Resistance of sunflower to the biotrophic oomycete Plasmopara halstedii is associated with a delayed hypersensitive response within the hypocotyls

Journal of Experimental Botany

Volumn 56, Issue 420, 2005, Pages 2683-2693

  Radwan, O ^a   Mouzeyar, S ^a   Venisse, J S ^a   Nicolas, P ^a   Bouzidi, M F ^a  

^a Diversity and Ecophysiology of Cereals   (France)

Author keywords

Defence related genes; Helianthus annuus; Hypersensitive reaction; Plasmopara halstedii

Indexed keywords

BIOCOMPATIBILITY; GENES; GROWTH KINETICS; MATHEMATICAL MODELS; PHOTOSYNTHESIS;

DEFENSE RELATED GENES; HELIANTHUS ANNUS; HYPERSENSITIVE REACTION; PLASMOPARA HALSTEDII;

PLANTS (BOTANY);

HYDROGEN PEROXIDE; SALICYLIC ACID;

ARTICLE; DRUG EFFECT; GENE; GENE EXPRESSION REGULATION; GENETICS; IMMUNOLOGY; METABOLISM; MICROBIOLOGY; OOMYCETES; PHYSIOLOGY; PLANT DISEASE; PLANT GROWTH; SEEDLING; SUNFLOWER;

GENE EXPRESSION REGULATION, PLANT; GENES, PLANT; HELIANTHUS; HYDROGEN PEROXIDE; HYPOCOTYL; OOMYCETES; PLANT DISEASES; SALICYLIC ACID; SEEDLING;

HELIANTHUS; HELIANTHUS ANNUUS; NICOTIANA TABACUM; OOMYCETES; PERONOSPORA FARINOSA; PLASMOPARA HALSTEDII;

EID: 24944495783     PISSN: 00220957     EISSN: None     Source Type: Journal    
DOI: 10.1093/jxb/eri261     Document Type: Article

References (52)

