Biological Elicitors of Plant Secondary Metabolites: Mode of Action and Use in the Production of Nutraceutics

  • Simone Ferrari
Part of the Advances in Experimental Medicine and Biology book series (AEMB, volume 698)

Abstract

Many secondary metabolites of interest for human health and nutrition are produced by plants when they are under attack of microbial pathogens or insects. Treatment with elicitors derived from phytopathogens can be an effective strategy to increase the yield of specific metabolites obtained from plant cell cultures. Understanding how plant cells perceive microbial elicitors and how this perception leads to the accumulation of secondary metabolites, may help us improve the production of nutraceutics in terms of quantity and of quality of the compounds. The knowledge gathered in the past decades on elicitor perception and transduction is now being combined to high-throughput methodologies, such as transcriptomics and metabolomics, to engineer plant cells that produce compounds of interest at industrial scale.

Keywords

Salicylic Acid Secondary Metabolite Jasmonic Acid Secondary Metabolism Oxidative Burst 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

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References

  1. 1.
    Wink M. Evolution of secondary metabolites from an ecological and molecular phylogenetic perspective. Phytochemistry 2003; 64:3–19.PubMedCrossRefGoogle Scholar
  2. 2.
    Morrissey JP, Osbourn AE. Fungal resistance to plant antibiotics as a mechanism of pathogenesis. Microbiol Mol Biol Rev 1999; 63:708–724.PubMedGoogle Scholar
  3. 3.
    Zhao J, Davis LC, Verpoorte R. Elicitor signal transduction leading to production of plant secondary metabolites. Biotechnology Advances 2005; 23:283–333.PubMedCrossRefGoogle Scholar
  4. 4.
    VanEtten HD, Mansfield JW, Bailey JA et al. Two Classes of Plant Antibiotics: Phytoalexins versus “Phytoanticipins”. Plant Cell 1994; 6:1191–1192.PubMedCrossRefGoogle Scholar
  5. 5.
    Hammerschmidt R, Dann EK. The role of phytoalexins in plant protection. Novartis Found Symp 1999; 223:175–187.PubMedGoogle Scholar
  6. 6.
    Müller KO, Borger H. Experimentelle untersuchungen über die phytophthorainfestans-resistenz der kartoffel. Arb Biol Reichsanst Land Forstwirtsch 1940; 23:189–231.Google Scholar
  7. 7.
    Müller KO. Studies on phytoalexins: I. The formation and the immunological significance of phytoalexin produced by Phaseolus vulgaris in response to infections with Sclerotinia fructicola and Phytophthora infestans. Aust J Biol Sci 1958; 11:275–300.Google Scholar
  8. 8.
    Paxton J. Phytoalexins—a working redefinition. Phytopathol Z 1981; 101:106–109.CrossRefGoogle Scholar
  9. 9.
    Lamb C, Dixon RA. The oxidative burst in plant disease resistance. Annu Rev Plant Physiol Plant Mol Biol 1997; 48:251–275.PubMedCrossRefGoogle Scholar
  10. 10.
    Zhong JJ. Biochemical engineering of the production of plant-specific secondary metabolites by cell suspension cultures. Adv Biochem Eng Biotechnol 2001; 72:1–26.PubMedCrossRefGoogle Scholar
  11. 11.
    Memelink J, Kijne JW, van der HR et al. Genetic modification of plant secondary metabolite pathways using transcriptional regulators. Adv Biochem Eng Biotechnol 2001; 72:103–125.PubMedGoogle Scholar
  12. 12.
    Sato F, Hashimoto T, Hachiya A et al. Metabolic engineering of plant alkaloid biosynthesis. Proc Natl Acad Sci USA 2001; 98:367–372.PubMedCrossRefGoogle Scholar
  13. 13.
    He P, Shan L, Sheen J. Elicitation and suppression of microbe-associated molecular pattern-triggered immunity in plant-microbe interactions. Cell Microbiol 2007; 9:1385–1396.PubMedCrossRefGoogle Scholar
  14. 14.
    Parker JE. Plant recognition of microbial patterns. Trends Plant Sci 2003; 8:245–247.PubMedCrossRefGoogle Scholar
  15. 15.
    Nurnberger T, Brunner F, Kemmerling B et al. Innate immunity in plants and animals: striking similarities and obvious differences. Immunol Rev 2004; 198:249–266.PubMedCrossRefGoogle Scholar
  16. 16.
    Granado J, Felix G, Boller T. Perception of Fungal Sterols in Plants (Subnanomolar Concentrations of Ergosterol Elicit Extracellular Alkalinization in Tomato Cells). Plant Physiol 1995; 107:485–490.PubMedGoogle Scholar
  17. 17.
    Menke FL, Parchmann S, Mueller MJ et al. Involvement of the octadecanoid pathway and protein phosphorylation in fungal elicitor-induced expression of terpenoid indole alkaloid biosynthetic genes in catharanthus roseus. Plant Physiol 1999; 119:1289–1296.PubMedCrossRefGoogle Scholar
  18. 18.
