 and PR-5 and accumulate high levels of camalexin after pathogen inoculation. Plant Cell 11:1393–1404PubMedCentralPubMedGoogle Scholar
  55. Neuhoff V, Arold N, Taube D (1988) Improved staining of proteins in polyacrylamide gels including isoelectric-focusing gels with clear background at nanogram sensitivity using Coomassie Brilliant Blue G-250 and R-250. Electrophoresis 9:255–262PubMedCrossRefGoogle Scholar
  56. Noctor G, Arisi ACM, Jouanin L, Foyer CH (1998) Manipulation of glutathione and amino acid biosynthesis in the chloroplast. Plant Physiol 118:471–482PubMedCentralPubMedCrossRefGoogle Scholar
  57. Pageau K, Reisdorf-Cren M, Morot-Gaudry JF, Masclaux-Daubresse C (2006) The two senescence-related markers GS1 (cytosolic glutamine synthetase) and GDH (glutamate dehydrogenase), involved in nitrogen mobilisation are differentially regulated during pathogen attack, by stress hormones and reactive oxygen species in Nicotiana tabacum L. leaves. J Exp Bot 57:547–557PubMedCrossRefGoogle Scholar
  58. Parisy V, Poinssot B, Owsianowski L, Buchala A, Glazebrook J, Mauch F (2007) Identification of PAD2 as a γ-glutamylcysteine synthetase highlights the importance of glutathione in disease resistance of Arabidopsis. Plant J 49:159–172PubMedCrossRefGoogle Scholar
  59. Pasternak M, Lim B, Wirtz M, Hell R, Cobbett CS, Meyer AJ (2008) Restricting glutathione biosynthesis to the cytosol is sufficient for normal plant development. Plant J 53:999–1012PubMedCrossRefGoogle Scholar
  60. Pérez-García A, Cánovas FM, Gallardo F, Hirel B, de Vicente A (1995) Differential expression of glutamine synthetase isoforms in tomato detached leaflets infected with Pseudomonas syringae pv. tomato. Mol Plant Microbe Interact 8:96–103CrossRefGoogle Scholar
  61. Pieterse CMJ, Van Loon LC (2004) NPR1: the spider in the web of induced resistance signaling pathways. Curr Opin Plant Biol 7:456–464PubMedCrossRefGoogle Scholar
  62. Pieterse CMJ, Leon-Reyes A, Van der Ent S, Van Wees SCM (2009) Networking by small-molecule hormones in plant immunity. Nat Chem Biol 5:308–316PubMedCrossRefGoogle Scholar
  63. Rogers EE, Ausubel FM (1997) Arabidopsis enhanced disease susceptibility mutants exhibit enhanced susceptibility to several bacterial pathogens and alterations in PR-1 gene expression. Plant Cell 9:305–316PubMedCentralPubMedGoogle Scholar
  64. Ruiz JM, Blumwald E (2002) Salinity-induced glutathione synthesis in Brassica napus. Planta 214:965–969PubMedCrossRefGoogle Scholar
  65. Ryang SH, Chung SY, Lee SH, Cha JS, Kim HY, Cho TJ (2002) Isolation of pathogen-induced Chinese cabbage genes by subtractive hybridization employing selective adaptor ligation. Biochem Biophys Res Commun 299:352–359PubMedCrossRefGoogle Scholar
  66. Sambrook J, Russell D (2001) Molecular cloning: a laboratory manual, 3rd edn. Cold Spring Harbor Laboratory Press, New YorkGoogle Scholar
  67. Shah J, Tsui F, Klessig DF (1997) Characterization 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 10:69–78PubMedCrossRefGoogle Scholar
  68. Sinha R, Chattopadhyay S (2010) Changes in the leaf proteome profile of Mentha arvensis in response to Alternaria alternata infection. J Prot. doi:10.1016/j.jprot.2010.11.009
