Defence signalling triggered by Flg22 and Harpin is integrated into a different stilbene output in Vitis cells

PLoS ONE

Volumn 7, Issue 7, 2012, Pages

  Chang, Xiaoli ^a   Nick, Peter ^a  

^a KARLSRUHE INSTITUTE OF TECHNOLOGY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; HARPIN; MITOGEN ACTIVATED PROTEIN KINASE; PROTEIN FLG22; STILBENE; UNCLASSIFIED DRUG;

ALKALINIZATION; APOPTOSIS; ARTICLE; CALCIUM TRANSPORT; CONTROLLED STUDY; CYTOSKELETON; ENZYME ACTIVITY; GENE EXPRESSION; GRAPE; INNATE IMMUNITY; NEGATIVE FEEDBACK; NONHUMAN; OXIDATIVE STRESS; PLANT CELL; PLANT DEFENSE; RESPIRATORY BURST; SIGNAL TRANSDUCTION; VITIS; VITIS RUPESTRIS;

ANTIGENS, BACTERIAL; BACTERIAL OUTER MEMBRANE PROTEINS; CELL DEATH; CELL MEMBRANE PERMEABILITY; CELL RESPIRATION; CELLS, CULTURED; GENE EXPRESSION REGULATION, PLANT; GENES, PLANT; HYDROGEN-ION CONCENTRATION; MAP KINASE SIGNALING SYSTEM; MICROTUBULES; PLANT DISEASES; PLANT IMMUNITY; REACTIVE OXYGEN SPECIES; STILBENES; VITIS;

BACTERIA (MICROORGANISMS); VITIS; VITIS RUPESTRIS; VITIS VINIFERA;

EID: 84863682060     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0040446     Document Type: Article

References (81)

