OCP3 is an important modulator of NPR1-mediated jasmonic acid-dependent induced defenses in Arabidopsis

BMC Plant Biology

Volumn 10, Issue , 2010, Pages

  Ramírez, Vicente ^a   Van der Ent, Sjoerd ^b   García Andrade, Javier ^a   Coego, Alberto ^a   Pieterse, Corné M J ^b   Vera, Pablo ^a  

^a Ciudad Politécnica de la Innovación   (Spain)

^b UTRECHT UNIVERSITY   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

ARABIDOPSIS; HYALOPERONOSPORA; PSEUDOMONAS; PSEUDOMONAS FLUORESCENS;

EID: 84860257922     PISSN: None     EISSN: 14712229     Source Type: Journal    
DOI: 10.1186/1471-2229-10-199     Document Type: Article

References (71)

1. Hardham AR, Jones DA, Takemoto D. Cytoskeleton and cell wall function in penetration resistance. Curr Opin Plant Biol 2007, 10(4):342-348. 10.1016/j.pbi.2007.05.001, 17627866.
2. Kunkel BN, Brooks DM. Cross talk between signaling pathways in pathogen defense. Current Opinion in Plant Biology 2002, 5(4):325-331. 10.1016/S1369-5266(02)00275-3, 12179966.
3. Pieterse CM, Leon-Reyes A, Van der Ent S, Van Wees SC. Networking by small-molecule hormones in plant immunity. Nat Chem Biol 2009, 5(5):308-316. 10.1038/nchembio.164, 19377457.
4. Robert-Seilaniantz A, Navarro L, Bari R, Jones JDG. Pathological hormone imbalances. Current Opinion in Plant Biology 2007, 10(4):372-379. 10.1016/j.pbi.2007.06.003, 17646123.
5. Thomma B, Penninckx I, Broekaert WF, Cammue BPA. The complexity of disease signaling in Arabidopsis. Current Opinion in Immunology 2001, 13(1):63-68. 10.1016/S0952-7915(00)00183-7, 11154919.
6. Pieterse CM, Dicke M. Plant interactions with microbes and insects: from molecular mechanisms to ecology. Trends Plant Sci 2007, 12(12):564-569. 10.1016/j.tplants.2007.09.004, 17997347.
7. Thaler JS, Owen B, Higgins VJ. The role of the jasmonate response in plant susceptibility to diverse pathogens with a range of lifestyles. Plant Physiol 2004, 135(1):530-538. 10.1104/pp.104.041566, 429405, 15133157.
8. Bostock RM. Signal crosstalk and induced resistance: straddling the line between cost and benefit. Annu Rev Phytopathol 2005, 43:545-580. 10.1146/annurev.phyto.41.052002.095505, 16078895.
9. Glazebrook J. Contrasting mechanisms of defense against biotrophic and necrotrophic pathogens. Annu Rev Phytopathol 2005, 43:205-227. 10.1146/annurev.phyto.43.040204.135923, 16078883.
10. Bari R, Jones JD. Role of plant hormones in plant defence responses. Plant Mol Biol 2009, 69(4):473-488. 10.1007/s11103-008-9435-0, 19083153.
11. Poelman EH, Broekgaarden C, Van Loon JJ, Dicke M. Early season herbivore differentially affects plant defence responses to subsequently colonizing herbivores and their abundance in the field. Mol Ecol 2008, 17(14):3352-3365. 10.1111/j.1365-294X.2008.03838.x, 18565114.
12. Stout MJ, Thaler JS, Thomma BP. Plant-mediated interactions between pathogenic microorganisms and herbivorous arthropods. Annu Rev Entomol 2006, 51:663-689. 10.1146/annurev.ento.51.110104.151117, 16332227.
13. Van der Putten WH, Vet LEM, Harvey JA, Wackers FL. Linking above- and belowground multitrophic interactions of plants, herbivores, pathogens, and their antagonists. Trends Ecol Evol 2001, 16(10):547-554.
14. Dong X. NPR1, all things considered. Curr Opin Plant Biol 2004, 7(5):547-552. 10.1016/j.pbi.2004.07.005, 15337097.
