Microbial Pathogens Trigger Host DNA Double-Strand Breaks Whose Abundance Is Reduced by Plant Defense Responses

PLoS Pathogens

Volumn 10, Issue 4, 2014, Pages

  Song, Junqi ^a   Bent, Andrew F ^a  

^a UNIVERSITY OF WISCONSIN MADISON   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ATM PROTEIN; ATR PROTEIN; HISTONE H2AX; MAMP RECEPTOR; NPR1 PROTEIN; PARAQUAT; PEPTIDES AND PROTEINS; REACTIVE OXYGEN METABOLITE; SALICYLIC ACID; UNCLASSIFIED DRUG; ARABIDOPSIS PROTEIN; PLANT DNA;

ARABIDOPSIS; ARTICLE; BACTERIAL GROWTH; CELL DEATH; COMET ASSAY; CONTROLLED STUDY; DOUBLE STRANDED DNA BREAK; GENE EXPRESSION; IMMUNOBLOTTING; MICROORGANISM; MUTANT; NECROSIS; NONHUMAN; PHOSPHORYLATION; PHYTOPHTHORA INFESTANS; PLANT DEFENSE; PSEUDOMONAS SYRINGAE; GENETICS; HOST PATHOGEN INTERACTION; METABOLISM; MICROBIOLOGY; MUTATION; PHYSIOLOGY; PLANT DISEASE;

ARABIDOPSIS; ARABIDOPSIS PROTEINS; DNA BREAKS, DOUBLE-STRANDED; DNA, PLANT; HOST-PATHOGEN INTERACTIONS; MUTATION; PLANT DISEASES; PSEUDOMONAS SYRINGAE; REACTIVE OXYGEN SPECIES;

EID: 84901317655     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1004030     Document Type: Article

References (91)