1. Jones JD, Dangl JL, (2006) The plant immune system. Nature 444: 323-329.
2. Cunnac S, Lindeberg M, Collmer A, (2009) Pseudomonas syringae type III secretion system effectors: repertoires in search of functions. Curr Opin Microbiol 12: 53-60.
3. Tsuda K, Katagiri F, (2010) Comparing signalling mechanisms engaged in pattern-triggered and effector-triggered immunity. Curr Opin Plant Biol 13: 459-465.
4. Block A, Li G, Fu ZQ, Alfano JR, (2008) Phytopathogen type III effector weaponry and their plant targets. Curr Opin Plant Biol 11: 396-403.
5. Boller T, Felix G, (2009) A renaissance of elicitors: perception of microbe-associated molecular patterns and danger signals by pattern-recognition receptors. Annu Rev Plant Biol 60: 379-406.
6. Boller T, He SY, (2009) Innate immunity in plants: an arms race between pattern recognition receptors in plants and effectors in microbial pathogens. Science 324: 742-744.
7. Felix G, Duran JD, Volko S, Boller T, (1999) Plants have a sensitive perception system for the most conserved domain of bacterial flagellin. Plant J 18: 265-276.
8. Lee J, Klüsener B, Tsiamis G, Stevens C, Neyt C, et al. (2001) HrpZ(Psph) from the plant pathogen Pseudomonas syringae pv. phaseolicola binds to lipid bilayers and forms an ion-conducting pore in vitro. Proc Natl Acad Sci U S A 98: 289-294.
9. Jeworutzki E, Roeflsema MR, Anschütz U, Krol E, Elzenga JT, et al. (2010) Early signalling through the Arabidopsis pattern recognition receptor FLS2 and EFR involves Ca2+-associated opening of plasma membrane anion channels. Plant J 62: 367-378.
10. Gómez-Gómez L, Boller T, (2000) FLS2: an LRR receptor-like kinase involved in the perception of the bacterial elicitor flagellin in Arabidopsis. Mol Cell 5: 1003-1011.
11. Nürnberger T, (1999) Signal perception in plant pathogen defense. Cell Mol Life Sci 55: 167-182.
12. Zipfel C, Kunze G, Chinchilla D, Caniard A, Jones JDG, et al. (2006) Perception of the bacterial PAMP EF-Tu by the receptor EFR restricts Agrobacterium-mediated transformation. Cell 125: 749-760.
13. Zipfel C, Robatzek S, Navarro L, Oakeley EJ, Jones JDG, et al. (2004) Bacterial disease resistance in Arabidopsis through ffiagellin perception. Nature 428: 764-767.
14. Chinchilla D, Bauer Z, Regenass M, Boller T, Felix G, (2006) The Arabidopsis receptor kinase FLS2 binds flg22 and determines the specificity of flagellin perception. Plant Cell 18: 465-476.
15. Chinchilla D, Zipfel C, Robatzek S, Kemmerling B, Nürnberger T, et al. (2007) A flagellin-induced complex of the receptor FLS2 and BAK1 initiates plant defence. Nature 448: 497-500.
16. Nicaise V, Roux M, Zipfel C, (2009) Recent advances in PAMP-triggered immunity against bacteria: pattern recognition receptors watch over and raise the alarm. Plant Physiology 150: 1638-1647.
17. He P, Shan L, Lin NC, Martin GB, Kemmerling B, et al. (2006) Specific bacterial suppressors of MAMP signalling upstream of MAPKKK in Arabidopsis innate immunity. Cell 125: 563-575.
18. Abramovitch RB, Janjusevic R, Stebbins CE, Martin GB, (2006) Type III effector AvrPtoB requires intrinsic E3 ubiquitin ligase activity to suppress plant cell death and immunity. Proc Natl Acad Sci U S A 103: 2851-2856.
19. Kim JG, Taylor KW, Hotson A, Keegan M, Schmelz EA, et al. (2008) XopD SUMO protease affects host transcription, promotes pathogen growth, and delays symptom development in Xanthomonas-infected tomato leaves. Plant Cell 20: 1915-1929.
20. Hauck P, Thilmony R, He SY, (2003) A Pseudomonas syringae type III effector suppresses cell wall-based extracellular defense in susceptible Arabidopsis plants. Proc Natl Acad Sci U S A 100: 8577-8582.
21. Chisholm ST, Coaker G, Day B, Staskawicz BJ, (2006) Host-microbe interactions: shaping the evolution of the plant immune response. Cell 124: 803-814.