15. Nomura K, Melotto M, He SY. Suppression of host defense in compatible plant-Pseudomonas syringae interactions. Curr Opin Plant Biol 2005, 8(4):361-368. 10.1016/j.pbi.2005.05.005, 15936244.
16. Doherty HM, Selvendran RR, Bowles DJ. THE WOUND RESPONSE OF TOMATO PLANTS CAN BE INHIBITED BY ASPIRIN AND RELATED HYDROXYBENZOIC ACIDS. Physiological and Molecular Plant Pathology 1988, 33(3):377-384.
17. Penacortes H, Albrecht T, Prat S, Weiler EW, Willmitzer L. Aspirin Prevents Wound-Induced Gene-Expression in Tomato Leaves by Blocking Jasmonic Acid Biosynthesis. Planta 1993, 191(1):123-128.
18. Spoel SH, Koornneef A, Claessens SM, Korzelius JP, Van Pelt JA, Mueller MJ, Buchala AJ, Metraux JP, Brown R, Kazan K, et al. NPR1 modulates cross-talk between salicylate- and jasmonate-dependent defense pathways through a novel function in the cytosol. Plant Cell 2003, 15(3):760-770. 10.1105/tpc.009159, 150028, 12615947.
19. Koornneef A, Pieterse CM. Cross talk in defense signaling. Plant Physiol 2008, 146(3):839-844. 10.1104/pp.107.112029, 2259093, 18316638.
20. Reymond P, Farmer EE. Jasmonate and salicylate as global signals for defense gene expression. Current Opinion in Plant Biology 1998, 1(5):404-411. 10.1016/S1369-5266(98)80264-1, 10066616.
21. Spoel SH, Dong X. Making sense of hormone crosstalk during plant immune responses. Cell Host Microbe 2008, 3(6):348-351. 10.1016/j.chom.2008.05.009, 18541211.
22. van Loon LC, Bakker PA, Pieterse CM. Systemic resistance induced by rhizosphere bacteria. Annu Rev Phytopathol 1998, 36:453-483. 10.1146/annurev.phyto.36.1.453, 15012509.
23. Van SC, Van der Ent S, Pieterse CM. Plant immune responses triggered by beneficial microbes. Curr Opin Plant Biol 2008, 11(4):443-448. 10.1016/j.pbi.2008.05.005, 18585955.
24. Durrant WE, Dong X. Systemic acquired resistance. Annu Rev Phytopathol 2004, 42:185-209. 10.1146/annurev.phyto.42.040803.140421, 15283665.
25. Gaffney T. Requirement for salicylic acid for the induction of systemic acquired resistance. Science 1993, 261:754-756. 10.1126/science.261.5122.754, 17757215.
26. Pieterse CM, van Wees SC, van Pelt JA, Knoester M, Laan R, Gerrits H, Weisbeek PJ, van Loon LC. A novel signaling pathway controlling induced systemic resistance in Arabidopsis. Plant Cell 1998, 10(9):1571-1580. 10.1105/tpc.10.9.1571, 144073, 9724702.
27. Truman W, Bennett MH, Kubigsteltig I, Turnbull C, Grant M. Arabidopsis systemic immunity uses conserved defense signaling pathways and is mediated by jasmonates. Proc Natl Acad Sci USA 2007, 104(3):1075-80. 16, 10.1073/pnas.0605423104, 1783366, 17215350.
28. Attaran E, Zeier TE, Griebel T, Zeier J. Methyl salicylate production and jasmonate signaling are not essential for systemic acquired resistance in Arabidopsis. Plant Cell 2009, 21(3):954-71. 10.1105/tpc.108.063164, 2671706, 19329558.
29. Van der Ent S, Van Wees SC, Pieterse CM. Jasmonate signaling in plant interactions with resistance-inducing beneficial microbes. Phytochemistry 2009, 70(13-14):1581-1588. 10.1016/j.phytochem.2009.06.009, 19712950.
30. Conrath U, Beckers GJ, Flors V, Garcia-Agustin P, Jakab G, Mauch F, Newman MA, Pieterse CM, Poinssot B, Pozo MJ, et al. Priming: getting ready for battle. Mol Plant Microbe Interact 2006, 19(10):1062-1071. 10.1094/MPMI-19-1062, 17022170.
