UV-induced DNA damage promotes resistance to the biotrophic pathogen Hyaloperonospora parasitica in arabidopsis

Plant Physiology

Volumn 148, Issue 2, 2008, Pages 1021-1031

  Kunz, Bernard A ^a   Dando, Paige K ^a   Grice, Desma M ^a,b   Mohr, Peter G ^a,c   Schenk, Peer M ^b   Cahill, David M ^a  

^a DEAKIN UNIVERSITY   (Australia)

^b UNIVERSITY OF QUEENSLAND   (Australia)

^c UNIVERSITY OF ARIZONA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARABIDOPSIS; ARABIDOPSIS THALIANA; HYALOPERONOSPORA PARASITICA; PERONOSPORACEAE;

EID: 57749117109     PISSN: 00320889     EISSN: 15322548     Source Type: Journal    
DOI: 10.1104/pp.108.125435     Document Type: Article

References (105)

1. A-H-Mackerness S, John CF, Jordan B, Thomas B (2001) Early signaling components in ultraviolet-B responses: distinct roles for different reactive oxygen species and nitric oxide. FEBS Lett 489: 237-242
2. Allen RL, Bittner-Eddy PD, Grenville-Briggs LJ, Meitz JC, Rehmany AP, Rose LE, Beynon JL (2004) Host-parasite coevolutionary conflict between Arabidopsis and downy mildew. Science 306: 1957-1960
3. Birrell GW, Giaever G, Chu AM, Davis RW, Brown JM (2001) A genomewide screen in Saccharomyces cerevisiae for genes affecting UV radiation sensitivity. Proc Natl Acad Sci USA 98: 12608-12613
4. Bonomelli A, Mercier L, Franchel J, Baillieul F, Benizri E, Mauro MC (2004) Response of grapevine defences to UV-C exposure. Am J Enol Vitic 55: 51-59
5. Borie B, Jeandet P, Parize PA, Bessis R, Adrian M (2004) Resveratrol and stilbene synthase mRNA production in grapevine leaves treated with biotic and abiotic phytoalexin elicitors. Am J Enol Vitic 55: 60-64
6. Brash DE (1988) UV mutagenic photoproducts in Escherichia coli and human cells: a molecular genetics perspective on human skin cancer. Photochem Photobiol 48: 59-66
7. Brederode FT, Linthorst HJ, Bol JF (1991) Differential induction of acquired resistance and PR gene expression in tobacco by virus infection, ethephon treatment, UV light and wounding. Plant Mol Biol 17: 1117-1125
8. Britt AB, Chen JJ, Wykoff D, Mitchell D (1993) A UV-sensitive mutant of Arabidopsis defective in the repair of pyrimidine-pyrimidinone (6-4) dimers. Science 261: 1571-1574
9. Britt AB, Fiscus E (2003) Growth responses of Arabidopsis DNA repair mutants to solar irradiation. Physiol Plant 118: 183-192
10. Brosché M, Strid Å (2003) Molecular events following perception of ultraviolet-B radiation by plants. Physiol Plant 117: 1-10
11. Brown JE, Lu TY, Stevens C, Khan VA, Lu JY, Wilson CL, Collins DJ, Wilson MA, Igwegbe ECK, Chalutz E, et al (2001) The effect of low dose ultraviolet light-C seed treatment on induced resistance in cabbage to black rot (Xanthomonas campestris pv. Campestris). Crop Prot 20: 873-883
12. Casati P, Walbot V (2004) Rapid transcriptome responses of maize (Zea mays) to UV-B in irradiated and shielded tissues. Genome Biol 5: R16
13. Channon AG (1981) Downy mildew of Brassicas. In DM Spencer, ed, The Downy Mildews. Academic Press, London, pp 321-329
14. Chen JJ, Mitchell DL, Britt AB (1994) A light-dependent pathway for the elimination of UV-induced pyrimidine (6-4) pyrimidinone photoproducts in Arabidopsis. Plant Cell 6: 1311-1317
15. Chisholm ST, Coaker G, Day B, Staskawicz BJ (2006) Host-microbe interactions: shaping the evolution of the plant immune response. Cell 124: 803-814
