The role of nitric oxide in the interaction of Arabidopsis thaliana with the biotrophic fungi, Golovinomyces orontii and Erysiphe pisi

Frontiers in Plant Science

Volumn 4, Issue SEP, 2013, Pages

  Schlicht, Markus ^a   Kombrink, Erich ^a  

^a MAX PLANCK INSTITUTE FOR PLANT BREEDING RESEARCH   (Germany)

Author keywords

Disease resistance; Erysiphe pisi; Golovinomyces orontii; Plant defense signaling; Plant immunity; Plant microbe interaction; Powdery mildew

Indexed keywords

EID: 84897549407     PISSN: None     EISSN: 1664462X     Source Type: Journal    
DOI: 10.3389/fpls.2013.00351     Document Type: Article

References (82)

1. Arita, N. O., Cohen, M. F., Tokuda, G., and Yamasaki, H. (2007). Fluoro-metric detection of nitric oxide with diaminofluorescein (DAFs): applications and limitations for plant NO research in Nitric Oxide in Plant Growth, Development and Stress Physiology, eds L. Lamattina and J. C. Polacco (New York: Springer Verlag).
2. Asai, S., Mase, K., and Yoshioka, H. (2010). Role of nitric oxide and reactive oxygen species in disease resistance to necrotrophic pathogens. Plant Signal. Behav. 5, 872-874. doi: 10.4161/psb.5.7.11899
3. Asai, S., Ohta, K., and Yosh-ioka, H. (2008). MAPK signaling regulates nitric oxide and NADPH oxidase-dependent oxida-tive bursts in Nicotiana benthami-ana. Plant Cell 20, 1390-1406. doi: 10.1105/tpc.107.055855
4. Asai, S., and Yoshioka, H. (2009). Nitric oxide as a partner of reactive oxygen species participates in disease resistance to necrotrophic pathogen Botrytis cinerea in Nico-tiana benthamiana. Mol. Plant Microbe Interact. 22, 619-629. doi: 10.1094/MPMI-22-6-0619
5. Barroso, J. B., Corpas, F. J., Car-reras, A., Sandalio, L. M., Valder-rama, R., Palma, J. M., et al. (1999). Localization of nitric-oxide synthase in plant peroxisomes. J. Biol. Chem. 274, 36729-36733. doi: 10.1074/jbc.274.51.36729
6. Bartsch, M., Gobbato, E., Bednarek, P., Debey, S., Schultze, J. L., Bau-tor, J., et al. (2006). Salicylic acid-independent ENHANCED DISEASE SUSCEPTIBILITY1 signaling in Ara-bidopsis immunity and cell death is regulated by the monooxyge-nase FMO1 and the nudix hydrolase NUDT7. Plant Cell 18, 1038-1051. doi: 10.1105/tpc.105.039982
7. Bednarek, P., Pislewska-Bednarek, M., Svatoš, A., Schneider, B., Doubský, J., Mansurova, M., et al. (2009). A glucosinolate metabolism pathway in living plant cells mediates broad-spectrum antifungal defense. Science 323, 101-106. doi: 10.1126/science.1163732
8. Bellin, D., Asai, S., Delledonne, M., and Yoshioka, H. (2012). Nitric oxide as a mediator for defense responses. Mol. Plant Microbe Interact. 26, 271-277. doi: 10.1094/MPMI-09-12-0214-CR
9. Besson-Bard, A., Pugin, A., and Wen-dehenne, D. (2008). New insights into nitric oxide signaling in plants. Annu. Rev. Plant Biol. 59, 21-39. doi: 10.1146/annurev.arplant.59.032607. 092830
10. Boller, T., and 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. doi: 10.1146/annurev.arplant.57.032905. 105346
11. Chisholm, S. T., Coaker, G., Day, B., and Staskawicz, B. J. (2006). Host-microbe interactions: shaping the evolution of the plant immune response. Cell 124, 803-814. doi: 10.1016/j.cell.2006.02.008
12. Coll, N. S., Epple, P., and Dangl, J. L. (2011). Programmed cell death in the plant immune system. Cell Death Differ. 18, 1247-1256. doi: 10.1038/cdd.2011.37
13. Collins, N. C., Thordal-Christensen, H., Lipka, V., Bau, S., Kombrink, E., Qiu, J.-L., et al. (2003). SNARE-protein-mediated disease resistance at the plant cell wall. Nature 425, 973-977. doi: 10.1038/nature02076