22. Nomura K, Melotto M, He SY, (2005) Suppression of host defense in compatible plant-Pseudomonas syringae interactions. Curr Opin Plant Biol 8: 361-368.
23. Wei ZM, Laby RJ, Zumoff CH, Bauer DW, He SY, et al. (1992) Harpin, elicitor of the hypersensitive response produced by the plant pathogen Erwinia amylovora. Science 257: 85-88.
24. Baker CJ, Orlandi EW, Mock NM, (1993) Harpin, an elicitor of the hypersensitive response in tobacco caused by Erwinia amylovora, elicits active oxygen production in suspension cells. Plant Physiology 102: 134-344.
25. Bauer DW, Wei ZM, Beer SV, Collmer A, (1995) Erwinia chrysanthemi harpinEch: an elicitor of the hypersensitive response that contributes to soft-rot pathogenesis. Mol Plant Microbe In 8: 84-91.
26. Dong H, Delaney TP, Bauer DW, Beer SV, (1999) Harpin induces disease resistance in Arabidopsis through the systemic acquired resistance pathway mediated by salicylic acid and the NIM1 gene. Plant J 20: 207-215.
27. Samuel MA, Hall H, Krzymowska M, Drewiecka K, Hennig J, et al. (2005) SIPK signalling controls multiple components of harpin-induced cell death in tobacco. Plant J 42: 406-416.
28. Tampakaki AP, Skandalis N, Gazi AD, Bastaki MN, Sarris PF, et al. (2010) Playing the "Harp": Evolution of our understanding of hrp/hrc genes. Annu Rev Phytopathol 48: 347-370.
29. Desikan R, Reynolds A, Hancock JT, Neill SJ, (1998) Harpin and hydrogen peroxide both initiate programmed cell death but have differential effects on defence gene expression in Arabidopsis suspension cultures. Biochem J 330: 115-120.
30. Ichinose Y, Andi S, Doi R, Tanaka R, Taguchi F, et al. (2001) Generation of hydrogen peroxide is not required for harpin-induced apoptotic cell death in tobacco BY-2 cell suspension culture. Plant Physiol Bioch 39: 771-776.
31. Gopalan S, Wei W, He SY, (1996) Hrp gene-dependent induction of hin1: a plant gene activated rapidly by both harpins and the avrPto gene-mediated signal. Plant J 10; 591-600.
32. Lee J, Klessig DF, Nürnberger T, (2001b) A harpin binding site in tobacco plasma membranes mediates activation of the pathogenesis-related gene HIN1 independent of extracellular calcium but dependent on mitogen-activated protein kinase activity. Plant Cell 13: 1079-1093.
33. Qiao F, Chang XL, Nick P, (2010) The cytoskeleton enhances gene expression in the response to the Harpin elicitor in grapevine. J Exp Bot 61: 4021-4031.
34. Thomma BP, Nürnberger T, Joosten MH, (2011) Of PAMPs and effectors: the blurred PTI-ETI dichotomy. Plant Cell 23: 4-15.
35. Tsuda K, Sato M, Glazebrook J, Cohen JD, Katagiri F, (2008) Interplay between MAMP-triggered and SA-mediated defense responses. Plant J 53: 763-775.
36. Aslam SN, Erbs G, Morrissey KL, Newman MA, Chinchilla D, et al. (2009) Microbe-associated molecular pattern (MAMP) signatures, synergy, size and charge: inffiuences on perception or mobility and host defence responses. Mol Plant Pathol 10: 375-387.
37. Langcake P, (1981) Disease resistance of Vitis spp. and the production of resveratrol, ε-viniferin, α-viniferin and pterostilbene. Physiol Plant Pathol 18: 213-226.
38. Pezet R, Gindro K, Viret O, Richter H, (2004) Effects of resveratrol, viniferins and pterostilbenes on Plasmopara viticola zoospore mobility and disease development. Vitis 43: 145-148.
39. Poinssot B, Vandelle E, Bentéjac M, Adrian M, Levis C, et al. (2003) The endopolygalacturonase 1 from Botrytis cinerea activates grapevine defense reactions unrelated to its enzymatic activity. Mol Plant Microbe In 16: 553-564.
40. Aziz A, Heyraud A, Lambert B, (2004) Oligogalacturonide signal transduction, induction of defense-related responses and protection of grapevine against Botrytis cinerea. Planta 218: 767-774.