16. Conrath U (2006) Systemic acquired resistance. Plant Sign Behav 1: 179-184
17. Dangl JL, Holub EB, Debener T, Lehnackers H, Ritter C, Crute IR (1992) Genetic definition of loci involved in Arabidopsis pathogen interactions. In C Koncz, N Chua, J Schell, eds, Methods in Arabidopsis Research. World Scientific Publishing, Singapore, pp 393-418
18. Dangl JL, Jones JDG (2001) Plant pathogens and integrated defence responses to infection. Nature 411: 826-833
19. De Beer D, Joubert E, Gelderblom WCA, Manley M (2002) Phenolic compounds: a review of their possible role as in vivo antioxidants of wine. South African J Enol Viticul 23: 48-61
20. de Capdeville G, Wilson CL, Beer SV, Aist JA (2002) Alternative disease control agents induce resistance to blue mold in harvested 'red delicious' apple fruit. Phytopathology 92: 900-908
21. Demple B, Harrison L (1994) Repair of oxidative damage to DNA: enzymology and biology. Annu Rev Biochem 63: 915-948
22. Dianov GL, Thybo T, Dianova II, Lipinski LJ, Bohr VA (2000) Single nucleotide patch excision repair is the major pathway for removal of thymine glycol from DNA in human cell extracts. J Biol Chem 275: 11809-11813
23. Dodds PN, Lawrence GJ, Catanzariti AM, The T, Wang CIA, Ayliffe MA, Kobe B, Ellis JG (2006) Direct protein interaction underlies gene-forgene specificity and coevolution of the flax resistance genes and flax avirulence genes. Proc Natl Acad Sci USA 103: 8888-8893
24. Doetsch PW, Zasatawny TH, Martin AM, Dizdaroglu M (1995) Monomeric base damage products from adenine, guanine and thymine induced by exposure of DNA to ultraviolet radiation. Biochemistry 34: 737-742
25. Donofrio NM, Delaney TP (2001) Abnormal callose response phenotype and hypersusceptibility to Peronospora parasitica in defense-compromised Arabidopsis nim1-1 and salicylate hydroxylase-expressing plants. Mol Plant Microbe Interact 14: 439-450
26. Durrant WE, Dong X (2004) Systemic acquired resistance. Annu Rev Phytopathol 42: 185-209
27. El Ghaouth A, Wilson CL, Callahan AM (2003) Induction of chitinase, β-1,3-glucanase, and phenylalanine ammonia lyase in peach fruit by UV-C treatment. Phytopathology 93: 349-355
28. Fidantsef AL, Mitchell DL, Britt AB (2000) The Arabidopsis UVH1 gene is a homolog of the yeast repair endonuclease RAD1. Plant Physiol 124: 579-586
29. Filkowski J, Kovalchuk O, Kovalchuk I (2004) Genome stability of vtc1, tt4, and tt5 Arabidopsis thaliana mutants impaired in protection against oxidative stress. Plant J 38: 60-69
30. Flor HH (1971) Current status of the gene-for-gene concept. Annu Rev Phytopathol 9: 275-296
31. Foster R, Chua NH (1999) An Arabidopsis mutant with deregulated ABA gene expression: implications for negative regulator function. Plant J 17: 363-372
32. Foyer CH, Descouvieres P, Kunert KJ (1994) Protection against oxygen radicals: an important defense mechanism studied in transgenic plants. Plant Cell Environ 17: 507-523
33. Friedberg EC, Walker GC, Siede W, Wood RD, Schultz RA, Ellenberger T (2006) DNA Repair and Mutagenesis. American Society for Microbiology, Washington, DC
34. 2+ and stimulates gene expression in transgenic parsley cell cultures. Plant J 20: 209-227