14. Conrath, U., Amoroso, G., Köhle, H., and Sültemeyer, D. F. (2004). Non-invasive online detection of nitric oxide from plants and some other organisms by mass spectrom-etry. Plant J. 38, 1015-1022. doi: 10.1111/j.1365-313X.2004.02096.x
15. Corpas, F. J., Barroso, J. B., Carreras, A., Valderrama, R., Palma, J. M., León, A. M., et al. (2006). Constitutive arginine-dependent nitric oxide synthase activity in different organs of pea seedlings during plant development. Planta 224, 246-254. doi: 10.1007/s00425-005-0205-9
16. Corpas, F. J., Palma, J. M., Del Río, L. A., and Barroso, J. B. (2009). Evidence supporting the existence of L-arginine-dependent nitric oxide synthase activity in plants. New Phy-tol. 184, 9-14. doi: 10.1111/j.1469-8137.2009.02989.x
17. Delledonne, M., Xia, Y., Dixon, R. A., and Lamb, C. (1998). Nitric oxide functions as a signal in plant disease resistance. Nature 394, 585-588. doi: 10.1038/29087
18. Desikan, R., Griffiths, R., Hancock, J., and Neill, S. (2002). A new role for an old enzyme: nitrate reductase-mediated nitric oxide generation is required for abscisic acid-induced stomatal closure in Ara-bidopsis thaliana. Proc. Natl. Acad. Sci. U.S.A. 99, 16314-16318. doi: 10.1073/pnas.252461999
19. Deslandes, L., and Rivas, S. (2012). Catch me if you can: bacterial effectors and plant targets. Trends Plant Sci. 17, 644-655. doi: 10.1016/j.tplants.2012.06.011
20. Dodds, P. N., and Rathjen, J. P. (2010). Plant immunity: towards an integrated view of plant-pathogen interactions. Nat. Rev. Genet. 11, 539-548. doi: 10.1038/nrg2812
21. Durner, J., Wendehenne, D., and Klessig, D. F. (1998). Defense gene induction in tobacco by nitric oxide, cyclic GMP, and cyclic ADP-ribose. Proc. Natl. Acad. Sci. U.S.A. 95, 10328-10333. doi: 10.1073/pnas.95.17.10328
22. Ellis, C., Karafyllidis, I., and Turner, J. G. (2002). Constitutive activation of jasmonate signaling in an Arabidopsis mutant correlates with enhanced resistance to Erysiphe cichoracearum, Pseudomonas syringae, and Myzus persicae. Mol. Plant Microbe Interact. 15, 1025-1030. doi: 10.1094/MPMI.2002.15.10.1025
23. Floryszak-Wieczorek, J., Arasimow-icz, M., Milczarek, G., Jelen, H., and Jackowiak, H. (2007). Only an early nitric oxide burst and the following wave of secondary nitric oxide generation enhanced effective defence responses of pelargonium to a necrotrophic pathogen. New Phytol. 175, 718-730. doi: 10.1111/j.1469-8137.2007.02142.x
24. Gas, E., Flores-Pérez, U., Sauret-Güeto, S., and Rodríguez-Concepción, M. (2009). Hunting for plant nitric oxide synthase provides new evidence of a central role for plastids in nitric oxide metabolism. Plant Cell 21, 18-23. doi: 10.1105/tpc.108.065243
25. Glazebrook, J. (2005). Contrasting mechanisms of defense against biotrophic and necrotrophic pathogens. Annu. Rev. Phytopathol. 43, 205-227. doi: 10.1146/annurev.phyto.43.040204. 135923
26. Göhre, V., and Robatzek, S. (2008). Breaking the barriers: micro-bial effector molecules subvert plant immunity. Annu. Rev. Phytopathol. 46, 189-215. doi: 10.1146/annurev.phyto.46.120407. 110050
27. Göllner, K., Schweizer, P., Bai, Y., and Panstruga, R. (2008). Natural genetic resources of Ara-bidopsis thaliana reveal a high prevalence and unexpected phenotypic plasticity of RPW8-mediated powdery mildew resistance. New Phytol. 177, 725-742. doi: 10.1111/j.1469-8137.2007.02339.x
28. Gould, K. S., Lamotte, O., Klinguer, A., Pugin, A., and Wendehenne, D. (2003). Nitric oxide production in tobacco leaf cells: a generalized stress response? Plant Cell Environ. 26, 1851-1862. doi: 10.1046/j.1365-3040.2003.01101.x