  69. Slaymaker DH, Navarre DA, Clark D, del Pozo O, Martin GB, Klessig DF (2002) The tobacco salicylic acid-binding protein 3 (SABP3) is the chloroplast carbonic anhydrase, which exhibits antioxidant activity and plays a role in the hypersensitive defense response. Proc Natl Acad Sci USA 99:11640–11645PubMedCrossRefGoogle Scholar
  70. Snyman M, Cronjé MJ (2008) Modulation of heat shock factors accompanies salicylic acid-mediated potentiation of Hsp70 in tomato seedlings. J Exp Bot 59:2125–2132PubMedCrossRefGoogle Scholar
  71. Spoel SH, Koornneef A, Claessens SMC, Korzelius JP, Van Pelt JA, Mueller MJ, Buchala AJ, Me′traux J-P, Brown R, Kazan K, Van Loon LC, Dong X, Pieterse CMJ (2003) NPR1 modulates crosstalk between salicylate- and jasmonate-dependent defense pathways through a novel function in the cytosol. Plant Cell 15:760–770PubMedCentralPubMedCrossRefGoogle Scholar
  72. Tada T, Spoel SH, Pajerowska-Mukhtar K, Mou Z, Song J, Wang C, Zuo J, Dong X (2008) Plant immunity requires conformational changes of NPR1 via S-nitrosylation and thioredoxins. Science 321:952–956PubMedCrossRefGoogle Scholar
  73. Thomma B, Eggermont K, Penninckx I, Mauch-Mani B, Vogelsang R, Cammue B, Broekaert W (1998) Separate jasmonate-dependent and salicylate-dependent defense-response pathways in Arabidopsis are essential for resistance to distinct microbial pathogens. Proc Natl Acad Sci USA 95:15107–15111PubMedCrossRefGoogle Scholar
  74. Tsakraklides G, Martin M, Chalam R, Tarczynski MC, Schmidt A, Leustek T (2002) Sulfate reduction is increased in transgenic Arabidopsis thaliana expressing 5′-adenylylsulfate reductase from Pseudomonas aeruginosa. Plant J 32:879–889PubMedCrossRefGoogle Scholar
  75. Tuteja N, Mahajan S (2007) Further characterization of calcineurin B-like protein and its interacting partner CBL-interacting protein kinase from Pisum sativum. Plant Signal Behav 2:358–361PubMedCentralPubMedCrossRefGoogle Scholar
  76. Uknes S, Mauch-Mani B, Moyer M, Potter S, Williams S, Dincher S, Chandler D, Slusarenko A, Ward E, Ryals J (1992) Acquired resistance in Arabidopsis. Plant Cell 4:645–656PubMedCentralPubMedGoogle Scholar
  77. Van Loon LC, Rep M, Pieterse CMJ (2006) Significance of inducible defense-related proteins in infected plants. Annu Rev Phytopathol 44:135–162PubMedCrossRefGoogle Scholar
  78. Van Wees SCM, De Swart EAM, Van Pelt JA, Van Loon LC, Pieterse CMJ (2000) Enhancement of induced disease resistance by simultaneous activation of salicylate- and jasmonate-dependent defense pathways in Arabidopsis thaliana. Proc Natl Acad Sci USA 97:8711–8716PubMedCrossRefGoogle Scholar
  79. Verberne MC, Verpoorte R, Bol JF, Mercado-Blanco J, Linthorst HJM (2000) Overproduction of salicylic acid in plants by bacterial transgenes enhances pathogen resistance. Nat Biotechnol 18:779–783PubMedCrossRefGoogle Scholar
  80. Wang B, Wang Y, Wang Q, Luo G, Zhang Z, He C, He SJ, Zhang J, Gai J, Chen S (2004) Characterization of an NBS-LRR resistance gene homologue from soybean. J Plant Physiol 161:815–822PubMedCrossRefGoogle Scholar