1. Alvarez ME, Pennell RI, Meijer PJ, Ishikawa A, Dixon RA, Lamb C. 1998. Reactive oxygen intermediates mediate a systemic signal network in the establishment of plant immunity. Cell 92, 773-784.
2. Apostol I, Heinstein PF, Low PS. 1989. Rapid stimulation of an oxidative bust during elicitation of cultured plant cells: role in defense and signal transduction. Plant Physiology 90, 109-116.
3. Atkinson MM, Huang JS, Knopp JA. 1985. Hypersensitivity of suspension-cultured tobacco cells to pathogenic bacteria. Phytopathology 75, 1270-1274.
4. Bendahmane A, Kanyuka K, Baulcombe DC. 1999. The Rx gene from potato controls separate virus resistance and cell death responses. The Plant Cell 11, 781-792.
5. Bogorad L, Gubbins EJ, Krebbers E, et al. 1983. Cloning and physical mapping of maize plastid genes. Methods in Enzymology 97, 524-555.
6. Bradley DJ, Kjellbom P, Lamb CJ. 1992. Elicitor- and wound-induced oxidative cross-linking of a proline-rich plant cell wall protein: a novel, rapid defense response. Cell 70, 21-30.
7. Broekaert WF, Terras FR, Cammue BP, Osborn RW. 1995. Plant defensins: novel antimicrobial peptides as components of the host defense system. Plant Physiology 108, 1353-1358.
8. Cao H, Bowling SA, Gordon S, Dong X. 1994. Characterization of an Arabidopsis mutant that is non-responsive to inducers of systemic acquired resistance. The Plant Cell 6, 1583-1592.
9. Cao H, Glazebrook J, Clarke JD, Volko S, Dong X. 1997. The Arabidopsis NPR1 gene that controls systemic acquired resistance encodes a novel protein containing ankyrin repeats. Cell 88, 57-63.
10. Cao H, Li X, Dong X. 1998. Generation of broad-spectrum disease resistance by overexpression of an essential regulatory gene in systemic acquired resistance. Proceedings of the National Academy of Sciences, USA 95, 6531-6536.
11. Century KS, Holub EB, Staskawicz BJ. 1995. NDR1, a locus of Arabidopsis thaliana that is required for disease resistance to both a bacterial and a fungal pathogen. Proceedings of the National Academy of Sciences, USA 92, 6597-6601.
12. Coffeen WC, Wolpert TJ. 2004. Purification and characterization of serine proteases that exhibit caspase-like activity and are associated with programmed cell death in Avena sativa. The Plant Cell 16, 857-873.
13. Concetta de Pinto M, Tommasi F, De Gara L. 2002. Changes in the antioxidant systems as part of the signaling pathway responsible for the programmed cell death activated by nitric oxide and reactive oxygen species in tobacco bright-yellow 2 cells. Plant Physiology 130, 698-708.
14. Dangl JL, Dietrich RA, Richberg MH. 1996. Death don't have no mercy: cell death programs in plant-microbe interactions. The Plant Cell 8, 1793-1807.
15. del Pozo O, Lam E. 2003. Expression of the baculovirus p35 protein in tobacco affects cell death progression and compromises N gene-mediated disease resistance response to Tobacco Mosaic Virus. Molecular Plant-Microbe Interactions 16, 485-494.
16. del Pozo O, Lam E. 1998. Caspases and programmed cell death in the hypersensitive response of plants to pathogens. Current Biology 8, 1129-1132.
17. Delledonne M, Xia Y, Dixon RA, Lamb C. 1998. Nitric oxide functions as a signal in plant disease resistance. Nature 394, 585-588.
18. Delledonne M, Zeier J, Marocco A, Lamb C. 2001. Signal interactions between nitric oxide and reactive oxygen intermediates in the plant hypersensitive disease resistance response. Proceedings of the National Academy of Sciences, USA 6, 13454-13459.
19. Dempsey DA, Shah J, Klessing DF. 1999. Salicylic acid and disease resistance in plants. Critical Reviews in Plant Sciences 18, 547-575.
20. Desikan R, A-H-Mackemess S, Hancock JT, Neill SJ. 2001. Regulation of Arabidopsis transcriptome by oxidative stress. Plant Physiology 127, 159-172.
21. Fitzgerald HA, Chern MS, Navarre R, Ronald PC. 2004. Overexpression of (At)NPR1 in rice leads to a BTH- and environment-induced lesion-mimic/cell death phenotype. Molecular Plant-Microbe Interactions 17, 140-151.
22. Gray AB, Sackston WE. 1985. Early stages of infection of resistant and susceptible sunflower downy mildew. Canadian Journal of Botany 46, 5-10.
23. Gulya TJ, Sackston WE, Viranyi F, Masirevic S, Rashid KY. 1991. New races of the sunflower downy mildew pathogen (Plasmopara halstedii) in Europe and North and South America. Journal of Phytopathology 132, 303-311.
24. Hammond-Kosack KE, Jones JDG. 1996. Resistance gene-dependent plant defense responses. The Plant Cell 8, 1773-1791.
25. Hammond-Kosack KE, Silverman P, Raskin I, Jones JDG. 1996. Race-specific elicitors of Cladosporium fulvum induce changes in cell morphology and the synthesis of emylene and salicylic acid in tomato plants carrying the corresponding Cf disease resistance gene. Plant Physiology 110, 1381-1394.
26. Hermanns M, Slusarenko AJ, Schlaich NL. 2003. Organ-specificity in a plant disease is determined independently of R gene signalling. Molecular Plant-Microbe Interactions 16, 752-759.