29. Guo, F.-Q., and Crawford, N. M. (2005). Arabidopsis nitric oxide syn-thase1 is targeted to mitochondria and protects against oxidative damage and dark-induced senescence. Plant Cell 17, 3436-3450. doi: 10.1105/tpc.105.037770
30. Guo, F.-Q., Okamoto, M., and Crawford, N. M. (2003). Identification of a plant nitric oxide synthase gene involved in hormonal signaling. Science 302, 100-103. doi: 10.1126/sci-ence.1086770
31. Hardham, A. R., Jones, D. A., and Take-moto, D. (2007). Cytoskeleton and cell wall function in penetration resistance. Curr. Opin. Plant Biol. 10, 342-348. doi: 10.1016/j.pbi.2007.05.001
32. Jones, J. D. G., and Dangl, J. L. (2006). The plant immune system. Nature 444, 323-329. doi: 10.1038/nature05286
33. Koh, S., André, A., Edwards, H., Ehrhardt, D., and Somerville, S. (2005). Arabidopsis thaliana subcellular responses to compatible Erysiphe cichoracearum infections. Plant J. 44, 516-529. doi: 10.1111/j.1365-313X.2005.02545.x
34. Leitner, M., Vandelle, E., Gaupels, F., Bellin, D., and Delledonne, M. (2009). NO signals in the haze: nitric oxide signalling in plant defence. Curr. Opin. Plant Biol. 12, 451-458. doi: 10.1016/j.pbi.2009.05.012
35. Lindermayr, C., Sell, S., Müller, B., Leister, D., and Durner, J. (2010). Redox regulation of the NPR1-TGA1 system of Arabidopsis thaliana by nitric oxide. Plant Cell 22, 2894-2907. doi: 10.1105/tpc.109.066464
36. Lipka, V., Dittgen, J., Bednarek, P., Bhat, R., Wiermer, M., Stein, M., et al. (2005). Pre-and postinvasion defenses both contribute to non-host resistance in Arabidopsis. Science 310, 1180-1183. doi: 10.1126/sci-ence.1119409
37. Liu, G., Holub, E. B., Alonso, J. M., Ecker, J. R., and Fobert, P. R. (2005). An Arabidopsis NPR1-like gene, NPR4, is required for disease resistance. Plant J. 41, 304-318. doi: 10.1111/j.1365-313X.2004.02296.x
38. Micali, C., Göllner, K., Humphry, M., Consonni, C., and Panstruga, R. (2008). The powdery mildew disease of Arabidopsis: a paradigm for the interaction between plants and biotrophic fungi. Arabidopsis Book 6, e0115. doi: 10.1199/tab.0115
39. Mlíčková, K., Luhová, L., Lebeda, A., Mieslerová, B., and Peč, P. (2004). Reactive oxygen species generation and peroxidase activity during Oidium neolycopersici infection on Lycopersicon species. Plant Phys-iol. Biochem. 42, 753-761. doi: 10.1016/j.plaphy.2004.07.007
40. Modolo, L. V., Augusto, O., Almeida, I. M. G., Magalhaes, J. R., and Salgado, I. (2005). Nitrite as the major source of nitric oxide production by Arabidopsis thaliana in response to Pseudomonas syringae. FEBS Lett. 579, 3814-3820. doi: 10.1016/j.febslet.2005.05.078
41. Modolo, L. V., Augusto, O., Almeida, I. M. G., Pinto-Maglio, C. l. A. F., Oliveira, H. C., Seligman, K., et al. (2006). Decreased argi-nine and nitrite levels in nitrate reductase-deficient Arabidopsis thaliana plants impair nitric oxide synthesis and the hypersensitive response to Pseudomonas syringae. Plant Sci. 171, 34-40. doi: 10.1016/j.plantsci.2006.02.010
42. Moreau, M., Lee, G. I., Wang, Y., Crane, B. R., and Klessig, D. F. (2008). AtNOS/AtNOA1 is a functional Arabidopsis thaliana cGTPase and not a nitric-oxide synthase. J. Biol. Chem. 283, 32957-32967. doi: 10.1074/jbc.M804838200
43. Mur, L. A. J., Carver, T. L. W., and Prats, E. (2006). NO way to live; the various roles of nitric oxide in plant-pathogen interactions. J. Exp. Bot. 57, 489-505. doi: 10.1093/jxb/erj052