    Nurnberger T, Brunner F. Innate immunity in plants and animals: emerging parallels between the recognition of general elicitors and pathogen-associated molecular patterns. Curr Opin Plant Biol 2002; 5:318–324.PubMedCrossRefGoogle Scholar
  19. 19.
    Kessler A, Baldwin IT. Plant responses to insect herbivory: the emerging molecular analysis. Annu Rev Plant Biol 2002; 53:299–328.PubMedCrossRefGoogle Scholar
  20. 20.
    Schmelz EA, Carroll MJ, Leclere S et al. Fragments of ATP synthase mediate plant perception of insect attack. Proc Natl Acad Sci USA 2006; 103:8894–8899.PubMedCrossRefGoogle Scholar
  21. 21.
    Sirvent TM, Krasnoff SB, Gibson DM. Induction of hypericins and hyperforins in Hypericum perforatum in response to damage by herbivores. J Chem Ecol 2003; 29:2667–2681.PubMedCrossRefGoogle Scholar
  22. 22.
    Turlings TC, Loughrin JH, McCall PJ et al. How caterpillar-damaged plants protect themselves by attracting parasitic wasps. Proc Natl Acad Sci USA 1995; 92:4169–4174.PubMedCrossRefGoogle Scholar
  23. 23.
    McGurl B, Pearce G, Orozco Cardenas M et al. Structure, expression and antisense inhibition of the systemin precursor gene. Science 1992; 255:1570–1573.PubMedCrossRefGoogle Scholar
  24. 24.
    Doares SH, Syrovets T, Weiler EW et al. Oligogalacturonides and chitosan activate plant defensive genes through the octadecanoid pathway. Proc Natl Acad Sci USA 1995; 92:4095–4098.PubMedCrossRefGoogle Scholar
  25. 25.
    McGurl B, Pearce G, Ryan CA. Polypeptide signalling for plant defence genes. Biochem Soc Symp 1994; 60:149–154.PubMedGoogle Scholar
  26. 26.
    Constabel CP, Bergey DR, Ryan CA. Systemin activates synthesis of wound-inducible tomato leaf polyphenol oxidase via the octadecanoid defense signaling pathway. Proc Natl Acad Sci USA 1995; 92:407–411.PubMedCrossRefGoogle Scholar
  27. 27.
    Funk C, Brodelius P. Phenylpropanoid metabolism in suspension cultures of vanilla planifolia andr: IV. Induction of vanillic acid formation. Plant Physiol 1992;99(1):256–262.PubMedCrossRefGoogle Scholar
  28. 28.
    Lo SC, Nicholson RL. Reduction of light-induced anthocyanin accumulation in inoculated sorghum mesocotyls. Implications for a compensatory role in the defense response. Plant Physiol 1998; 116:979–989.PubMedCrossRefGoogle Scholar
  29. 29.
    Gomez-Gomez L, Boller T. FLS2: an LRR receptor-like kinase involved in the perception of the bacterial elicitor flagellin in Arabidopsis. Mol Cell 2000; 5:1003–1011.PubMedCrossRefGoogle Scholar
  30. 30.
    Chinchilla D, Bauer Z, Regenass M et al. The Arabidopsis receptor kinase FLS2 binds flg22 and determines the specificity of flagellin perception. Plant Cell 2006; 18:465–476.PubMedCrossRefGoogle Scholar
  31. 31.
    Zipfel C, Kunze G, Chinchilla D et al. Perception of the bacterial PAMP EF-Tu by the receptor EFR restricts Agrobacterium-mediated transformation. Cell 2006; 125:749–760.PubMedCrossRefGoogle Scholar
  32. 32.
    Kaku H, Nishizawa Y, Ishii-Minami N et al. Plant cells recognize chitin fragments for defense signaling through a plasma membrane receptor. Proc Natl Acad Sci USA 2006; 103:11086–11091.PubMedCrossRefGoogle Scholar
  33. 33.
    Scheer JM Ryan CA Jr. The systemin receptor SR160 from Lycopersicon peruvianum is a member of the LRR receptor kinase family. Proc Natl Acad Sci USA 2002; 99:9585–9590.PubMedCrossRefGoogle Scholar
  34. 34.
    Ji C, Okinaka Y, Takeuchi Y et al. Specific Binding of the Syringolide Elicitors to a Soluble Protein Fraction from Soybean Leaves. Plant Cell 1997; 9:1425–1433.PubMedCrossRefGoogle Scholar
  35. 35.
    Garcia-Brugger A, Lamotte O, Vandelle E et al. Early signaling events induced by elicitors of plant defenses. Mol Plant Microbe Interact 2006; 19:711–724.PubMedCrossRefGoogle Scholar
  36. 36.
    Bolwell GP, Bindschedler LV, Blee KA et al. The apoplastic oxidative burst in response to biotic stress in plants: a three-component system. J Exp Bot 2002; 53:1367–1376.PubMedCrossRefGoogle Scholar
  37. 37.