31. Pieterse CMJ, Van Pelt JA, Ton J, Parchmann S, Mueller MJ, Buchala AJ, Metraux JP, Van Loon LC. Rhizobacteria-mediated induced systemic resistance (ISR) in Arabidopsis requires sensitivity to jasmonate and ethylene but is not accompanied by an increase in their production. Physiological and Molecular Plant Pathology 2000, 57(3):123-134.
32. Beckers GJ, Jaskiewicz M, Liu Y, Underwood WR, He SY, Zhang S, Conrath U. Mitogen-activated protein kinases 3 and 6 are required for full priming of stress responses in Arabidopsis thaliana. Plant Cell 2009, 21(3):944-953. 10.1105/tpc.108.062158, 2671697, 19318610.
33. Jung HW, Tschaplinski TJ, Wang L, Glazebrook J, Greenberg JT. Priming in systemic plant immunity. Science 2009, 324(5923):89-91. 10.1126/science.1170025, 19342588.
34. Pozo MJ, Van Der Ent S, Van Loon LC, Pieterse CMJ. Transcription factor MYC2 is involved in priming for enhanced defense during rhizobacteria-induced systemic resistance in Arabidopsis thaliana. New Phytologist 2008, 180(2):511-523. 10.1111/j.1469-8137.2008.02578.x, 18657213.
35. Van der Ent S, Verhagen BW, Van Doorn R, Bakker D, Verlaan MG, Pel MJ, Joosten RG, Proveniers MC, Van Loon LC, Ton J, et al. MYB72 is required in early signaling steps of rhizobacteria-induced systemic resistance in Arabidopsis. Plant Physiol 2008, 146(3):1293-1304. 10.1104/pp.107.113829, 2259080, 18218967.
36. Pieterse CM, Van Loon LC. NPR1: the spider in the web of induced resistance signaling pathways. Curr Opin Plant Biol 2004, 7(4):456-464. 10.1016/j.pbi.2004.05.006, 15231270.
37. Mou Z, Fan W, Dong X. Inducers of plant systemic acquired resistance regulate NPR1 function through redox changes. Cell 2003, 113(7):935-944. 10.1016/S0092-8674(03)00429-X, 12837250.
38. Glazebrook J, Chen W, Estes B, Chang HS, Nawrath C, Metraux JP, Zhu T, Katagiri F. Topology of the network integrating salicylate and jasmonate signal transduction derived from global expression phenotyping. Plant J 2003, 34(2):217-228. 10.1046/j.1365-313X.2003.01717.x, 12694596.
39. Leon-Reyes A, Spoel SH, De Lange ES, Abe H, Kobayashi M, Tsuda S, Millenaar FF, Welschen RA, Ritsema T, Pieterse CM. Ethylene modulates the role of NONEXPRESSOR OF PATHOGENESIS-RELATED GENES1 in cross talk between salicylate and jasmonate signaling. Plant Physiol 2009, 149(4):1797-1809. 10.1104/pp.108.133926, 2663751, 19176718.
40. Johansson A, Staal J, Dixelius C. Early responses in the Arabidopsis-Verticillium longisporum pathosystem are dependent on NDR1, JA- and ET-associated signals via cytosolic NPR1 and RFO1. Mol Plant Microbe Interact 2006, 19(9):958-969. 10.1094/MPMI-19-0958, 16941900.
41. Stein E, Molitor A, Kogel KH, Waller F. Systemic resistance in Arabidopsis conferred by the mycorrhizal fungus Piriformospora indica requires jasmonic acid signaling and the cytoplasmic function of NPR1. Plant Cell Physiol 2008, 49(11):1747-1751. 10.1093/pcp/pcn147, 18842596.
42. Yuan Y, Zhong S, Li Q, Zhu Z, Lou Y, Wang L, Wang J, Wang M, Yang D, He Z. Functional analysis of rice NPR1-like genes reveals that OsNPR1/NH1 is the rice orthologue conferring disease resistance with enhanced herbivore susceptibility. Plant Biotechnol J 2007, 5(2):313-324. 10.1111/j.1467-7652.2007.00243.x, 17309686.