44. Murashige, T., and Skoog, F. (1962). A revised medium for rapid growth and bioassays with tobacco tissue cultures. Physiol. Plant 15, 473-497. doi: 10.1111/j.1399-3054.1962. tb08052.x
45. O'Connell, R. J., and Panstruga, R. (2006). Tête à tête inside a plant cell: establishing compatibility between plants and biotrophic fungi and oomycetes. New Phytol. 171, 699-718. doi: 10.1111/j.1469-8137.2006.01829.x
46. Oliveira, H. C., Saviani, E. E., Oliveira, J. F. P., and Salgado, I. (2010). Nitrate reductase-dependent nitric oxide synthesis in the defense response of Arabidopsis thaliana against Pseudomonas syringae. Trop. Plant Pathol. 35, 104-107. doi: 10.1590/S1982-56762010000200005
47. Perchepied, L., Balagué, C., Riou, C., Claudel-Renard, C., Rivière, N., Grezes-Besset, B., et al. (2010). Nitric oxide participates in the complex interplay of defense-related signaling pathways controlling disease resistance to Sclerotinia sclerotiorum in Arabidopsis thaliana. Mol. Plant Microbe Interact. 23, 846-860. doi: 10.1094/MPMI-23-7-0846
48. Piterková, J., Hofman, J., Mieslerová, B., Sedláøová, M., Luhová, L., Lebeda, A., et al. (2011). Dual role of nitric oxide in Solanum spp.- Oidium neolycopersici interactions. Environ. Exp. Bot. 74, 37-44. doi: 10.1016/j.envexpbot.2011.04.016
49. Piterková, J., PetřIvalský, M., Luhová, L., Mieslerová, B., Sedlářvá, M., and Lebeda, A. (2009). Local and systemic production of nitric oxide in tomato responses to powdery mildew infection. Mol. Plant Pathol. 10, 501-513. doi: 10.1111/j.1364-3703.2009.00551.x
50. Plotnikova, J. M., Reuber, T. L., Ausubel, F. M., and Pfister, D. H. (1998). Powdery mildew pathogene-sis of Arabidopsis thaliana. Mycologia 90, 1009-1016. doi: 10.2307/3761274
51. Prats, E., Carver, T. L. W., and Mur, L. A. J. (2008). Pathogen-derived nitric oxide influences formation of the appressorium infection structure in the phytopathogenic fungus Blume-ria graminis. Res. Microbiol. 159, 476-480. doi: 10.1016/j.resmic.2008. 04.001
52. Prats, E., Mur, L. A. J., Sanderson, R., and Carver, T. L. W. (2005). Nitric oxide contributes both to papilla-based resistance and the hypersensitive response in barley attacked by Blumeria graminis f. sp. hordei. Mol. Plant Pathol. 6, 65-78. doi: 10.1111/j.1364-3703.2004. 00266.x
53. Rafiqi, M., Ellis, J. G., Ludowici, V. A., Hardham, A. R., and Dodds, P. N. (2012). Challenges and progress towards understanding the role of effectors in plant-fungal interactions. Curr. Opin. Plant Biol. 15, 477-482. doi: 10.1016/j.pbi.2012.05.003
54. Rasul, S., Dubreuil-Maurizi, C., Lam-otte, O., Koen, E., Poinssot, B., Alcaraz, G., et al. (2012). Nitric oxide production mediates oligogalacturonide-triggered immunity and resistance to Botrytis cinerea in Arabidopsis thaliana. Plant Cell Environ. 35, 1483-1499. doi: 10.1111/j.1365-3040.2012.02505.x
55. Reuber, T. L., Plotnikova, J. M., Dewd-ney, J., Rogers, E. E., Wood, W., and Ausubel A, Frederick M. (1998). Correlation of defense gene induction defects with powdery mildew susceptibility in Arabidopsis enhanced disease susceptibility mutants. Plant J. 16, 473-485. doi: 10.1046/j.1365-313x.1998.00319.x
56. Rockel, P., Strube, F., Rockel, A., Wildt, J., and Kaiser, W. M. (2002). Regulation of nitric oxide (NO) production by plant nitrate reductase in vivo and in vitro. J. Exp. Bot. 53, 103-110. doi: 10.1093/jexbot/53.366.103
57. Saenz, G. S., and Taylor, J. W. (1999). Phylogeny of the Erysiphales (powdery mildews) inferred from internal transcribed spacer ribosomal DNA sequences. Can. J. Bot. 77, 150-168.