27. Holub EB, Beynon JL. 1997. Symbiology of mouse-ear cress (Arabidopsis thaliana) and oomycetes. Advances in Botanical Research 24, 227-273.
28. Hu X, Bideney DL, Yalpani N, Duvick JP, Crasta O, Folkerts O, Lu G. 2003. Overexpression of gene encoding hydrogen peroxide-generating oxalate oxidase evokes defense responses in sunflower. Plant Physiology 133, 170-181.
29. Hu X, Reddy AS. 1997. Cloning and expression of a PR5-like protein from Arabidopsis: inhibition of fungal growth by bacterially expressed protein. Plant Molecular Biology 34, 949-959.
30. Jakobek JL, Lindgren PB. 1993. Generalized induction of defense responses in bean is not correlated with the induction of the hypersensitive reaction. The Plant Cell 5, 49-56.
31. Lamb C, Dixon RA. 1997. The oxidative burst in plant disease resistance. Annual Review of Plant Physiology and Plant Molecular Biology 48, 251-275.
32. Lamb CJ, Lawton MA, Dron M, Dixon RA. 1989. Signals and transduction mechanisms for activation of plant defences against microbial attack. Cell 56, 215-224.
33. Morrissey LP, Osbourn AE. 1999. Fungal resistance to plant antibiotics as a mechanism of pathogenesis. Microbiology and Molecular Biology Reviews 63, 708-724.
34. Mou Z, Fan W, Dong X. 2003. Inducers of plant systemic acquired resistance regulate NPR1 function through redox changes. Cell 113, 815-816.
35. Mouzeyar S, Tourvieille De Labrouhe D, Vear F. 1993. Histopathological studies of resistance of sunflower (Helianthus annuus L.) to downy mildew (Plasmopara halstedii). Journal Phytopathology 139, 289-297.
36. Mouzeyar S, Tourvieille De Labrouhe D, Vear F. 1994. Effect of host-race combination on resistance of sunflower (Helianthus annuus L.) to downy mildew (Plasmopara halstedii). Journal of Phytopathology 141, 249-258.
37. Pieterse CM J, van Wees SCM, van Pelt JA, Knoester M, Lean R, Gerrits H, Weisbeek PJ, van Loon LC. 1998. A novel signaling pathway controlling induced systemic resistance in Arabidopsis. The Plant Cell 10, 1571-1480.
38. Pontier D, Gan S, Amasino RM, Roby D, Lam E. 1999. Markers for hypersensitive response and senescence show distinct patterns of expression. Plant Molecular Biology 39, 1243-1255.
39. Pontier D, Godiard L, Marco Y, Roby D. 1994. HSR203J, a tobacco gene whose activation is rapid, highly localized and specific for incompatible plant/pathogen interactions. The Plant Journal 5, 507-521.
40. Pontier D, Tronchet M, Rogowski P, Lam E, Roby D. 1998. Activation of hsr203, a plant gene expressed during incompatible plant-pathogen interactions, is correlated with programmed cell death. Molecular Plant-Microbe Interactions 11, 544-554.
41. Radwan O, Bouzidi MF, Nicolas P, Mouzeyar S. 2004. Development of PCR markers for the P15/P18 locus for resistance to Plasmopara halstedii in sunflower, Helianthus annuus L. from complete CC-NBS-LRR sequences. Theoretical and Applied Genetics 109, 176-185.
42. Radwan O, Bouzidi MF, Vear F, Philippon J, Tourvieille de Labrouhe D, Nicolas P, Mouzeyar S. 2003. Identification of non-TIR-NBS-LRR markers linked to PL5/PL8 locus for resistance to downy mildew in sunflower. Theoretical and Applied Genetics 106, 1438-1446.
43. Sackston WE. 1992. Cotyledon Limited Infection (CLI) and Leaf Disk Immersion (LDI) inoculation of sunflower by downy mildew (Plasmopara halstedii). In: Proceedings of the 13th Sunflower International Conference, Pisa, Italy, 840-848.
44. Sesma A, Osbourn AE. 2004. The rice leaf blast pathogen undergoes developmental processes typical of root-infecting fungi. Nature 431, 516-517.
45. Smith CJ. 1996. Accumulation of phytoalexins defence mechanism and stimulus response system. The New Phytologist 132, 1-45.
46. Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgens DG. 1997. The CLUSTAL-X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Research 25, 4876-4882.
47. 2 accumulation in papillae and hypersensitive response during the barley-powdery mildew interaction. The Plant Journal 11, 1187-1194.
48. Torres MA, Dangl JL, Jones JDG. 2002. Arabidopsis gp91 phox homologs AtrbohD and AtrbohF are required for accumulation of reactive oxygen intermediates in the plant defense response. Proceedings of the National Academy of Sciences, USA 8, 517-522.
49. Tronchet M, Ranty B, Marco Y, Roby D. 2001. Hsr203 antisense suppression in tobacco accelerates development of hypersensitive cell death. The Plant Journal 27, 115-127.
50. Viranyi F, Mohamed SA. 1985. Factors associated with downy mildew resistance in sunflower. Acta Phytopathologica Academica Sciencia Hungarica 20, 137-139.
51. Vranceanu V, Pirvu N, Stoenescu FL. 1981. New sunflower downy mildew resistance genes and their management. Helia 4, 23-27.
52. Yu IC, Parker J, Bent AF. 1998. Gene-for-gene disease resistance without the hypersensitive response in Arabidopsis dnd1 mutant. Proceedings of the National Academy of Sciences, USA 95, 7819-7824.