    Doke N, Miura Y, Sanchez LM et al. The oxidative burst protects plants against pathogen attack: mechanism and role as an emergency signal for plant bio-defence—a review. Gene 1996; 179:45–51.PubMedCrossRefGoogle Scholar
  38. 38.
    Mahady GB, Liu C, Beecher CW. Involvement of protein kinase and G proteins in the signal transduction of benzophenanthridine alkaloid biosynthesis. Phytochemistry 1998; 48:93–102.PubMedCrossRefGoogle Scholar
  39. 39.
    Rajasekhar VK, Lamb C, Dixon RA. Early events in the signal pathway for the oxidative burst in soybean cells exposed to avirulent pseudomonas syringae pv glycinea. Plant Physiol 1999; 120:1137–1146.PubMedCrossRefGoogle Scholar
  40. 40.
    Zhao J, Sakai K. Multiple signalling pathways mediate fungal elicitor-induced beta-thujaplicin biosynthesis in Cupressus lusitanica cell cultures. J Exp Bot 2003; 54:647–656.PubMedCrossRefGoogle Scholar
  41. 41.
    Trewavas AJ, Malho R. Ca2+ signalling in plant cells: the big network! Curr Opin Plant Biol 1998; 1:428–433.PubMedCrossRefGoogle Scholar
  42. 42.
    White PJ, Broadley MR. Calcium in plants. Ann Bot (Lond) 2003; 92:487–511.CrossRefGoogle Scholar
  43. 43.
    Umemura K, Ogawa N, Koga J et al. Elicitor activity of cerebroside, a sphingolipid elicitor, in cell suspension cultures of rice. Plant Cell Physiol 2002; 43:778–784.PubMedCrossRefGoogle Scholar
  44. 44.
    Vogeli U, Vogeli-Lange R, Chappell J. Inhibition of phytoalexin biosynthesis in elicitor-treated tobacco cell-suspension cultures by calcium/calmodulin antagonists. Plant Physiol 1992; 100:1369–1376.PubMedCrossRefGoogle Scholar
  45. 45.
    Chandra S, Heinstein PF, Low PS. Activation of phospholipase A by plant defense elicitors. Plant Physiol 1996; 110:979–986.PubMedGoogle Scholar
  46. 46.
    Kasparovsky T, Blein JP, Mikes V. Ergosterol elicits oxidative burst in tobacco cells via phospholipase A2 and protein kinase C signal pathway. Plant Physiol Biochem 2004; 42:429–435.PubMedCrossRefGoogle Scholar
  47. 47.
    Legendre L, Yueh YG, Crain R et al. Phospholipase C activation during elicitation of the oxidative burst in cultured plant cells. J Biol Chem 1993; 268:24559–24563.PubMedGoogle Scholar
  48. 48.
    van der Luit AH, Piatti T, van Doorn A et al. Elicitation of suspension-cultured tomato cells triggers the formation of phosphatidic acid and diacylglycerol pyrophosphate. Plant Physiol 2000; 123:1507–1516.PubMedCrossRefGoogle Scholar
  49. 49.
    Kurosaki F, Tsurusawa Y, Nishi A. Breakdown of phosphatidylinositol during the elicitation of phytoalexin production in cultured carrot cells. Plant Physiol 1987; 85:601–604.PubMedCrossRefGoogle Scholar
  50. 50.
    Walton TJ, Cooke CJ, Newton RP et al. Evidence that generation of inositol 1,4,5-trisphosphate and hydrolysis of phosphatidylinositol 4,5-bisphosphate are rapid responses following addition of fungal elicitor which induces phytoalexin synthesis in lucerne (Medicago sativa) suspension culture cells. Cell Signal 1993; 5:345–356.PubMedCrossRefGoogle Scholar
  51. 51.
    Zhao J, Guo Y, Kosaihira A et al. Rapid accumulation and metabolism of polyphosphoinositol and its possible role in phytoalexin biosynthesis in yeast elicitor-treated Cupressus lusitanica cell cultures. Planta 2004; 219:121–131.PubMedCrossRefGoogle Scholar
  52. 52.
    Benschop JJ, Mohammed S, O’flaherty M et al. Quantitative phospho-proteomics of early elicitor signalling in Arabidopsis. Mol Cell Proteomics 2007;6(7):1198–1214.PubMedCrossRefGoogle Scholar
  53. 53.
    Nuhse TS, Boiler T, Peck SC. A plasma membrane syntaxin is phosphorylated in response to the bacterial elicitor flagellin. J Biol Chem 2003; 278:45248–45254.PubMedCrossRefGoogle Scholar
  54. 54.
    Peck SC, Nuhse TS, Hess D et al. Directed proteomics identifies a plant-specific protein rapidly phosphorylated in response to bacterial and fungal elicitors. Plant Cell 2001; 13:1467–1475.PubMedCrossRefGoogle Scholar
  55. 55.