1. Jackson SP, Bartek J, (2009) The DNA-damage response in human biology and disease. Nature 461: 1071-1078.
2. Ciccia A, Elledge SJ, (2010) The DNA damage response: making it safe to play with knives. Mol Cell 40: 179-204.
3. Sedelnikova OA, Redon CE, Dickey JS, Nakamura AJ, Georgakilas AG, et al. (2010) Role of oxidatively induced DNA lesions in human pathogenesis. Mutat Res 704: 152-159.
4. Ambur OH, Davidsen T, Frye SA, Balasingham SV, Lagesen K, et al. (2009) Genome dynamics in major bacterial pathogens. FEMS Microbiol Rev 33: 453-470.
5. Weitzman MD, Lilley CE, Chaurushiya MS, (2010) Genomes in conflict: maintaining genome integrity during virus infection. Annu Rev Microbiol 64: 61-81.
6. Nougayrede JP, Homburg S, Taieb F, Boury M, Brzuszkiewicz E, et al. (2006) Escherichia coli induces DNA double-strand breaks in eukaryotic cells. Science 313: 848-851.
7. Toller IM, Neelsen KJ, Steger M, Hartung ML, Hottiger MO, et al. (2011) Carcinogenic bacterial pathogen Helicobacter pylori triggers DNA double-strand breaks and a DNA damage response in its host cells. Proc Natl Acad Sci U S A 108: 14944-14949.
8. Chakraborty SP, Kar Mahapatra S, Sahu SK, Das S, Tripathy S, et al. (2011) Internalization of Staphylococcus aureus in lymphocytes induces oxidative stress and DNA fragmentation: possible ameliorative role of nanoconjugated vancomycin. Oxid Med Cell Longev 2011: 942123.
9. Rakkestad KE, Skaar I, Ansteinsson VE, Solhaug A, Holme JA, et al. (2010) DNA damage and DNA damage responses in THP-1 monocytes after exposure to spores of either Stachybotrys chartarum or Aspergillus versicolor or to T-2 toxin. Toxicol Sci 115: 140-155.
10. Touati E, (2010) When bacteria become mutagenic and carcinogenic: lessons from H. pylori. Mutat Res 703: 66-70.
11. Mangerich A, Knutson CG, Parry NM, Muthupalani S, Ye W, et al. (2012) Infection-induced colitis in mice causes dynamic and tissue-specific changes in stress response and DNA damage leading to colon cancer. Proc Natl Acad Sci U S A 109: E1820-1829.
12. Arthur JC, Perez-Chanona E, Muhlbauer M, Tomkovich S, Uronis JM, et al. (2012) Intestinal inflammation targets cancer-inducing activity of the microbiota. Science 338: 120-123.
13. Dodds PN, Rathjen JP, (2010) Plant immunity: towards an integrated view of plant-pathogen interactions. Nat Rev Genet 11: 539-548.
14. Murphy K, Travers P, Walport M, Janeway C (2012) Janeway's immunobiology. New York: Garland Science. xix, 868 p. p.
15. Rakoff-Nahoum S, Medzhitov R, (2009) Toll-like receptors and cancer. Nat Rev Cancer 9: 57-63.
16. Lamb C, Dixon RA, (1997) The Oxidative Burst in Plant Disease Resistance. Annu Rev Plant Physiol Plant Mol Biol 48: 251-275.
17. O'Brien JA, Daudi A, Butt VS, Bolwell GP, (2012) Reactive oxygen species and their role in plant defence and cell wall metabolism. Planta 236: 765-779.
18. Roldan-Arjona T, Ariza RR, (2009) Repair and tolerance of oxidative DNA damage in plants. Mutat Res 681: 169-179.
19. Waterworth WM, Drury GE, Bray CM, West CE, (2011) Repairing breaks in the plant genome: the importance of keeping it together. New Phytol 192: 805-822.
20. Balestrazzi A, Confalonieri M, Macovei A, Dona M, Carbonera D, (2011) Genotoxic stress and DNA repair in plants: emerging functions and tools for improving crop productivity. Plant Cell Rep 30: 287-295.
21. Rogakou EP, Pilch DR, Orr AH, Ivanova VS, Bonner WM, (1998) DNA double-stranded breaks induce histone H2AX phosphorylation on serine 139. J Biol Chem 273: 5858-5868.
22. Iacovoni JS, Caron P, Lassadi I, Nicolas E, Massip L, et al. (2010) High-resolution profiling of gammaH2AX around DNA double strand breaks in the mammalian genome. EMBO J 29: 1446-1457.
23. Abraham RT, (2001) Cell cycle checkpoint signaling through the ATM and ATR kinases. Genes Dev 15: 2177-2196.
24. Sperka T, Wang J, Rudolph KL, (2012) DNA damage checkpoints in stem cells, ageing and cancer. Nat Rev Mol Cell Biol 13: 579-590.
25. Friesner JD, Liu B, Culligan K, Britt AB, (2005) Ionizing radiation-dependent gamma-H2AX focus formation requires ataxia telangiectasia mutated and ataxia telangiectasia mutated and Rad3-related. Mol Biol Cell 16: 2566-2576.