35. Frohnmeyer H, Staiger D (2003) Ultraviolet-B radiation-mediated responses in plants. Balancing damage and protection. Plant Physiol 133: 1420-1428
36. Gallego F, Fleck O, Li A, Wyrzykowska J, Tinland B (2000) AtRAD1, a plant homologue of human and yeast nucleotide excision repair endonucleases, is involved in dark repair of UV damages and recombination. Plant J 21: 507-518
37. Green R, Fluhr R (1995) UV-B-induced PR-1 accumulation is mediated by active oxygen species. Plant Cell 7: 203-212
38. Gunasekera TS, Paul ND, Ayres PG (1997) The effects of ultraviolet-B (UV-B: 290-320nm) radiation on blister blight disease of tea (Camellia sinensis). Plant Pathol 46: 179-185
39. Hefner E, Preuss SB, Britt AB (2003) Arabidopsis mutants sensitive to gamma irradiation include the homologue of the human repair gene ERCC1. J Exp Bot 54: 669-680
40. Holley SR, Yalamanchill RD, Moura DS, 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 Physiol 132: 1728-1738
41. Holub EB, Beynon JL, Crute IR (1994) Phenotypic and genotypic characterisation of interactions between isolates of Peronospora parasitica and accessions of Arabidopsis thaliana. Mol Plant Microbe Interact 7: 223-239
42. Jenkins GI, Brown BA (2007) UV-B perception and signal transduction. In GC Whitelam, KJ Halliday, eds, Light and Plant Development, Vol 30. Blackwell Publishing, Oxford, pp 155-182
43. Jenkins ME, Harlow GR, Liu Z, Shotwell MA, Ma J, Mount DW (1995) Radiation-sensitive mutants of Arabidopsis thaliana. Genetics 140: 725-732
44. Jiang CZ, Yee J, Mitchell DL, Britt AB (1997a) Photorepair mutants of Arabidopsis. Proc Natl Acad Sci USA 94: 7441-7445
45. Jiang CZ, Yen CN, Cronin K, Mitchell D, Britt AB (1997b) UV- and gamma-radiation sensitive mutants of Arabidopsis thaliana. Genetics 147: 1401-1409
46. Jones JD, Dangl JL (2006) The plant immune system. Nature 444: 323-329
47. Kalbin G, Hidema J, Brosché M, Kumagai T, Bornman JF, Strid Å (2001) UV-B-induced DNA damage and expression of defence genes under UV-B stress: tissue-specific molecular marker analysis in leaves. Plant Cell Environ 24: 983-990
48. Kobayashi N, Katsumi S, Imoto K, Nakagawa A, Miyagawa S, Furumura M, Mori T (2001) Quantitation and visualization of ultraviolet-induced DNA damage using specific antibodies. Pigment Cell Res 14: 94-102
49. Koch E, Slusarenko A (1990) Arabidopsis is susceptible to infection by a downy mildew fungus. Plant Cell 2: 437-445
50. Koornneef M (1990) Mutations affecting testa colour in Arabidopsis. Arabidopsis Inf Serv 28: 1-4
51. Kucera B, Leubner-Metzger G, Wellmann E (2003) Distinct ultravioletsignalling pathways in bean leaves. DNA damage is associated with β-1,3-glucanase gene induction, but not with flavonoid formation. Plant Physiol 133: 1445-1452
52. Landry LG, Chapple CCS, Last RL (1995) Arabidopsis mutants lacking phenolic sunscreens exhibit enhanced ultraviolet-B injury and oxidative damage. Plant Physiol 109: 1159-1166
53. Landry LG, Stapleton AE, Lim J, Hoffman P, Hays JB, Walbot V, Last RL (1997) An Arabidopsis photolyase mutant is hypersensitive to ultraviolet-B radiation. Proc Natl Acad Sci USA 94: 328-332
54. Le Page F, Kwoh EE, Avrutskaya A, Gentil A, Leadon SA, Sarasin A, Cooper PK (2000) Transcription-coupled repair of 8-oxoguanine: requirement for XPG, TFIIH, and CSB and implications for Cockayne Syndrome. Cell 101: 159-171