58. Samalova, M., Johnson, J., Illes, M., Kelly, S., Fricker, M., and Gurr, S. (2013). Nitric oxide generated by the rice blast fungus Magnaporthe oryzae drives plant infection. New Phytol. 197, 207-222. doi: 10.1111/j.1469-8137.2012.04368.x
59. Schmittgen, T. D., and Livak, K. J. (2008). Analyzing real-time PCR data by the comparative CT method. Nat. Protoc. 3, 1101-1108. doi: 10.1038/nprot.2008.73
60. Shi, H.-T., Li, R.-J., Cai, W., Liu, W., Wang, C.-L., and Lu, Y.-T. (2012). Increasing nitric oxide content in Arabidopsis thaliana by expressing rat neuronal nitric oxide synthase resulted in enhanced stress tolerance. Plant Cell Physiol. 53, 344-357. doi: 10.1093/pcp/pcr181
61. Stein, M., Dittgen, J., Sánchez-Rodríguez, C., Hou, B.-H., Molina, A., Schulze-Lefert, P., et al. (2006). Arabidopsis PEN3/PDR8, an ATP binding cassette transporter, contributes to nonhost resistance to inappropriate pathogens that enter by direct penetration. Plant Cell 18, 731-746. doi: 10.1105/tpc.105. 038372
62. Straus, M. R., Rietz, S., van Themaat, E., Bartsch, M., and Parker, J. E. (2010). Salicylic acid antagonism of EDS1-driven cell death is important for immune and oxidative stress responses in Arabidopsis. Plant J. 62, 628-640. doi: 10.1111/j.1365-313X.2010.04178.x
63. Stuible, H.-P., and Kombrink, E. (2004). The hypersensitive response and its role in disease resistance, in Fungal Disease Resistance in Plants - Biochemistry, Molecular Biology and Genetic Engineering, ed. Z. K. Punja (Binghamton, NY: Haworth Press), 57-92.