26. Kinner A, Wu W, Staudt C, Iliakis G, (2008) Gamma-H2AX in recognition and signaling of DNA double-strand breaks in the context of chromatin. Nucleic Acids Res 36: 5678-5694.
27. Lucht JM, Mauch-Mani B, Steiner HY, Metraux JP, Ryals J, et al. (2002) Pathogen stress increases somatic recombination frequency in Arabidopsis. Nat Genet 30: 311-314.
28. Kovalchuk I, Kovalchuk O, Kalck V, Boyko V, Filkowski J, et al. (2003) Pathogen-induced systemic plant signal triggers DNA rearrangements. Nature 423: 760-762.
29. Yao Y, Kathiria P, Kovalchuk I, (2013) A systemic increase in the recombination frequency upon local infection of Arabidopsis thaliana plants with oilseed rape mosaic virus depends on plant age, the initial inoculum concentration and the time for virus replication. Front Plant Sci 4: 61.
30. Choi JJ, Klosterman SJ, Hadwiger LA, (2001) A comparison of the effects of DNA-damaging agents and biotic elicitors on the induction of plant defense genes, nuclear distortion, and cell death. Plant Physiol 125: 752-762.
31. Kunz BA, Cahill DM, Mohr PG, Osmond MJ, Vonarx EJ, (2006) Plant responses to UV radiation and links to pathogen resistance. Int Rev Cytol 255: 1-40.
32. Durrant WE, Wang S, Dong XN, (2007) Arabidopsis SNI1 and RAD51D regulate both gene transcription and DNA recombination during the defense response. Proc Natl Acad Sci U S A 104: 4223-4227.
33. Wang S, Durrant WE, Song J, Spivey NW, Dong X, (2010) Arabidopsis BRCA2 and RAD51 proteins are specifically involved in defense gene transcription during plant immune responses. Proc Natl Acad Sci U S A 107: 22716-22721.
34. Song J, Durrant WE, Wang S, Yan S, Tan EH, et al. (2011) DNA repair proteins are directly involved in regulation of gene expression during plant immune response. Cell Host Microbe 9: 115-124.
35. Adams-Phillips L, Wan J, Tan X, Dunning FM, Meyers BC, et al. (2008) Discovery of ADP-ribosylation and other plant defense pathway elements through expression profiling of four different Arabidopsis-Pseudomonas R-avr interactions. Mol Plant Microbe Interact 21: 646-657.
36. Adams-Phillips L, Briggs AG, Bent AF, (2010) Disruption of poly(ADP-ribosyl)ation mechanisms alters responses of Arabidopsis to biotic stress. Plant Physiol 152: 267-280.
37. Mur LA, Kenton P, Lloyd AJ, Ougham H, Prats E, (2008) The hypersensitive response; the centenary is upon us but how much do we know? J Exp Bot 59: 501-520.
38. Ryerson DE, Heath MC, (1996) Cleavage of nuclear DNA into oligonucleosomal fragments during cell death induced by fungal infection or by abiotic treatments. Plant Cell 8: 393-402.
39. Kunkel BN, Bent AF, Dahlbeck D, Innes RW, Staskawicz BJ, (1993) RPS2, an Arabidopsis disease resistance locus specifying recognition of Pseudomonas syringae strains expressing the avirulence gene avrRpt2. Plant Cell 5: 865-875.
40. Yu GL, Katagiri F, Ausubel FM, (1993) Arabidopsis mutations at the RPS2 locus result in loss of resistance to Pseudomonas syringae strains expressing the avirulence gene avrRpt2. Mol Plant Microbe Interact 6: 434-443.
41. Boch J, Joardar V, Gao L, Robertson TL, Lim M, et al. (2002) Identification of Pseudomonas syringae pv. tomato genes induced during infection of Arabidopsis thaliana. Mol Microbiol 44: 73-88.
42. Whalen MC, Innes RW, Bent AF, Staskawicz BJ, (1991) Identification of Pseudomonas syringae pathogens of Arabidopsis and a bacterial locus determining avirulence on both Arabidopsis and soybean. Plant Cell 3: 49-59.
43. Ritter C, Dangl JL, (1996) Interference between two specific pathogen recognition events mediated by distinct plant disease resistance genes. Plant Cell 8: 251-257.
44. Yu I-C, Parker J, Bent AF, (1998) Gene-for-gene disease resistance without the hypersensitive response in Arabidopsis dnd1 mutant. Proc Natl Acad Sci USA 95: 7819-7824.
45. Gao X, Chen X, Lin W, Chen S, Lu D, et al. (2013) Bifurcation of Arabidopsis NLR immune signaling via Ca(2)(+)-dependent protein kinases. PLoS Pathog 9: e1003127.
46. Zhang C, Gutsche AT, Shapiro AD, (2004) Feedback control of the Arabidopsis hypersensitive response. Mol Plant Microbe Interact 17: 357-365.