55. Li J, Ou-Lee TM, Raba R, Amundson RG, Last RL (1993) Arabidopsis flavonoid mutants are hypersensitive to UV-B irradiation. Plant Cell 5:171-179
56. Liu Z, Hall JD, Mount DW (2001) Arabidopsis UVH3 gene is a homolog of the Saccharomyces cerevisiae RAD2 and human XPG DNA repair genes. Plant J 26: 329-338
57. Liu Z, Hossain GS, Islas-Osuna MA, Mitchell DL, Mount DW (2000) Repair of UV damage in plants by nucleotide excision repair: Arabidopsis UVH1 DNA repair gene is a homolog of Saccharomyces cerevisiae Rad1. Plant J 21: 519-528
58. Lois R (1994) Accumulation of UV-absorbing flavonoids induced by UV-B radiation in Arabidopsis thaliana L. I. Mechanisms of UV-resistance in Arabidopsis. Planta 194: 498-503
59. Maeda K, Kimura S, Demura T, Takeda J, Ozeki Y (2005) DcMYB1 as a transcriptional activator of the carrot phenylalanine ammonia-lyase gene (DcPAL1) in response to elicitor treatment, UV-B irradiation and the dilution effect. Plant Mol Biol 59: 739-752
60. Matsunaga T, Hieda K, Nikaido O (1991) Wavelength dependent formation of thymine dimers and [6-4] photoproducts in DNA by monochromatic ultraviolet light ranging from 150 to 365 nm. Photochem Photobiol 54: 403-410
61. Mercier J, Baka M, Reddy B, Corcuff R, Arul J (2001) Short-wave ultraviolet irradiation for control of decay caused by Botrytis cinerea in bell pepper: Induced resistance and germicidal effects. J Am Soc Hortic Sci 126: 128-133
62. Mercier J, Roussel D, Charles MT, Arul J (2000) Systemic and local responses associated with UV- and pathogen-induced resistance to Botrytis cinerea in stored carrot. Phytopathology 90: 981-986
63. Mitchell DL, Jin J, Cleaver JE (1991) Relative induction of cyclobutane dimers and cytosine photohydrates in DNA irradiated in vitro and in vivo with ultraviolet-C and ultraviolet-B light. Photochem Photobiol 54: 741-746
64. Mitchell DL, Nairn RS (1989) The biology of the (6-4) photoproduct. Photochem Photobiol 49: 805-819
65. Mohr PG, Cahill DM (2003) Abscisic acid influences the susceptibility of Arabidopsis thaliana to Pseudomonas syringae pv. tomato and Peronospora parasitica. Funct Plant Biol 30: 461-469
66. Molinier J, Oakeley EJ, Niederhauser O, Kovalchuk I, Hohn B (2005) Dynamic response of plant genome to ultraviolet radiation and other genotoxic stresses. Mutat Res 571: 235-247
67. Mori T, Nakane M, Hattori T, Matsunaga T, Ihara M, Nikaido O (1991) Simultaneous establishment of monoclonal antibodies specific for either cyclobutane pyrimidine dimer or (6-4) photoproduct from the same mouse immunized with ultraviolet-irradiated DNA. Photochem Photobiol 54: 225-232
68. Nakajima S, Sugiyama M, Iwai S, Hitomi K, Otoshi E, Kim ST, Jiang CZ, Todo T, Britt AB, Yamamoto K (1998) Cloning and characterization of a gene (UVR3) required for photorepair of 6-4 photoproducts in Arabidopsis thaliana. Nucleic Acids Res 26: 638-644
69. Nawrath C, Heck S, Parinthawong N, Métraux JP (2002) EDS5, an essential component of salicylic acid-dependent signalling for disease resistance in Arabidopsis, is a member of the MATE transporter family. Plant Cell 14: 275-286
70. Pang Q, Hays JB (1991) UV-B inducible and temperature-sensitive photoreactivation of cyclobutane pyrimidine dimers in Arabidopsis thaliana. Plant Physiol 95: 536-543