64. Suzuki, N., Kojima, H., Urano, Y., Kikuchi, K., Hirata, Y., and Nagano, T. (2002). Orthogonality of calcium concentration and ability of 4,5-diaminofluorescein to detect NO. J. Biol. Chem. 277, 47-49. doi: 10.1074/jbc.M108195200
65. Tada, Y., Spoel, S. H., Pajerowska-Mukhtar, K., Mou, Z., Song, J., Wang, C., et al. (2008). Plant immunity requires conformational changes of NPR1 via S-nitrosylation and thiore-doxins. Science 321, 952-956. doi: 10.1126/science.1156970
66. Takken, F. L. W., and Goverse, A. (2012). How to build a pathogen detector: structural basis of NB-LRR function. Curr. Opin. Plant Biol. 15, 375-384. doi: 10.1016/j.pbi.2012. 05.001
67. Vlot, A. C., Dempsey, D. M. A., and Klessig, D. F. (2009). Salicylic acid, a multifaceted hormone to combat disease. Annu. Rev. Phy-topathol. 47, 177-206. doi: 10.1146/ annurev.phyto.050908.135202
68. Vogel, J., and Somerville, S. (2000). Isolation and characterization of powdery mildew-resistant Arabidop-sis mutants. Proc. Natl. Acad. Sci. U.S.A. 97, 1897-1902. doi: 10.1073/pnas.030531997
69. Wang, J., and Higgins, V. J. (2005). Nitric oxide has a regulatory effect in the germination of conidia of Colletotrichum coccodes. Fungal Genet. Biol. 42, 284-292. doi: 10.1016/j.fgb.2004.12.006
70. Wang, Y.-Q., Feechan, A., Yun, B.-W., Shafiei, R., Hofmann, A., Taylor, P., et al. (2009). S-nitrosylation of AtSABP3 antagonizes the expression of plant immunity. J. Biol. Chem. 284, 2131-2137. doi: 10.1074/jbc.M806782200
71. Weßling, R., and Panstruga, R. (2012). Rapid quantification of plant-powdery mildew interactions by qPCR and conidiospore counts. Plant Methods 8, 35. doi: 10.1186/1746-4811-8-35
72. Wiermer, M., Feys, B. J., and Parker, J. E. (2005). Plant immunity: the EDS1 regulatory node. Curr. Opin. Plant Biol. 8, 383-389. doi: 10.1016/j.pbi.2005.05.010
73. Wilkinson, J. Q., and Crawford, N. M. (1993). Identification and characterization of a chlorate-resistant mutant of Arabidopsis thaliana with mutations in both nitrate reductase structural genes NIA1 and NIA2. Mol. Gen. Genet. 239, 289-297.
74. Williams, B., and Dickman, M. (2008). Plant programmed cell death: can't live with it; can't live without it. Mol. Plant Pathol. 9, 531-544. doi: 10.1111/j.1364-3703.2008.00473.x
75. Yamasaki, H., and Sakihama, Y. (2000). Simultaneous production of nitric oxide and peroxynitrite by plant nitrate reductase: in vitro evidence for the NR-dependent formation of active nitrogen species. FEBS Lett. 468, 89-92. doi: 10.1016/S0014-5793(00)01203-5
76. Yamasaki, H., Sakihama, Y., and Taka-hashi, S. (1999). An alternative pathway for nitric oxide production in plants: new features of an old enzyme. Trends Plant Sci. 4, 128-129. doi: 10.1016/S1360-1385(99)01393-X
77. Yoshioka, H., Mase, K., Yoshioka, M., Kobayashi, M., and Asai, S. (2011). Regulatory mechanisms of nitric oxide and reactive oxygen species generation and their role in plant immunity. Nitric Oxide 25, 216-221. doi: 10.1016/j.niox.2010.12.008
78. Yun, B.-W., Feechan, A., Yin, M., Saidi, N. B. B., Le Bihan, T., Yu, M., et al. (2011). S-nitrosylation of NADPH oxidase regulates cell death in plant immunity. Nature 478, 264-268. doi: 10.1038/nature10427
79. Zago, E., Morsa, S., Dat, J. F., Alard, P., Ferrarini, A., Inzé, D., et al. (2006). Nitric oxide- and hydrogen peroxide-responsive gene regulation during cell death induction in tobacco. Plant Physiol. 141, 404-411. doi: 10.1104/pp.106.078444
80. Zeidler, D., Zähringer, U., Gerber, I., Dubery, I., Hartung, T., Bors, W., et al. (2004). Innate immunity in Ara-bidopsis thaliana: lipopolysaccharides activate nitric oxide synthase (NOS) and induce defense genes. Proc. Natl. Acad. Sci. U.S.A. 101, 15811-15816. doi: 10.1073/pnas.0404536101
81. Zeier, J., Delledonne, M., Mishina, T., Severi, E., Sonoda, M., and Lamb, C. (2004). Genetic elucidation of nitric oxide signaling in incompatible plant-pathogen interactions. Plant Physiol. 136, 2875-2886. doi: 10.1104/pp.104.042499
82. Zimmerli, L., Stein, M., Lipka, V., Schulze-Lefert, P., and Somerville, S. (2004). Host and non-host pathogens elicit different jas-monate/ethylene responses in Arabidopsis. Plant J. 40, 633-646. doi: 10.1111/j.1365-313X.2004.02236.x