43. van Wees SC, de Swart EA, van Pelt JA, van Loon LC, Pieterse CM. Enhancement of induced disease resistance by simultaneous activation of salicylate- and jasmonate-dependent defense pathways in Arabidopsis thaliana. Proc Natl Acad Sci USA 2000, 97(15):8711-8716. 10.1073/pnas.130425197, 27013, 10890883.
44. Grant MR, Jones JD. Hormone (dis)harmony moulds plant health and disease. Science 2009, 324(5928):750-752. 10.1126/science.1173771, 19423816.
45. Coego A, Ramirez V, Gil MJ, Flors V, Mauch-Mani B, Vera P. An Arabidopsis homeodomain transcription factor, OVEREXPRESSOR OF CATIONIC PEROXIDASE 3, mediates resistance to infection by necrotrophic pathogens. Plant Cell 2005, 17(7):2123-2137. 10.1105/tpc.105.032375, 1167556, 15923348.
46. Chini A, Fonseca S, Fernandez G, Adie B, Chico JM, Lorenzo O, Garcia-Casado G, Lopez-Vidriero I, Lozano FM, Ponce MR, et al. The JAZ family of repressors is the missing link in jasmonate signalling. Nature 2007, 448(7154):666-671. 10.1038/nature06006, 17637675.
47. Thines B, Katsir L, Melotto M, Niu Y, Mandaokar A, Liu G, Nomura K, He SY, Howe GA, Browse J. JAZ repressor proteins are targets of the SCF(COI1) complex during jasmonate signalling. Nature 2007, 448(7154):661-665. 10.1038/nature05960, 17637677.
48. Xie DX, Feys BF, James S, Nieto-Rostro M, Turner JG. COI1: an Arabidopsis gene required for jasmonate-regulated defense and fertility. Science 1998, 280(5366):1091-1094. 10.1126/science.280.5366.1091, 9582125.
49. Ramirez V, Coego A, Lopez A, Agorio A, Flors V, Vera P. Drought tolerance in Arabidopsis is controlled by the OCP3 disease resistance regulator. Plant J 2009,
50. Jirage D, Tootle TL, Reuber TL, Frost LN, Feys BJ, Parker JE, Ausubel FM, Glazebrook J. Arabidopsis thaliana PAD4 encodes a lipase-like gene that is important for salicylic acid signaling. Proc Natl Acad Sci USA 1999, 96(23):13583-13588. 10.1073/pnas.96.23.13583, 23991, 10557364.
51. Lawton K, Weymann K, Friedrich L, Vernooij B, Uknes S, Ryals J. Systemic acquired resistance in Arabidopsis requires salicylic acid but not ethylene. Mol Plant Microbe Interact 1995, 8(6):863-870.
52. Cao H, Bowling SA, Gordon AS, Dong X. Characterization of an Arabidopsis Mutant That Is Nonresponsive to Inducers of Systemic Acquired Resistance. Plant Cell 1994, 6(11):1583-1592. 10.1105/tpc.6.11.1583, 160545, 12244227.
53. Melotto M, Underwood W, Koczan J, Nomura K, He SY. Plant stomata function in innate immunity against bacterial invasion. Cell 2006, 126(5):969-980. 10.1016/j.cell.2006.06.054, 16959575.
54. Beattie GA, Lindow SE. The secret life of foliar bacterial pathogens on leaves. Annu Rev Phytopathol 1995, 33:145-172. 10.1146/annurev.py.33.090195.001045, 18294082.
55. Zipfel C, Robatzek S, Navarro L, Oakeley EJ, Jones JD, Felix G, Boller T. Bacterial disease resistance in Arabidopsis through flagellin perception. Nature 2004, 428(6984):764-767. 10.1038/nature02485, 15085136.
56. Ton J, De Vos M, Robben C, Buchala A, Metraux JP, Van Loon LC, Pieterse CM. Characterization of Arabidopsis enhanced disease susceptibility mutants that are affected in systemically induced resistance. Plant J 2002, 29(1):11-21. 10.1046/j.1365-313x.2002.01190.x, 12060223.