  81. Wildermuth MC, Dewdney J, Wu G, Ausubel FM (2001) Isochorismate synthase is required to synthesize salicylic acid for plant defence. Nature 414:562–571PubMedCrossRefGoogle Scholar
  82. Wingate VMP, Lawton MA, Lamb CJ (1988) Glutathione causes a massive and selective induction of plant defense genes. Plant Physiol 87:206–210PubMedCentralPubMedCrossRefGoogle Scholar
  83. Xiang C, Werner BL, Christensen EM, Oliver DJ (2001) The biological functions of glutathione revisited in Arabidopsis transgenic plants with altered glutathione levels. Plant Physiol 126:564–574PubMedCentralPubMedCrossRefGoogle Scholar
  84. Yoshida S, Tamaoki M, Ioki M, Ogawa D, Sato Y, Aono M, Kubo A, Saji S, Saji H, Satoh S, Nakajima N (2009) Ethylene and salicylic acid control glutathione biosynthesis in ozone-exposed Arabidopsis thaliana. Physiol Plant 136:284–298PubMedCrossRefGoogle Scholar
  85. Zhang X, Mou Z (2009) Extracellular pyridine nucleotides induce PR gene expression and disease resistance in Arabidopsis. Plant J 57:302–312PubMedCrossRefGoogle Scholar
  86. Zhang YL, Fan WH, Kinkema M, Li X, Dong X (1999) Interaction 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 96:6523–6528PubMedCrossRefGoogle Scholar
  87. Zhang G, Chen M, Li L, Xu Z, Chen X, Guo J, Ma Y (2009a) Overexpression of the soybean GmERF3 gene, an AP2/ERF type transcription factor for increased tolerances to salt, drought, and diseases in transgenic tobacco. J Exp Bot 60:3781–3796PubMedCrossRefGoogle Scholar
  88. Zhang X, Chen S, Mou Z (2009b) Nuclear localization of NPR1 is required for regulation of salicylate tolerance, isochorismate synthase 1 expression and salicylate accumulation in Arabidopsis. J Plant Physiol 167:144–148CrossRefGoogle Scholar
  89. Zhou N, Tootle TL, Tsui F, Klessig DF, Glazebrook J (1998) PAD4 functions upstream from salicylic acid to control defense responses in Arabidopsis. Plant Cell 10:1021–1030PubMedCentralPubMedGoogle Scholar
  90. Zhou JM, Trifa Y, Silva H, Pontier D, Lam E, Shah J, Klessig DF (2000) NPR1 diffrerentially 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 13:191–202PubMedCrossRefGoogle Scholar
  91. Zhu YL, Pilon-Smits EAH, Tarun AS, Weber SU, Jouanin L, Terry N (1999) Cadmium tolerance and accumulation in Indian mustard is enhanced by overexpressing γ-glutamylcysteine synthetase. Plant Physiol 121:1169–1177PubMedCentralPubMedCrossRefGoogle Scholar
  92. Ziadi S, Poupard P, Brisset M, Paulin JP, Simoneau P (2001) Characterization in apple leaves of two subclasses of PR-10 transcripts inducible by acibenzolar-S-methyl, a functional analogue of salicylic acid. Physiol Mol Plant Pathol 59:33–43CrossRefGoogle Scholar
  93. Zielinski RE (1998) Calmodulin and calmodulin-binding proteins in plants. Annu Rev Plant Physiol Plant Mol Biol 49:697–725PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2011

Authors and Affiliations

  • Srijani Ghanta
    • 1
  • Dipto Bhattacharyya
    • 1
  • Ragini Sinha
    • 1
  • Anindita Banerjee
    • 1
  • Sharmila Chattopadhyay
    • 1
  1. 1.Plant Biotechnology Laboratory, Drug Development/Diagnostics and Biotechnology DivisionIndian Institute of Chemical Biology (A unit of Council of Scientific and Industrial Research)KolkataIndia

Personalised recommendations