    Allwood EG, Davies DR, Gerrish C et al. Phosphorylation of phenylalanine ammonia-lyase: evidence for a novel protein kinase and identification of the phosphorylated residue. FEBS Lett 1999; 457:47–52.PubMedCrossRefGoogle Scholar
  56. 56.
    Asai T, Tena G, Plotnikova J et al. MAP kinase signalling cascade in Arabidopsis innate immunity. Nature 2002; 415:977–983.PubMedCrossRefGoogle Scholar
  57. 57.
    Petersen M, Brodersen P, Naested H et al. Arabidopsis map kinase 4 negatively regulates systemic acquired resistance. Cell 2000; 103:1111–1120.PubMedCrossRefGoogle Scholar
  58. 58.
    Droillard MJ, Thibivilliers S, Cazale AC et al. Protein kinases induced by osmotic stresses and elicitor molecules in tobacco cell suspensions: two crossroad MAP kinases and one osmoregulation-specific protein kinase. FEBS Lett 2000; 474:217–222.PubMedCrossRefGoogle Scholar
  59. 59.
    Kumar D, Klessig DF. Differential induction of tobacco MAP kinases by the defense signals nitric oxide, salicylic acid, ethylene and jasmonic acid. Mol Plant Microbe Interact 2000; 13:347–351.PubMedCrossRefGoogle Scholar
  60. 60.
    Romeis T, Piedras P, Zhang S et al. Rapid Avr9-and Cf-9-dependent activation of MAP kinases in tobacco cell cultures and leaves: convergence of resistance gene, elicitor, wound and salicylate responses. Plant Cell 1999; 11:273–287.PubMedCrossRefGoogle Scholar
  61. 61.
    Kovtun Y, Chiu WL, Tena G et al. Functional analysis of oxidative stress-activated mitogen-activated protein kinase cascade in plants. Proc Natl Acad Sci USA 2000; 97:2940–2945.PubMedCrossRefGoogle Scholar
  62. 62.
    Nuhse TS, Peck SC, Hirt H et al. Microbial elicitors induce activation and dual phosphorylation of the Arabidopsis thaliana MAPK 6. J Biol Chem 2000; 275:7521–7526.PubMedCrossRefGoogle Scholar
  63. 63.
    Cardinale, F, Jonak C, Ligterink W et al. Differential activation of four specific MAPK pathways by distinct elicitors. J Biol Chem 2000; 275:36734–36740.PubMedCrossRefGoogle Scholar
  64. 64.
    Cardinale F, Meskiene I, Ouaked F et al. Convergence and divergence of stress-induced mitogen-activated protein kinase signaling pathways at the level of two distinct mitogen-activated protein kinase kinases. Plant Cell 2002; 14:703–711.PubMedGoogle Scholar
  65. 65.
    Ligterink W, Kroj T, zur NU et al. Receptor-mediated activation of a MAP kinase in pathogen defense of plants. Science 1997; 276:2054–2057.PubMedCrossRefGoogle Scholar
  66. 66.
    Yang KY, Liu Y, Zhang S. Activation of a mitogen-activated protein kinase pathway is involved in disease resistance in tobacco. Proc Natl Acad Sci USA 2001; 98:741–746.PubMedCrossRefGoogle Scholar
  67. 67.
    Hu X, Neill SJ, Fang J et al. Mitogen-activated protein kinases mediate the oxidative burst and saponin synthesis induced by chitosan in cell cultures of Panax ginseng. Sci China C Life Sci 2004; 47:303–312.PubMedCrossRefGoogle Scholar
  68. 68.
    Vandelle E, Poinssot B, Wendehenne D et al. Integrated signaling network involving calcium, nitric oxide and active oxygen species but not mitogen-activated protein kinases in BcPG1-elicited grapevine defenses. Mol Plant Microbe Interact 2006; 19:429–440.PubMedCrossRefGoogle Scholar
  69. 69.
    Levine A, Tenhaken R, Dixon R et al. H2O2 from the oxidative burst orchestrates the plant hypersensitive disease resistance response. Cell 1994; 79:583–593.PubMedCrossRefGoogle Scholar
  70. 70.
    Apostol I, Heinstein PF, Low PS. Rapid stimulation of an oxidative burst during elicitation of cultured plant cells. Plant Physiol 1989; 90:109–116.PubMedCrossRefGoogle Scholar
  71. 71.
    Aziz A, Poinssot B, Daire X et al. Laminarin elicits defense responses in grapevine and induces protection against Botrytis cinerea and Plasmopara viticola. Mol Plant Microbe Interact 2003; 16:1118–1128.PubMedCrossRefGoogle Scholar
  72. 72.
    Legendre L, Rueter S, Heinstein PF et al. Characterization of the oligogalacturonide-induced oxidative burst in cultured soybean (glycine max) cells. Plant Physiol 1993; 102:233–240.PubMedGoogle Scholar
  73. 73.
    Meyer A, Puhler A, Niehaus K. The lipopolysaccharides of the phytopathogen Xanthomonas campestris pv. campestris induce an oxidative burst reaction in cell cultures of Nicotiana tabacum. Planta 2001; 213:214–222.PubMedCrossRefGoogle Scholar
  74. 74.
