Dual role of nitric oxide in Solanum spp.-Oidium neolycopersici interactions

Environmental and Experimental Botany

Volumn 74, Issue 1, 2011, Pages 37-44

  Piterková, Jana ^a   Hofman, Jakub ^a   Mieslerová, Barbora ^a   Sedlářová, Michaela ^a   Luhová, Lenka ^a   Lebeda, Aleš ^a   Petřivalský, Marek ^a  

^a PALACKÝ UNIVERSITY   (Czech Republic)

Author keywords

Hypersensitive reaction; Nitric oxide; Oidium neolycopersici; Powdery mildew; Solanum spp.; Tomato

Indexed keywords

DICOTYLEDON; DISEASE RESISTANCE; FRUIT; FUNGAL DISEASE; GENOTYPE-ENVIRONMENT INTERACTION; GERMINATION; HOST-PATHOGEN INTERACTION; MOLECULAR ANALYSIS; NITRIC OXIDE; PATHOGENICITY; SCAVENGER;

ERYSIPHALES; LYCOPERSICON; LYCOPERSICON ESCULENTUM; OIDIUM NEOLYCOPERSICI; SOLANUM;

EID: 80054018713     PISSN: 00988472     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.envexpbot.2011.04.016     Document Type: Article

References (58)

1. Arasimowicz M., Floryszak-Wieczorek J. Nitric oxide as a bioactive signalling molecule in plant stress responses. Plant Sci. 2007, 172:876-887.
2. Asai S., Yoshioka H. Nitric oxide as a partner of reactive oxygen species participates in disease resistance to necrotrophic pathogen Botrytis cinerea in Nicotiana benthamiana. Mol. Plant: Microbe Interact. 2009, 22:619-629.
3. Asai S., Mase K., Yoshioka H. Role of nitric oxide and reactive oxide species in disease resistance to necrotrophic pathogens. Plant Signal. Behav. 2010, 5:872-874.
4. Barhoom S., Sharon A. cAMP regulation of " pathogenic" and " saprophytic" fungal spore germination. Fungal Gen. Biol. 2004, 41:317-326.
5. Bolwell G.P. Role of active oxygen species and NO in plant defence response. Curr. Opin. Plant Biol. 1999, 2:287-294.
6. Bolwell G.P., Wojtaszek P. Mechanisms for the generation of reactive oxygen species in plant defence - a broad perspective. Physiol. Mol. Plant Pathol. 1997, 51:347-366.
7. Conrath U., Amoroso G., Kohle H., Sultemeyer D.F. Noninvasive online detection of nitric oxide from plants and some other organisms by mass spectrometry. Plant J. 2004, 38:1015-1022.
8. del Río L.A., Corpas F.J., Barroso J.B. Nitric oxide and nitric oxide synthase activity in plants. Phytochemistry 2004, 65:783-792.
9. Danci O., Kolbert Z., Danci M., Bartha B., Erdei L. Relationship between virus traffic and nitric oxide (NO) production in tobacco roots. Acta Biol. Szeged. 2009, 53:17-20.
10. De Gara L., de Pinto M.C., Tommasi F. The antioxidant systems vis-à-vis reactive oxygen species during plant-pathogen interaction. Plant Physiol. Biochem. 2003, 41:863-870.
11. Delledonne M., Xia Y., Dixon R.A., Lamb C. Nitric oxide functions as a signal in plant disease resistance. Nature 1998, 394:585-588.
12. Delledonne M., Polverari A., Murgia I. The functions of nitric oxide-mediated signalling and changes in gene expression during the hypersensitive response. Antioxid. Redox Signal. 2003, 5:33-41.
13. Durner J., Wendehenne D., Klessig D.F. Defence gene induction in tobacco by nitric oxide, cyclic GMP, and cyclic ADP-ribose. Proc. Natl. Acad. Sci. U.S.A. 1998, 95:10328-10333.
14. Gessler N.N., Aver'yanov A.A., Belozerskaya T.A. Reactive oxygen species in regulation of fungal development. Biochemistry 2007, 72:1091-1109.
15. Golderer G., Werner E.R., Leitner S., Gröbner P., Werner-Felmayer G. Nitric oxide synthase is induced in sporulation of Physarum polycephalum. Genes Dev. 2001, 15:1299-1310.
16. Huang C., Groot T., Meijer-Dekens F., Niks R., Lindhout P. Hypersensitivity is the major mechanism of resistance to powdery mildew (Oidium lycopersicum) in Lycopersicon species. Eur. J. Plant Pathol. 1998, 104:399-407.
17. Johnson E.G., Sparks J.P., Dzikovski B., Crane B.R., Gibson D.M., Loria R. Plant-pathogenic Streptomyces species produce nitric oxide synthase-derived nitric oxide in response to host signals. Chem. Biol. 2008, 15:43-50.