47. Grant M, Brown I, Adams S, Knight M, Ainslie A, et al. (2000) The RPM1 plant disease resistance gene facilitates a rapid and sustained increase in cytosolic calcium that is necessary for the oxidative burst and hypersensitive cell death. Plant J 23: 441-450.
48. Collins AR, Azqueta A, (2012) DNA repair as a biomarker in human biomonitoring studies; further applications of the comet assay. Mutat Res 736: 122-129.
49. Dhawan A, Bajpayee M, Parmar D, (2009) Comet assay: a reliable tool for the assessment of DNA damage in different models. Cell Biol Toxicol 25: 5-32.
50. Mishina TE, Zeier J, (2007) Pathogen-associated molecular pattern recognition rather than development of tissue necrosis contributes to bacterial induction of systemic acquired resistance in Arabidopsis. Plant J 50: 500-513.
51. Huynh TV, Dahlbeck D, Staskawicz BJ, (1989) Bacterial blight of soybean: Regulation of a pathogen gene determining host cultivar specificity. Science 245: 1374-1377.
52. Pieterse CM, van Wees SC, Hoffland E, van Pelt JA, van Loon LC, (1996) Systemic resistance in Arabidopsis induced by biocontrol bacteria is independent of salicylic acid accumulation and pathogenesis-related gene expression. Plant Cell 8: 1225-1237.
53. Haas D, Defago G, (2005) Biological control of soil-borne pathogens by fluorescent pseudomonads. Nat Rev Microbiol 3: 307-319.
54. Lukas J, Lukas C, Bartek J, (2011) More than just a focus: The chromatin response to DNA damage and its role in genome integrity maintenance. Nat Cell Biol 13: 1161-1169.
55. Srivastava N, Gochhait S, de Boer P, Bamezai RN, (2009) Role of H2AX in DNA damage response and human cancers. Mutat Res 681: 180-188.
56. Huen MS, Grant R, Manke I, Minn K, Yu X, et al. (2007) RNF8 transduces the DNA-damage signal via histone ubiquitylation and checkpoint protein assembly. Cell 131: 901-914.
57. Song J, Bradeen JM, Naess SK, Raasch JA, Wielgus SM, et al. (2003) Gene RB cloned from Solanum bulbocastanum confers broad spectrum resistance to potato late blight. Proc Natl Acad Sci U S A 100: 9128-9133.
58. Kramer LC, Choudoir MJ, Wielgus SM, Bhaskar PB, Jiang J, (2009) Correlation between transcript abundance of the RB gene and the level of the RB-mediated late blight resistance in potato. Mol Plant Microbe Interact 22: 447-455.
59. Gardner RG, Panthee DR, (2010) NC 1 CELBR and NC 2 CELBR: Early Blight and Late Blight-resistant Fresh Market Tomato Breeding Lines. Hortscience 45: 975-976.
60. Bowler C, van Montagu M, Inze D, (1992) Superoxide dismutase and stress tolerance. Ann Rev Plant Physiol Plant Mol Biol 43: 83-116.
61. Levine A, Tenhaken R, Dixon R, Lamb CJ, (1994) H2O2 from the oxidative burst orchestrates the plant hypersensitive disease resistance response. Cell 79: 583-593.
62. Suzuki N, Miller G, Morales J, Shulaev V, Torres MA, et al. (2011) Respiratory burst oxidases: the engines of ROS signaling. Curr Opin Plant Biol 14: 691-699.
63. Torres MA, Dangl JL, Jones JD, (2002) Arabidopsis gp91phox homologues AtrbohD and AtrbohF are required for accumulation of reactive oxygen intermediates in the plant defense response. Proc Natl Acad Sci U S A 99: 517-522.
64. Rao MV, Paliyath G, Ormrod DP, Murr DP, Watkins CB, (1997) Influence of salicylic acid on H2O2 production, oxidative stress, and H2O2-metabolizing enzymes. Salicylic acid-mediated oxidative damage requires H2O2. Plant Physiol 115: 137-149.
65. Durrant WE, Dong X, (2004) Systemic acquired resistance. Annu Rev Phytopathol 42: 185-209.
66. Pieterse CM, Van der Does D, Zamioudis C, Leon-Reyes A, Van Wees SC, (2012) Hormonal modulation of plant immunity. Annu Rev Cell Dev Biol 28: 489-521.
67. Cao H, Bowling SA, Gordon S, Dong X, (1994) Characterization of an Arabidopsis mutant that is nonresponsive to inducers of systemic acquired resistance. Plant Cell 6: 1583-1592.
68. Kirik V, Bouyer D, Schobinger U, Bechtold N, Herzog M, et al. (2001) CPR5 is involved in cell proliferation and cell death control and encodes a novel transmembrane protein. Curr Biol 11: 1891-1895.