    Mithofer A, Fliegmann J, Daxberger A et al. Induction of H(2)O(2) synthesis by beta-glucan elicitors in soybean is independent of cytosolic calcium transients. FEBS Lett 2001; 508:191–195.PubMedCrossRefGoogle Scholar
  75. 75.
    Pauw B, van Duijn B, Kijne JW et al. Activation of the oxidative burst by yeast elicitor in Catharanthus roseus cells occurs independently of the activation of genes involved in alkaloid biosynthesis. Plant Mol Biol 2004; 55:797–805.PubMedGoogle Scholar
  76. 76.
    Xu X, Hu X, Neill SJ et al. Fungal elicitor induces singlet oxygen generation, ethylene release and saponin synthesis in cultured cells of Panax ginseng C. A. Meyer. Plant Cell Physiol 2005; 46:947–954.PubMedCrossRefGoogle Scholar
  77. 77.
    Desikan R, Hancock JT, Coffey MJ et al. Generation of active oxygen in elicited cells of Arabidopsis thaliana is mediated by a NADPH oxidase-like enzyme. FEBS Lett 1996; 382:213–217.PubMedCrossRefGoogle Scholar
  78. 78.
    Groom QJ, Torres MA, Fordham-Skelton AP et al. rbohA, a rice homologue of the mammalian gp91phox respiratory burst oxidase gene. Plant J 1996; 10:515–522.PubMedCrossRefGoogle Scholar
  79. 79.
    Keller T, Damude HG, Werner D et al. A plant homolog of the neutrophil NADPH oxidase gp91phox subunit gene encodes a plasma membrane protein with Ca2+ binding motifs. Plant Cell 1998; 10:255–266.PubMedCrossRefGoogle Scholar
  80. 80.
    Torres MA, Dangl JL, Jones JD. Arabidopsis gp91phox homologues AtrbohD and AtrbohF are required for accumulation of reactive oxygen intermediates in the plant defense response. Proc Natl Acad Sci USA 2002; 99:517–522.PubMedCrossRefGoogle Scholar
  81. 81.
    Torres MA, Jones JD, Dangl JL. Pathogen-induced NADPH oxidase-derived reactive oxygen intermediates suppress spread of cell death in Arabidopsis thaliana. Nat Genet 2005; 37:1130–1134.PubMedCrossRefGoogle Scholar
  82. 82.
    Jabs T, Tschope M, Colling C et al. Elicitor-stimulated ion fluxes and O2-from the oxidative burst are essential components in triggering defense gene activation and phytoalexin synthesis in parsley. Proc Natl Acad Sci USA 1997; 94:4800–4805.PubMedCrossRefGoogle Scholar
  83. 83.
    Degousee N, Triantaphylides C, Montillet JL. Involvement of oxidative processes in the signaling mechanisms leading to the activation of glyceollin synthesis in soybean (glycine max). Plant Physiol 1994; 104:945–952.PubMedGoogle Scholar
  84. 84.
    Guo ZJ, Lamb C, Dixon RA. Potentiation of the oxidative burst and isoflavonoid phytoalexin accumulation by serine protease inhibitors. Plant Physiol 1998; 118:1487–1494.PubMedCrossRefGoogle Scholar
  85. 85.
    Matsuda F, Miyagawa H, Ueno T. Involvement of reactive oxygen species in the induction of (S)-N-p-coumaroyloctopamine accumulation by beta-1,3-glucooligosaccharide elicitors in potato tuber tissues. Z Naturforsch (C) 2001; 56:228–234.Google Scholar
  86. 86.
    Kravchuk Z, Perkovs’ka HI, Dmytriiev OP. (Role of active forms of oxygen in the induction of phytoalexin synthesis in Allium cepa cells). Tsitol Genet 2003; 37:30–35.PubMedGoogle Scholar
  87. 87.
    Yamaguchi T, Tanabe S, Minami E et al. Activation of phospholipase D induced by hydrogen peroxide in suspension-cultured rice cells. Plant Cell Physiol 2004; 45:1261–1270.PubMedCrossRefGoogle Scholar
  88. 88.
    Galletti R, Denoux C, Gambetta S et al. The AtrbohD-mediated oxidative burst elicited by oligogalacturonides in Arabidopsis is dispensable for the activation of defense responses effective against Botrytis cinerea. Plant Physiol 2008; 148:1695–1706.PubMedCrossRefGoogle Scholar
  89. 89.
    Thoma I, Loeffler C, Sinha AK et al. Cyclopentenone isoprostanes induced by reactive oxygen species trigger defense gene activation and phytoalexin accumulation in plants. Plant J 2003; 34:363–375.PubMedCrossRefGoogle Scholar
  90. 90.
    Wu J, Ge X. Oxidative burst, jasmonic acid biosynthesis and taxol production induced by low-energy ultrasound in Taxus chinensis cell suspension cultures. Biotechnol Bioeng 2004; 85:714–721.PubMedCrossRefGoogle Scholar
  91. 91.