18. Jones H., Whipps J.M., Gurr S.J. The tomato powdery mildew fungus Oidium neolycopersici. Mol. Plant Pathol. 2001, 2:303-309.
19. Keller T., Damude H.G., Werner D., Doerner P., Dixon R.A., Lamb C. 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.
20. Kiss L., Cook R.T.A., Saenz G.S., Cunnington J.H., Takamatsu S., Pascoe I., Bardin M., Nicot P.C., Sato Y., Rosman A.Y. Identification of two powdery mildew fungi, Oidium neolycopersici sp. nov. and O. lycopersici, infecting tomato in different parts of the world. Mycol. Res. 2001, 105:684-697.
21. Kunert J. Effect of nitric oxide donors on survival of conidia, germination and growth of Aspergillus fumigatus in vitro. Folia Microbiol. 1995, 40:238-244.
22. Lamattina L., Garcia-Mata C., Graziano M., Pagnussat G. Nitric oxide: the versatility of an extensive signal molecule. Annu. Rev. Plant Physiol. 2003, 54:109-136.
23. Lazar E.E., Wills R.B.H., Ho B.T., Harris A.M., Spohr L.J. Antifungal effect of gaseous nitric oxide on mycelium growth, sporulation and spore germination of the postharvest horticulture pathogens, Aspergillus niger, Monilinia fructicola and Penicillium italicum. Lett. Appl. Microbiol. 2008, 46:688-692.
24. Lebeda A., Mieslerová B. Variability in pathogenicity of Oidium neolycopersici on Lycopersicon species. J. Plant Dis. Protect. 2002, 109:129-141.
25. Lebeda A., Reinink K. Histological characterization of resistance in Lactuca saligna to lettuce downy mildew (Bremia lactucae). Physiol. Mol. Plant Pathol. 1994, 44:125-139.
26. Maier J., Hecker R., Rockel P., Ninnemann H. Role of nitric oxide synthase in the light-induced development of sporangiophores in Phycomyces blakesleeanus. Plant Physiol. 2001, 126:1321-1330.
27. Mieslerová B., Lebeda A. Taxonomy, distribution and biology of the tomato powdery mildew (Oidium lycopersici). J. Plant Dis. Protect. 1999, 106:140-157.
28. Mieslerová B., Lebeda A., Kennedy R., Novotný R. Comparative morphological studies on tomato powdery mildew (Oidium neolycopersici). Acta Phytopathol. Entomol. Hun. 2002, 37:57-74.
29. Mieslerová B., Lebeda A., Kennedy R. Variation in Oidium neolycopersici development on host and nonhost plant species and their tissue defence response. Ann. Appl. Biol. 2004, 144:237-248.
30. Mlíčková K., Luhová L., Lebeda A., Mieslerová B., Peč P. Reactive oxygen species generation and peroxidase activity during Oidium neolycopersici infection on Lycopersicon species. Plant Physiol. Biochem. 2004, 42:753-761.
31. Modolo L.V., Augusto O., Almeida I.M., Magalhaes J.R., Salgado I. Nitrite as the major source of nitric oxide production by Arabidopsis thaliana in response to Pseudomonas syringae. FEBS Lett. 2005, 579:3814-3820.
32. Mur L.A., Santosa I.E., Laarhoven L.J., Holton N.J., Harren F.J., Smith A.R. Laser photoacoustic detection allows in planta detection of nitric oxide in tobacco following challenge with avirulent and virulent Pseudomonas syringae pathovars. Plant. Physiol. 2005, 138:1247-1258.
33. Mur L.A., Carver T.L., Prats E. NO way to live; the various roles of nitric oxide in plant-pathogen interactions. J. Exp. Bot. 2006, 57:489-505.
34. Mur L.A.J., Kenton P., Lloyd A.J., Ougham H., Prats E. The hypersensitive response; the centenary is upon us but how much do we know?. J. Exp. Bot. 2008, 59:501-520.
35. Neill S.J., Desikan R., Clarke A., Hurst R.D., Hancock J.T. Hydrogen peroxide and nitric oxide as signalling molecules in plants. J. Exp. Bot. 2002, 53:1237-1247.
36. Neill S.J., Desikan R., Hancock J.T. Nitric oxide signalling in plants. New Phytol. 2003, 159:11-35.
37. Neill S., Bright J., Desikan R., Hancock J., Harrison J., Wilson I. Nitric oxide evolution and perception. J. Exp. Bot. 2008, 59:25-35.
38. Panstruga R. Establishing compatibility between plants and obligate biotrophic pathogens. Curr. Opin. Plant Biol. 2003, 6:320-326.