69. Bowling SA, Clarke JD, Liu Y, Klessig DF, Dong X, (1997) The cpr5 mutant of Arabidopsis expresses both NPR1-dependent and NPR1-independent resistance. Plant Cell 9: 1573-1584.
70. Boller T, 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.
71. Kunze G, Zipfel C, Robatzek S, Niehaus K, Boller T, et al. (2004) The N terminus of bacterial elongation factor Tu elicits innate immunity in Arabidopsis plants. Plant Cell 16: 3496-3507.
72. Yan S, Wang W, Marques J, Mohan R, Saleh A, et al. (2013) Salicylic acid activates DNA damage responses to potentiate plant immunity. Mol Cell 52: 602-610.
73. Martin V, Chahwan C, Gao H, Blais V, Wohlschlegel J, et al. (2006) Sws1 is a conserved regulator of homologous recombination in eukaryotic cells. Embo J 25: 2564-2574.
74. Culligan K, Tissier A, Britt A, (2004) ATR regulates a G2-phase cell-cycle checkpoint in Arabidopsis thaliana. Plant Cell 16: 1091-1104.
75. Garcia V, Bruchet H, Camescasse D, Granier F, Bouchez D, et al. (2003) AtATM is essential for meiosis and the somatic response to DNA damage in plants. Plant Cell 15: 119-132.
76. Vespa L, Couvillion M, Spangler E, Shippen DE, (2005) ATM and ATR make distinct contributions to chromosome end protection and the maintenance of telomeric DNA in Arabidopsis. Genes Dev 19: 2111-2115.
77. Amiard S, Depeiges A, Allain E, White CI, Gallego ME, (2011) Arabidopsis ATM and ATR kinases prevent propagation of genome damage caused by telomere dysfunction. Plant Cell 23: 4254-4265.
78. Adachi S, Minamisawa K, Okushima Y, Inagaki S, Yoshiyama K, et al. (2011) Programmed induction of endoreduplication by DNA double-strand breaks in Arabidopsis. Proc Natl Acad Sci U S A 108: 10004-10009.
79. Menendez D, Shatz M, Azzam K, Garantziotis S, Fessler MB, et al. (2011) The Toll-like receptor gene family is integrated into human DNA damage and p53 networks. PLoS Genet 7: e1001360.
80. Gasser S, Orsulic S, Brown EJ, Raulet DH, (2005) The DNA damage pathway regulates innate immune system ligands of the NKG2D receptor. Nature 436: 1186-1190.
81. Jakobek JL, Lindgren PB, (1993) Generalized Induction of Defense Responses in Bean Is Not Correlated with the Induction of the Hypersensitive Reaction. Plant Cell 5: 49-56.
82. Pieterse CMJ, van Wees SCM, van Pelt JA, Knoester M, Laan R, et al. (1998) A novel signaling pathway controlling induced systemic resistance in Arabidopsis. Plant Cell 10: 1571-1580.
83. Verhagen BW, Glazebrook J, Zhu T, Chang HS, van Loon LC, et al. (2004) The transcriptome of rhizobacteria-induced systemic resistance in arabidopsis. Mol Plant Microbe Interact 17: 895-908.
84. Sumit R, Sahu BB, Xu M, Sandhu D, Bhattacharyya MK, (2012) Arabidopsis nonhost resistance gene PSS1 confers immunity against an oomycete and a fungal pathogen but not a bacterial pathogen that cause diseases in soybean. BMC Plant Biol 12: 87.
85. Park EJ, Chan DW, Park JH, Oettinger MA, Kwon J, (2003) DNA-PK is activated by nucleosomes and phosphorylates H2AX within the nucleosomes in an acetylation-dependent manner. Nucleic Acids Res 31: 6819-6827.
86. Kuhne M, Riballo E, Rief N, Rothkamm K, Jeggo PA, et al. (2004) A double-strand break repair defect in ATM-deficient cells contributes to radiosensitivity. Cancer Res 64: 500-508.
87. Karlsson KH, Stenerlow B, (2004) Focus formation of DNA repair proteins in normal and repair-deficient cells irradiated with high-LET ions. Radiat Res 161: 517-527.
88. Jiang M, Zhao L, Gamez M, Imperiale MJ, (2012) Roles of ATM and ATR-mediated DNA damage responses during lytic BK polyomavirus infection. PLoS Pathog 8: e1002898.
89. Katagiri F, Thilmony R, He SY, (2002) The Arabidopsis thaliana-pseudomonas syringae interaction. Arabidopsis Book 1: e0039.
90. Genger RK, Jurkowski GI, McDowell JM, Lu H, Jung HW, et al. (2008) Signaling pathways that regulate the enhanced disease resistance of Arabidopsis "defense, no death" mutants. Mol Plant Microbe Interact 21: 1285-1296.
91. Jackson JP, Johnson L, Jasencakova Z, Zhang X, PerezBurgos L, et al. (2004) Dimethylation of histone H3 lysine 9 is a critical mark for DNA methylation and gene silencing in Arabidopsis thaliana. Chromosoma 112: 308-315.