71. Paul ND (2000) Stratospheric ozone depletion, UV-B radiation and crop disease. Environ Pollut 108: 343-355
72. Peak MJ, Peak JG, Carnes BA (1987) Induction of direct and indirect single-strand breaks in human cell DNA by far- and near-ultraviolet radiations: action spectrum and mechanisms. Photochem Photobiol 45: 381-387
73. Perdiz D, Grof P, Mezzina M, Nikaido O, Moustacchi E, Sage E (2000) Distribution and repair of bipyrimidine photoproducts in solar UV-irradiated mammalian cells. J Biol Chem 275: 26732-26742
74. Quaite FE, Sutherland BM, Sutherland JC (1992a) Action spectrum for DNA damage in alfalfa lowers predicted impact of ozone depletion. Nature 358: 576-578
75. Quaite FE, Sutherland BM, Sutherland JC (1992b) Quantitation of pyrimidine dimers in DNA from UVB-irradiated alfalfa (Medicago sativa L.) seedlings. Appl Theor Electrophor 2: 171-175
76. Quaite FE, Takayanagi S, Ruffini J, Sutherland JC, Sutherland BM (1994) DNA damage levels determine cyclobutyl pyrimidine dimer repair mechanisms in alfalfa seedlings. Plant Cell 6: 1635-1641
77. Reardon JT, Bessho T, Kung HC, Bolton PH, Sancar A (1997) In vitro repair of oxidative DNA damage by human nucleotide excision repair system: possible explanation for neurodegeneration in xeroderma pigmentosum patients. Proc Natl Acad Sci USA 94: 9463-9468
78. Rice-Evans CA, Miller NJ, Papaga G (1997) Antioxidant properties of phenolic compounds. Trends Plant Sci 2: 152-159
79. Rosenstein BS, Mitchell DL (1987) Action spectra for the induction of pyrimidine (6-4) pyrimidone photoproducts and cyclobutane pyrimidine dimers in normal human skin fibroblasts. Photochem Photobiol 45: 775-781
80. Sancar A, Thompson C, Thresher RJ, Araujo F, Mo J, Ozgur S, Vagas E, Dawut L, Selby CP (2000) Photolyase/cryptochrome family blue-light photoreceptors use light energy to repair DNA or set the circadian clock. Cold Spring Harb Symp Quant Biol 65: 157-171
81. Sancar GB (1990) DNA photolyases: physical properties, action mechanism, and roles in dark repair. Mutat Res 236: 147-160
82. Satoh MS, Jones CJ, Woof RD, Lindahl T (1993) DNA excision-repair defect of xeroderma pigmentosum prevents removal of a class of oxygen free radical-induced base lesions. Proc Natl Acad Sci USA 90: 6335-6339
83. Sävenstrand H, Brosché M, Strid Aring; (2004) Ultraviolet-B signalling: Arabidopsis brassinosteroid mutants are defective in UV-B regulated defence gene expression. Plant Physiol Biochem 42: 687-694
84. Scott AD, Nelshabury M, Jones DH, Reed SH, Boiteux S, Waters R (1999) Spontaneous mutation, oxidative DNA damage, and the roles of base and nucleotide excision repair in the yeast Saccharomyces. Yeast 15: 205-218
85. Shirley BW, Kubasek WL, Storz G, Bruggeman E, Koorneef M, Ausubel FM, Goodman HM (1995) Analysis of Arabidopsis mutants deficient in flavonoid biosynthesis. Plant J 8: 659-671
86. Sohn KH, Lei R, Nemri A, Jones JDG (2007) The downy mildew effectors proteins ATR1 and ATR13 promote disease susceptibility in Arabidopsis thaliana. Plant Cell 19: 4077-4090
87. Stapleton AE, Walbot V (1994) Flavonoids can protectmaize DNA fromthe induction of ultraviolet radiation damage. Plant Physiol 105: 881-889
88. Stevens C, Khan VA, Lu JY, Wilson CL, Pusey PL, Kabwe MK, Igwegbe ECK, Chalutz E, Droby S (1998) The germicidal and hormetic effects of UV-C light on reducing brown rot disease and yeast microflora of peaches. Crop Prot 17: 75-84