    Brader G, Tas E, Palva ET. Jasmonate-dependent induction of indole glucosinolates in Arabidopsis by culture filtrates of the nonspecific pathogen Erwinia carotovora. Plant Physiol 2001; 126:849–860.PubMedCrossRefGoogle Scholar
  92. 92.
    Zhao J, Zheng SH, Fujita K et al. Jasmonate and ethylene signalling and their interaction are integral parts of the elicitor signalling pathway leading to beta-thujaplicin biosynthesis in Cupressus lusitanica cell cultures. J Exp Bot 2004; 55:1003–1012.PubMedCrossRefGoogle Scholar
  93. 93.
    Tassoni A, Fornale S, Franceschetti M et al. Jasmonates and Na-orthovanadate promote resveratrol production in Vitis vinifera cv. Barbera cell cultures. New Phytol 2005; 166:895–905.PubMedCrossRefGoogle Scholar
  94. 94.
    Clarke A, Mur LA, Darby RM et al. Harpin modulates the accumulation of salicylic acid by Arabidopsis cells via apoplastic alkalization. J Exp Bot 2005; 56:3129–3136.PubMedCrossRefGoogle Scholar
  95. 95.
    Dorey S, Kopp M, Geoffroy P et al. Hydrogen peroxide from the oxidative burst is neither necessary nor sufficient for hypersensitive cell death induction, phenylalanine ammonia lyase stimulation, salicylic acid accumulation, or scopoletin consumption in cultured tobacco cells treated with elicitin. Plant Physiol 1999; 121:163–172.PubMedCrossRefGoogle Scholar
  96. 96.
    Klarzynski O, Plesse B, Joubert JM et al. Linear beta-1,3 glucans are elicitors of defense responses in tobacco. Plant Physiol 2000; 124:1027–1038.PubMedCrossRefGoogle Scholar
  97. 97.
    Mishina TE, Zeier J. Pathogen-associated molecular pattern recognition rather than development of tissue necrosis contributes to bacterial induction of systemic acquired resistance in Arabidopsis. Plant J 2007; 50:500–513.PubMedCrossRefGoogle Scholar
  98. 98.
    Qian ZG, Zhao ZJ, Xu Y et al. Novel chemically synthesized salicylate derivative as an effective elicitor for inducing the biosynthesis of plant secondary metabolites. Biotechnol Prog 2006; 22:331–333.PubMedCrossRefGoogle Scholar
  99. 99.
    Pitta-Alvarez SI, Spollansky TC, Giulietti AM. The influence of different biotic and abiotic elicitors on the production and profile of tropane alkaloids in hairy root cultures of Brugmansia candida. Enzyme Microb Technol 2000; 26:252–258.PubMedCrossRefGoogle Scholar
  100. 100.
    Alves LM, Kalan EB, Heisler EG. An in vitro control mechanism for potato stress metabolite biosynthesis. Plant Physiol 1981; 68:1465–1467.PubMedCrossRefGoogle Scholar
  101. 101.
    Nakazato Y, Tamogami S, Kawai H et al. Methionine-induced phytoalexin production in rice leaves. Biosci Biotechnol Biochem 2000; 64:577–583.PubMedCrossRefGoogle Scholar
  102. 102.
    Khosroushahi AY, Valizadeh M, Ghasempour A et al. Improved Taxol production by combination of inducing factors in suspension cell culture of Taxus baccata. Cell Biol Int 2006; 30:262–269.PubMedCrossRefGoogle Scholar
  103. 103.
    Zhang B, Ramonell K, Somerville S et al. Characterization of early, chitin-induced gene expression in Arabidopsis. Mol Plant Microbe Interact 2002; 15:963–970.PubMedCrossRefGoogle Scholar
  104. 104.
    Zipfel C, Robatzek S, Navarro L et al. Bacterial disease resistance in Arabidopsis through flagellin perception. Nature 2004; 428:764–767.PubMedCrossRefGoogle Scholar
  105. 105.
    Schuhegger R, Nafisi M, Mansourova M et al. CYP71B15 (PAD3) catalyzes the final step in camalexin biosynthesis. Plant Physiol 2006; 141:1248–1254.PubMedCrossRefGoogle Scholar
  106. 106.
    Ferrari S, Galletti R, Denoux C et al. Resistance to botrytis cinerea induced in Arabidopsis by elicitors is independent of salicylic acid, ethylene or jasmonate signaling but requires PAD3. Plant Physiol 2007; 144:367–379.PubMedCrossRefGoogle Scholar
  107. 107.
    Thomma BP, Nelissen I, Eggermont K et al. Deficiency in phytoalexin production causes enhanced susceptibility of Arabidopsis thaliana to the fungus Alternaria brassicicola. Plant J 1999; 19:163–171.PubMedCrossRefGoogle Scholar
  108. 108.
    The Arabidopsis Genome Initiative. Analysis of the genome sequence of the flowering plant Arabidopsis thaliana. Nature 2000; 408:796–815.CrossRefGoogle Scholar
  109. 109.