41. Vandelle E, Poinssot B, Wendehenne D, Bentéjac M, Alain P, (2006) Integrated signalling network involving calcium, nitric oxide, and active oxygen species but not mitogen-activated protein kinases in BcPG1-elicited grapevine defenses. Mol Plant Microbe In 19: 429-440.
42. Nürnberger T, Scheel D, (2001) Signal transmission in the plant immune response. Trends Plant Sci 6: 372-379.
43. Jabs T, Tschöpe M, Colling C, Hahlbrock K, Scheel D, (1997) 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 U S A 94: 4800-4805.
44. Ding JP, Pickard BG, (1993) Mechanosensory calcium-selective cation channels in epidermal cells. Plant J 3: 83-110.
45. Zhang S, Klessig DF, (2001) MAPK cascades in plant defence signalling. Trends Plant Sci 6: 520-527.
46. Jonak C, Ökrész L, Bögre L, Hirt H, (2002) Complexity, cross talk and integration of plant MAP kinase signalling. Curr Opin Plant Biol 5: 415-424.
47. Nick P, (2011) Mechanics of the Cytoskeleton. In: Wojtaszek P, editors. pp. 53-90 editor. Mechanical Integration of Plant Cells and Plants. Springer Berlin Heidelberg. pp.
48. Wojtaszek P, (1997) Oxidative burst: an early plant response to pathogen infection. Biochem J 322: 681-692.
49. Lamb C, Dixon RA, (1997) The oxidative burst in plant disease resistance. Annu Rev Plant Physiol Plant Mol Biol 48: 251-275.
50. Kortekamp A, (2006) Expression analysis of defence-related genes in grapevine after inoculation with a host and a non-host pathogens. Plant Physiol Bioch 44: 58-67.
51. Reid KE, Olsson N, Schlosser J, Peng F, Lund ST, (2006) An optimized grapevine RNA isolation procedure and statistical determination of reference genes for real-time RT-PCR during berry development. BMC Plant Biology 6: 27.
52. Belhadj A, Telef N, Saigne C, Cluzet S, Barrieu F, et al. (2008) Effect of methyl jasmonate in combination with carbohydrates on gene expression of PR proteins, stilbene and anthocyanin accumulation in grapevine cell cultures. Plant Physiol Bioch 46: 493-499.
53. Chang X, Heene E, Qiao F, Nick P, (2011) The Phytoalexin Resveratrol Regulates the Initiation of Hypersensitive Cell Death in Vitis Cell. PLoS ONE 6: e26405 Doi:10.1371/journal.pone.0026405.
54. Schmidt SM, Panstruga R, (2007) Cytoskeleton functions in plant-microbe interactions. Physiol Mol Plant P 71: 135-148.
55. Felix G, Regenass M, Boller T, (1993) Specific perception of subnanomolar concentrations of chitin fragments by tomato cells: induction of extracellular alkalinization, changes in protein phosphorylation, and establishment of a refractory state. Plant J 4: 307-316.
56. Di Gaspero G, Cipriani G, (2003) Nucleotide biding site/leucine-rich repeats, Pto-like, receptor-like kinases related to disease resistance in grapevine. Mol Genet Genomics 269: 612-623.
57. Haapalainen M, Engelhardt S, Küfner I, Li Chun-Mei, Nürnberger T, et al. (2011) Functional mapping of harpin HrpZ of Pseudomonas syringae reveals the sites responsible for protein oligomerization, lipid interactions and plant defence induction. Mol Plant Pathol 12: 151-166.
58. Hohenberger P, Eing C, Straessner R, Durst S, Frey W, et al. (2011) Plant actin controls membrane permeability. Biochim Biophys Acta 1808: 2304-2312.
59. Komis G, Illés P, Beck M, Šamaj J, (2011) Microtubules and mitogen-activated protein kinase signalling. Curr Opin Plant Biol 14: 650-657.
60. Wang S, Kurepa J, Hashimoto T, Smalle JA, (2011) Salt Stress-Induced Disassembly of Arabidopsis Cortical Microtubule Arrays Involves 26S Proteasome-Dependent Degradation of SPIRAL1. Plant Cell 23: 3412-3427.
61. Yalamanchili RD, Stratmann JW, (2002) Ultraviolet-B activates components of the systemin signalling pathway in Lycopersicon peruvianum suspension-cultured cells. J Biol Chem 277: 28424-28430.
62. Holley SR, Yalamanchili RD, Moura SD, Ryan CA, Stratmann JW, (2003) Convergence of signalling pathways induced by systemin, oligosaccharide elicitors, and ultraviolet-B radiation at the level of mitogen-activated protein kinases in Lycopersicon peruvianum suspension-cultured cells. Plant Physiology 132: 1728-1738.