57. van Wees SC, Luijendijk M, Smoorenburg I, van Loon LC, Pieterse CM. Rhizobacteria-mediated induced systemic resistance (ISR) in Arabidopsis is not associated with a direct effect on expression of known defense-related genes but stimulates the expression of the jasmonate-inducible gene Atvsp upon challenge. Plant Mol Biol 1999, 41(4):537-549. 10.1023/A:1006319216982, 10608663.
58. Corbineau F, Rudnicki RM, Come D. The Effects of Methyl Jasmonate on Sunflower (Helianthus-Annuus L) Seed-Germination and Seedling Development. Plant Growth Regulation 1988, 7(3):157-169.
59. Staswick PE, Su W, Howell SH. Methyl jasmonate inhibition of root growth and induction of a leaf protein are decreased in an Arabidopsis thaliana mutant. Proc Natl Acad Sci USA 1992, 89(15):6837-6840. 10.1073/pnas.89.15.6837, 49599, 11607311.
60. Franceschi VR, Grimes HD. Induction of soybean vegetative storage proteins and anthocyanins by low-level atmospheric methyl jasmonate. Proc Natl Acad Sci USA 1991, 88(15):6745-6749. 10.1073/pnas.88.15.6745, 52165, 11607204.
61. Tamari G, Borochov A, Weiss D. Methyl Jasmonate Induces Anthocyanin Synthesis and Flavonoid Gene-Transcription in Petunia Corollas. J Cell Biochem 1995, 505-505.
62. Spoel SH, Mou Z, Tada Y, Spivey NW, Genschik P, Dong X. Proteasome-mediated turnover of the transcription coactivator NPR1 plays dual roles in regulating plant immunity. Cell 2009, 137(5):860-872. 10.1016/j.cell.2009.03.038, 2704463, 19490895.
63. Tada Y, Spoel SH, Pajerowska-Mukhtar K, Mou Z, Song J, Wang C, Zuo J, Dong X. Plant immunity requires conformational changes [corrected] of NPR1 via S-nitrosylation and thioredoxins. Science 2008, 321(5891):952-956. 10.1126/science.1156970, 18635760.
64. Cao H, Li X, Dong X. Generation of broad-spectrum disease resistance by overexpression of an essential regulatory gene in systemic acquired resistance. Proc Natl Acad Sci USA 1998, 95(11):6531-6536. 10.1073/pnas.95.11.6531, 34547, 9601001.
65. Kinkema M, Fan W, Dong X. Nuclear localization of NPR1 is required for activation of PR gene expression. Plant Cell 2000, 12(12):2339-2350. 10.1105/tpc.12.12.2339, 102222, 11148282.
66. Sappl PG, Onate-Sanchez L, Singh KB, Millar AH. Proteomic analysis of glutathione S-transferases of Arabidopsis thaliana reveals differential salicylic acid-induced expression of the plant-specific phi and tau classes. Plant Mol Biol 2004, 54(2):205-219. 10.1023/B:PLAN.0000028786.57439.b3, 15159623.
67. Edwards K, Johnstone C, Thompson C. A simple and rapid method for the preparation of plant genomic DNA for PCR analysis. Nucleic Acids Res 1991, 19(6):1349. 10.1093/nar/19.6.1349, 333874, 2030957.
68. Mehrtens F, Kranz H, Bednarek P, Weisshaar B. The Arabidopsis transcription factor MYB12 is a flavonol-specific regulator of phenylpropanoid biosynthesis. Plant Physiol 2005, 138(2):1083-1096. 10.1104/pp.104.058032, 1150422, 15923334.
69. Pieterse CM, van Wees SC, Hoffland E, van Pelt JA, van Loon LC. Systemic resistance in Arabidopsis induced by biocontrol bacteria is independent of salicylic acid accumulation and pathogenesis-related gene expression. Plant Cell 1996, 8(8):1225-1237. 10.1105/tpc.8.8.1225, 161233, 8776893.
70. King EO, Ward MK, Raney DE. Two simple media for the demonstration of pyocyanin and fluorescin. J Lab Clin Med 1954, 44(2):301-307.
71. Koch E, Slusarenko A. Arabidopsis is susceptible to infection by a downy mildew fungus. Plant Cell 1990, 2(5):437-445. 10.1105/tpc.2.5.437, 159900, 2152169.