    D’Auria JC, Gershenzon J. The secondary metabolism of Arabidopsis thaliana: growing like a weed. Curr Opin Plant Biol 2005; 8, 308–316.PubMedCrossRefGoogle Scholar
  110. 110.
    Eulgem T. Regulation of the Arabidopsis defense transcriptome. Trends Plant Sci 2005; 10:71–78.PubMedCrossRefGoogle Scholar
  111. 111.
    Ferrari S, Galletti R, Denoux C et al. Resistance to botrytis cinerea induced in Arabidopsis by elicitors is independent of salicylic acid, ethylene or jasmonate signaling but requires PAD3. Plant Physiol 2007; 144:367–379.PubMedCrossRefGoogle Scholar
  112. 112.
    Huang X, von Rad U, Durner J. Nitric oxide induces transcriptional activation of the nitric oxide-tolerant alternative oxidase in Arabidopsis suspension cells. Planta 2002; 215:914–923.PubMedCrossRefGoogle Scholar
  113. 113.
    Marathe R, Guan Z, Anandalakshmi R et al. Study of Arabidopsis thaliana resistome in response to cucumber mosaic virus infection using whole genome microarray. Plant Mol Biol 2004; 55:501–520.PubMedCrossRefGoogle Scholar
  114. 114.
    Narusaka Y, Narusaka M, Seki M et al. The cDNA microarray analysis using an Arabidopsis pad3 mutant reveals the expression profiles and classification of genes induced by Alternaria brassicicola attack. Plant Cell Physiol 2003; 44:377–387.PubMedCrossRefGoogle Scholar
  115. 115.
    Navarro L, Zipfel C, Rowland O et al. The transcriptional innate immune response to flg22. Interplay and overlap with Avr gene-dependent defense responses and bacterial pathogenesis. Plant Physiol 2004; 135:1113–1128.PubMedCrossRefGoogle Scholar
  116. 116.
    Schenk PM, Kazan K, Wilson I et al. Coordinated plant defense responses in Arabidopsis revealed by microarray analysis. Proc Natl Acad Sci USA 2000; 97:11655–11660.PubMedCrossRefGoogle Scholar
  117. 117.
    Suzuki H, Reddy MS, Naoumkina M et al. Methyl jasmonate and yeast elicitor induce differential transcriptional and metabolic reprogramming in cell suspension cultures of the model legume Medicago truncatula. Planta 2005; 220:696–707.PubMedCrossRefGoogle Scholar
  118. 118.
    Gachon CM, Langlois-Meurinne M, Henry Y et al. Transcriptional coregulation of secondary metabolism enzymes in Arabidopsis: functional and evolutionary implications. Plant Mol Biol 2005; 58:229–245.PubMedCrossRefGoogle Scholar
  119. 119.
    Ramonell K, Berrocal-Lobo M, Koh S et al. Loss-of-function mutations in chitin responsive genes show increased susceptibility to the powdery mildew pathogen erysiphe cichoracearum. Plant Physiol 2005; 138:1027–1036.PubMedCrossRefGoogle Scholar
  120. 120.
    Goossens A, Hakkinen ST, Laakso I et al. A functional genomics approach toward the understanding of secondary metabolism in plant cells. Proc Natl Acad Sci USA 2003; 100:8595–8600.PubMedCrossRefGoogle Scholar
  121. 121.
    Larkin PJ, Miller JA, Allen RS et al. Increasing morphinan alkaloid production by over-expressing codeinone reductase in transgenic Papaver somniferum. Plant Biotechnol J 2007; 5:26–37.PubMedCrossRefGoogle Scholar
  122. 122.
    Chang MC, Eachus RA, Trieu W et al. Engineering Escherichia coli for production of functionalized terpenoids using plant P450s. Nat Chem Biol 2007; 3:274–277.PubMedCrossRefGoogle Scholar
  123. 123.
    Chatel G, Montiel G, Pre M et al. CrMYCl, a Catharanthus roseus elicitor-and jasmonate-responsive bHLH transcription factor that binds the G-box element of the strictosidine synthase gene promoter. J Exp Bot 2003; 54:2587–2588.PubMedCrossRefGoogle Scholar
  124. 124.
    Menke FL, Champion A, Kijne JW et al. A novel jasmonate-and elicitor-responsive element in the periwinkle secondary metabolite biosynthetic gene Str interacts with a jasmonate-and elicitor-inducible AP2-domain transcription factor ORCA2. EMBO J 1999; 18:4455–4463.PubMedCrossRefGoogle Scholar
  125. 125.
    van der Fits L, Memelink J. ORCA3, a jasmonate-responsive transcriptional regulator of plant primary and secondary metabolism. Science 2000; 289:295–297.PubMedCrossRefGoogle Scholar
  126. 126.
    van der Fits L, Memelink J. The jasmonate-inducible AP2/ERF-domain transcription factor ORCA3 activates gene expression via interaction with a jasmonate-responsive promoter element. Plant J 2001; 25:43–53.PubMedCrossRefGoogle Scholar
  127. 127.