63. Zhang A, Jiang M, Zhang J, Tan M, Hu X, (2006) Mitogen-activated protein kinase is involved in abscisic acid-Induced antioxidant defense and acts downstream of reactive oxygen species production in leaves of maize plants. Plant Physiology 141: 475-487.
64. Desikan R, Hancock JT, Ichimura K, Shinozaki K, Neill SJ, (2001) Harpin induces activation of the Arabidopsis mitogen-activated protein kinases AtMPK4 and AtMPK6. Plant Physiology 126: 1579-1587.
65. Nühse TS, Peck SC, Hirt H, Boller T, (2000) Microbial elicitors induce activation and dual phosphorylation of the Arabidopsis thaliana MAPK6. J Biol Chem 275: 7521-7526.
66. Mészáros T, Helfer A, Hatzimasoura E, Magyar Z, Serazetdinova L, et al. (2006) The Arabidopsis MAP kinase kinase MKK1 participates in defence responses to the bacterial elicitor flagellin. Plant J 48: 485-498.
67. Robatzek S, Chinchilla D, Boller T, (2006) Ligand-induced endocytosis of the pattern recognition receptor FLS2 in Arabidopsis. Gene Dev 20: 537-542.
68. Navarro L, Zipfel C, Rowland O, Keller I, Robatzek S, et al. (2004) Interplay between flg22 innate immune response, Avr9-race-specific defense response and other bacterial interactions. Plant Physiology 135: 1-16.
69. Torres MA, Jones JDG, Dangl JL, (2006) Reactive oxygen species signalling in response to pathogens. Plant Physiology 141: 373-378.
70. Zhang J, Shao F, Li Y, Cui H, Chen L, et al. (2007) A Pseudomonas syringae effector inactivates MAPKs to suppress PAMP-induced immunity in plants. Cell Host Microbe 1: 175-185.
71. Jeandet P, Douillet-Breuil AC, Bessis R, Debord S, Sbaghi M, et al. (2002) Phytoalexins from the Vitaceae: biosynthesis, phytoalexin gene expression in transgenic plants, antifungal activity, and metabolism. J Agr Food Chem 50: 2731-2741.
72. Adrian M, Jeandet P, Veneau J, Weston LA, Bessis R, (1997) Biological activity of resveratrol, a stilbenic compound from grapevines, against Botrytis cinerea, the causal agent for gray mold. J Chem Ecol 23: 1689-1702.
73. Bruno G, Sparapano L, (2006) Effects of three esca-associated fungi on Vitis vinifera L.: III. Enzymes produced by the pathogens and their role in fungus-to-plant or in fungus-to-fungus interactions. Physiol Mol Plant P 69: 182-194.
74. Celimene CC, Smith DR, Young RA, Stanosz GR, (2001) In vitro inhibition of Sphaeropsis sapinea by natural stilbenes. Phytochemistry 56: 161-165.
75. Pezet R, Gindro K, Viret O, Spring JL, (2004) Glycosylation and oxidative dimerization of resveratrol are respectively associated to sensitivity and resistance of grapevine cultivars to downy mildew. Physiol Mol Plant P 65: 297-303.
76. Tropf S, Lanz T, Rensing SA, Schröder J, Schröder G, (1994) Evidence that stilbene synthases have developed from chalcone synthases several times in the course of evolution. J Mol Evol 38: 610-618.
77. Bellin D, Peressotti E, Merdinoglu D, Wiedemann-Merdinoglu S, Adam-Blondon AF, et al. (2009) Resistance to Plasmopara viticola in grapevine 'Bianca' is controlled by a major dominant gene causing localised necrosis at the infection site. Theor Appl Genet 120: 163-176.
78. Casagrande K, Falginella L, Castellarin SD, Testolin R, Di Gaspero G, (2011) Defence responses in Rpv3-dependent resistance to grapevine downy mildew. Planta 234: 1097-1099.
79. Lai Z, Wang F, Zheng Z, Fan B, Chen Z, (2011) A critical role of autophagy in plant resistance to necrotrophic fungal pathogens. Plant J 66: 953-968.
80. Maisch J, Nick P, (2007) Actin in involved in auxin-dependent patterning. Plant Physiology 143: 1696-1704.
81. Gaff DF, Okong'O-Ogola O, (1971) The use of non-permeating pigments for testing the survival of cells. J Exp Bot 22: 756-758.