89. Stevens C, Khan VA, Wilson Lu JY, Chalutz E, Droby S (2005) The effect of fruit orientation of postharvest commodities following low dose ultraviolet light-C treatment on host induced resistance to decay. Crop Prot 24: 756-759
90. Stevens C, Liu J, Khan VA, Lu JY, Kabwe MK, Wilson CL, Igwegbe ECK, Chalutz E, Droby S (2004) The effects of low-dose ultraviolet light-C treatment on polygalacturonase activity, delay ripening and Rhizopus soft rot development of tomatoes. Crop Prot 23: 551-554
91. Stratmann J (2003) Ultraviolet-B radiation co-opts defense signalling pathways. Trends Plant Sci 8: 526-533
92. Suesslin C, Frohnmeyer H (2003) An Arabidopsis mutant defective in UV-B light-mediated responses. Plant J 33: 591-601
93. Swindell WR (2006) The association among gene expression responses to nine abiotic stress treatments in Arabidopsis thaliana. Genetics 174: 1811-1824
94. Tanaka A, Sakamoto A, Ishigaki Y, Nikaido O, Sun G, Hase Y, Shikazono N, Tano S, Watanabe H (2002) An ultraviolet-B-resistant mutant with enhanced DNA repair in Arabidopsis. Plant Physiol 129: 64-71
95. Torres MA, Jones JDG, Dangl JL (2006) Reactive oxygen species signaling in response to pathogens. Plant Physiol 141: 373-378
96. Ulm R, Baumann A, Oravecz A, Máté Z, Ádám É, Oakeley EJ, Schäfer E, Nagy F (2004) Genome-wide analysis of gene expression reveals function of the bZIP transcription factor HY5 in the UV-B response of Arabidopsis. Proc Natl Acad Sci USA 101: 1397-1402
97. Ulm R, Ichimura K, Mizoguchi T, Peck SC, Zhu T, Wang X, Shinozaki K, Paszkowski J (2001) Distinct regulation of salinity and genotoxic stress responses by Arabidopsis MAP kinase phosphatase 1. EMBO J 21: 6483-6493
98. Ulm R, Nagy F (2005) Signalling and gene regulation in response to ultraviolet light. Curr Opin Plant Biol 8: 477-482
99. Van Loon LC, Van Strien EA (1999) The families of pathogenesis-related proteins, their activities and comparative analysis of PR-1 type proteins. Physiol Mol Plant Pathol 55: 85-97
100. Ward ER, Uknes SJ, Williams SC, Dincher SS, Wiederhold DL, Alexander DC, Ahl-Goy P, Métraux JP, Ryals JA (1991) Coordinate gene activity in response to agents that induce systemic acquired resistance. Plant Cell 3: 1085-1094
101. Warren RF, Henk A, Mowery P, Holub E, Innes RW (1998) A mutation within the leucine-rich repeat domain of the Arabidopsis disease resistance gene RPS5 partially suppress multiple bacterial and downy mildew resistance genes. Plant Cell 10: 1439-1452
102. Waterworth WM, Jiang Q, West CE, Nikaido M, Bray CM (2002) Characterization of Arabidopsis photolyase enzymes and analysis of their role in protection from ultraviolet-B radiation. J Exp Bot 53: 1005-1015
103. Wei H, Ca Q, Rahn R, Zhang X, Wang Y, Lebwohl M (1998) DNA structural integrity and base composition affect ultraviolet light-induced oxidative DNA damage. Biochemistry 37: 6485-6490
104. Xiong L, Schumaker KS, Zhu JK (2002) Cell signalling during cold, drought and salt stress. Plant Cell 14: S165-S183
105. Yalpani N, Enyedi AJ, León J, Raskin I (1994) Ultraviolet light and ozone stimulate accumulation of salicylic acid, pathogenesis-related proteins and virus resistance in tobacco. Planta 193: 372-376