    Bino RJ, Hall RD, Fiehn O et al. Potential of metabolomics as a functional genomics tool. Trends Plant Sci 2004; 9:418–425.PubMedCrossRefGoogle Scholar
  128. 128.
    Hall R, Beale M, Fiehn O et al. Plant metabolomics: the missing link in functional genomics strategies. Plant Cell 2002; 14:1437–1440.PubMedCrossRefGoogle Scholar
  129. 129.
    Walker TS, Bais HP, Halligan KM et al. Metabolic profiling of root exudates of Arabidopsis thaliana. J Agric Food Chem 2003; 51:2548–2554.PubMedCrossRefGoogle Scholar
  130. 130.
    Bednarek P, Schneider B, Svatos A et al. Structural complexity, differential response to infection and tissue specificity of indolic and phenylpropanoid secondary metabolism in Arabidopsis roots. Plant Physiol 2005; 138:1058–1070.PubMedCrossRefGoogle Scholar
  131. 131.
    Ketchum RE, Rithner CD, Qiu D et al. Taxus metabolomics: methyl jasmonate preferentially induces production of taxoids oxygenated at C-13 in Taxus x media cell cultures. Phytochemistry 2003; 62:901–909.PubMedCrossRefGoogle Scholar
  132. 132.
    Broeckling CD, Huhman DV, Farag MA et al. Metabolic profiling of Medicago truncatula cell cultures reveals the effects of biotic and abiotic elicitors on metabolism. J Exp Bot 2005; 56:323–336.PubMedCrossRefGoogle Scholar
  133. 133.
    Hirai MY, Fujiwara T, Awazuhara M et al. Global expression profiling of sulfur-starved Arabidopsis by DNA macroarray reveals the role of O-acetyl-1-serine as a general regulator of gene expression in response to sulfur nutrition. Plant J 2003; 33:651–663.PubMedCrossRefGoogle Scholar
  134. 134.
    Hirai MY, Sugiyama K, Sawada Y et al. Omics-based identification of Arabidopsis Myb transcription factors regulating aliphatic glucosinolate biosynthesis. Proc Natl Acad Sci USA 2007; 104:6478–6483.PubMedCrossRefGoogle Scholar
  135. 135.
    Hahn MG, Darvill AG, Albersheim P. Host-Pathogen Interactions: XIX. The endogenous elicitor, a fragment of a plant cell wall polysaccharide that elicits phytoalexin accumulation in soybeans. Plant Physiol 1981; 68:1161–1169.PubMedCrossRefGoogle Scholar
  136. 136.
    Hadwiger LA, Beckman JM. Chitosan as a component of pea-fusarium solani interactions. Plant Physiol 1980; 66:205–211.PubMedCrossRefGoogle Scholar
  137. 137.
    Keen NT, Yoshikawa M, Wang MC. Phytoalexin elicitor activity of carbohydrates from phytophthora megasperma f.Sp. Glycinea and other sources. Plant Physiol 1983; 71:466–471.PubMedCrossRefGoogle Scholar
  138. 138.
    Ricci P, Bonnet P, Huet JC et al. Structure and activity of proteins from pathogenic fungi phytophthora eliciting necrosis and acquired resistance in tobacco. Eur J Biochem 1989; 183:555–563.PubMedCrossRefGoogle Scholar
  139. 139.
    Brunner F, Rosahl S, Lee J et al. Pep-13:a plant defense-inducing pathogen-associated pattern from Phytophthora transglutaminases. EMBO J 2002; 21:6681–6688.PubMedCrossRefGoogle Scholar
  140. 140.
    Gomez-Gomez L, Felix G, Boller T. A single locus determines sensitivity to bacterial flagellin in Arabidopsis thaliana. Plant J 1999; 18:277–284.PubMedCrossRefGoogle Scholar
  141. 141.
    Lotan T, Fluhr R. Xylanase, a novel elicitor of pathogenesis-related proteins in tobacco, uses a non-ethylene pathway for induction. Plant Physiol 1990; 93:811–817.PubMedCrossRefGoogle Scholar
  142. 142.
    Poinssot B, Vandelle E, Bentejac M et al. The endopolygalacturonase 1 from Botrytis cinerea activates grapevine defense reactions unrelated to its enzymatic activity. Mol Plant Microbe Interact 2003; 16:553–564.PubMedCrossRefGoogle Scholar
  143. 143.
    Kunze G, Zipfel C, Robatzek S et al. The N terminus of bacterial elongation factor Tu elicits innate immunity in Arabidopsis plants. Plant Cell 2004; 16:3496–3507.PubMedCrossRefGoogle Scholar

Copyright information

© Landes Bioscience and Springer Science+Business Media, LLC 2010

Authors and Affiliations

  • Simone Ferrari
    • 1
  1. 1.Dipartimento di Biologia VegetaleUniversità degli Studi di RomaRomeItaly

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