39. Piterková J., Petřivalský M., Luhová L., Mieslerová B., Sedlářová M., Lebeda A. Local and systemic production of nitric oxide in tomato responses to powdery mildew infection. Mol. Plant Pathol. 2009, 10:201-213.
40. Planchet E., Sonoda M., Zeier J., Kaiser W.M. Nitric oxide (NO) as an intermediate in the cryptogein induced hypersensitive response - a critical re-evaluation. Plant Cell Environ. 2006, 29:59-69.
41. Prats E., Mur L.A.J., Sanderson R., Carver T.L.W. Nitric oxide contributes both to papilla-based resistance and the hypersensitive response in barley attacked by Blumeria graminis f. sp. hordei. Mol. Plant Pathol. 2005, 6:65-78.
42. Prats E., Carver T.L.W., Mur L.A.J. Pathogen-derived nitric oxide influences formation of the appressorium infection structure in the phytopathogenic fungus Blumeria graminis. Res. Microbiol. 2008, 159:476-480.
43. Sedlářová M., Petřivalský M., Piterková J., Kočířová J., Luhová L., Lebeda A. Influence of nitric oxide and reactive oxygen species on development of lettuce downy mildew in Lactuca spp. Eur. J. Plant Pathol. 2011, 129:267-280.
44. Shetty N.P., Jørgensen H.J.L., Jensen J.D., Collinge D.B., Shetty H.S. Roles of reactive oxygen species in interactions between plants and pathogens. Eur. J. Plant Pathol. 2008, 121:267-280.
45. Tada Y., Mori T., Shinogi T., Yao N., Takahashi S., Betsuyaku S. Nitric oxide and reactive oxygen species do not elicit hypersensitive cell death but induce apoptosis in the adjacent cells during the defence response of oat. Mol. Plant Microbe Interact. 2004, 17:245-253.
46. Tománková K., Luhová L., Petřivalský M., Peč P., Lebeda A. Biochemical aspects of reactive oxygen species formation in the interaction between Lycopersicon spp. and Oidium neolycopersici. Physiol. Mol. Plant Pathol. 2006, 68:22-32.
47. Tucker S.L., Talbot N.J. Surface attachment and pre-penetration stage development by plant pathogenic fungi. Annu. Rev. Phytopathol. 2001, 39:385-417.
48. Turrion-Gomez J.L., Benito E.P. Flux of nitric oxide between the necrotrophic pathogen Botrytis cinerea and the host plant. Mol. Plant Pathol. 2011, 12. doi: 10.1111/j.1364-3703.2010.00695.x.
49. Wang J, Higgins V.J. Nitric oxide has a regulatory effect in the germination of conidia of Colletotrichum coccodes. Fungal Gen. Biol. 2005, 42:284-292.
50. Wendehenne D., Pugin A., Klessig D.F., Durner J. Nitric oxide: comparative synthesis and signalling in animal and plant cells. Trends Plant Sci. 2001, 4:177-183.
51. Wendehenne D., Durner J., Klessig D.F. Nitric oxide: a new player in plant signalling and defence responses. Curr. Opin. Plant Biol. 2004, 7:449-455.
52. Wilson I.D., Neill S.J., Hancock J.T. Nitric oxide synthesis and signalling in plants. Plant Cell. Environ. 2008, 31:622-631.
53. Xu J. MAP kinases in fungal pathogens. Fungal Gen. Biol. 2000, 31:137-152.
54. Yamasaki H., Sakihama Y., Takahashi S. An alternative pathway for nitric oxide production: new features of an old enzyme. Trends Plant Sci. 1999, 4:128-129.
55. Yoshioka H., Asai S., Yoshioka M., Kobayashi M. Molecular mechanisms of generation for nitric oxide and reactive oxygen species, and role of the radical burst in plant immunity. Mol. Cells 2009, 28:321-329.
56. Zaninotto F., La Camera S., Polverari A., Delledonne M. Cross talk between reactive nitrogen and oxygen species during the hypersensitive disease resistance response. Plant Physiol. 2006, 141:379-383.
57. Zeier J., Delledonne M., Mishina T., Severi E., Sonoda M., Lamb C. Genetic elucidation of nitric oxide signalling in incompatible plant-pathogen interactions. Plant Physiol. 2004, 136:2875-2888.
58. Zemojtel T., Frohlich A., Palmieri M.C., Kolanczyk M., Mikula I., Wyrwicz L.S., Wanker E.E., Mundlos S., Vingron M., Martasek P., Durner J. Plant nitric oxide synthase: a never-ending story?. Trends Plant Sci. 2006, 11:524-525.