DNA double-strand breaks induce the expression of flavin-containing monooxygenase and reduce root meristem size in Arabidopsis thaliana

Genes to Cells

Volumn 20, Issue 8, 2015, Pages 636-646

  Chen, Poyu ^a   Umeda, Masaaki ^a,b  

^a NARA INSTITUTE OF SCIENCE AND TECHNOLOGY   (Japan)

^b JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

DIMETHYLANILINE MONOOXYGENASE; HYDROGEN PEROXIDE; PHLEOMYCIN; REACTIVE OXYGEN METABOLITE; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR SOG1; UNCLASSIFIED DRUG; 4,6-DINITRO-O-CRESOL; ARABIDOPSIS PROTEIN; BLEOMYCIN; DIMETHYLANILINE MONOOXYGENASE (N-OXIDE FORMING); DINITRO ORTHO CRESOL; OXYGENASE; PLANT DNA; SOG1 PROTEIN, ARABIDOPSIS;

ARABIDOPSIS THALIANA; ARTICLE; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; DOUBLE STRANDED DNA BREAK; FMO1 GENE; GENE INACTIVATION; GENE OVEREXPRESSION; HOMEOSTASIS; MERISTEM; MUTANT; NONHUMAN; PLANT GENE; PLANT ROOT; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN BINDING; PROTEIN EXPRESSION; ROOT GROWTH; ROOT MERISTEM SIZE; TRANSGENIC PLANT; ARABIDOPSIS; CHEMISTRY; DRUG EFFECTS; GENETICS; METABOLISM; PHYSIOLOGY;

ARABIDOPSIS; ARABIDOPSIS THALIANA;

ARABIDOPSIS; ARABIDOPSIS PROTEINS; BLEOMYCIN; DINITROCRESOLS; DNA BREAKS, DOUBLE-STRANDED; DNA, PLANT; GENE KNOCKOUT TECHNIQUES; HYDROGEN PEROXIDE; MERISTEM; OXYGENASES; PLANT ROOTS; REACTIVE OXYGEN SPECIES; TRANSCRIPTION FACTORS;

EID: 84938414159     PISSN: 13569597     EISSN: 13652443     Source Type: Journal    
DOI: 10.1111/gtc.12255     Document Type: Article

References (51)

1. Adachi, S., Minamisawa, K., Okushima, Y., Inagaki, S., Yoshiyama, K., Kondou, Y., Kaminuma, E., Kawashima, M., Toyoda, T., Matsui, M., Kurihara, D., Matsunaga, S. & Umeda, M. (2011) Programmed induction of endoreduplication by DNA double-strand breaks in Arabidopsis. Proc. Natl Acad. Sci. USA 108, 10004-10009.
2. Berdy, J. (1980) Bleomycin-type antibiotics. In: Amino Acid and Peptide Antibiotics - Handbook of Antibiotic Compounds, IV (1) (ed. Berdy, J.), pp. 459-497. Boca Raton, FL: CRC Press.
3. Choi, J.J., Klosterman, S.J. & Hadwiger, L.A. (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.
4. Culligan, K.M., Robertson, C.E., Foreman, J., Doerner, P. & Britt, A.B. (2006) ATR and ATM play both distinct and additive roles in response to ionizing radiation. Plant J. 48, 947-961.
5. Culligan, K.M., Tissier, A. & Britt, A.B. (2004) ATR regulates a G2-phase cell-cycle checkpoint in Arabidopsis thaliana. Plant Cell 16, 1091-1104.
6. De Veylder, L., Larkin, J.C. & Schnittger, A. (2011) Molecular control and function of endoreplication in development and physiology. Trends Plant Sci. 16, 624-634.
7. Dunand, C., Crèvecoeur, M. & Penel, C. (2007) Distribution of superoxide and hydrogen peroxide in Arabidopsis root and their influence on root development: possible interaction with peroxidases. New Phytol. 174, 332-341.
8. Foreman, J., Demidchik, V., Bothwell, J.H.F., Mylona, P., Miedema, H., Torres, M.A., Linstead, P., Costa, S., Brownlee, C., Jones, J.D.G., Davies, J.M. & Dolan, L. (2003) Reactive oxygen species produced by NADPH oxidase regulate plant cell growth. Nature 422, 442-446.
9. Garcia, V., Bruchet, H., Camescasse, D., Granier, F., Bouchez, D. & Tissier, A. (2003) AtATM is essential for meiosis and the somatic response to DNA damage in plants. Plant Cell 15, 119-132.
10. Harper, J.W. & Elledge, S.J. (2007) The DNA damage response: ten years after. Mol. Cell 28, 739-745.
11. Hines, R.N., Cashman, J.R., Philpot, R.M., Williams, D.E. & Ziegler, D.M. (1994) The mammalian flavin-containing monooxygenases: molecular characterization and regulation of expression. Toxicol. Appl. Pharmacol. 125, 1-6.
12. Koch, M., Vorwerk, S., Masur, C., Sharifi-Sirchi, G., Olivieri, N. & Schlaich, N.L. (2006) A role for a flavin-containing mono-oxygenase in resistance against microbial pathogens in Arabidopsis. Plant J. 47, 629-639.
13. Kovtun, Y., Chiu, W.L., Tena, G. & Sheen, J. (2000) Functional analysis of oxidative stress-activated mitogen-activated protein kinase cascade in plants. Proc. Natl Acad. Sci. USA 97, 2940-2945.
14. Lucht, J.M., Mauch-Mani, B., Steiner, H.Y., Metraux, J.P., Ryals, J. & Hohn, B. (2002) Pathogen stress increases somatic recombination frequency in Arabidopsis. Nat. Genet. 30, 311-314.
15. Maeda, H., Fukuyasu, Y., Yoshida, S., Fukuda, M., Saeki, K., Matsuno, H., Yamauchi, Y., Yoshida, K., Hirata, K. & Miyamoto, K. (2004) Fluorescent probes for hydrogen peroxide based on a non-oxidative mechanism. Angew. Chem. Int. Ed. Engl. 43, 2389-2391.
16. Menon, S.G., Sarsour, E.H., Spitz, D.R., Higashikubo, R., Sturm, M., Zhang, H. & Goswami, P.C. (2003) Redox regulation of the G1 to S phase transition in the mouse embryo fibroblast cell cycle. Cancer Res. 63, 2109-2117.
17. Mishina, T.E. & Zeier, J. (2006) The Arabidopsis flavin-dependent monooxygenase FMO1 is an essential component of biologically induced systemic acquired resistance. Plant Physiol. 141, 1666-1675.
18. Monshausen, G.B., Bibikova, T.N., Messerli, M.A., Shi, C. & Gilroy, S. (2007) Oscillations in extracellular pH and reactive oxygen species modulate tip growth of Arabidopsis root hairs. Proc. Natl Acad. Sci. USA 104, 20996-21001.
19. Muller, E.G. (1991) Thioredoxin deficiency in yeast prolongs S phase and shortens the G1 interval of the cell cycle. J. Biol. Chem. 266, 9194-9202.
20. 2 is insufficient to elicit cell death in tobacco. Plant Cell Environ. 28, 548-561.
21. Nakagawa, T., Ishiguro, S. & Kimura, T. (2009) Gateway vectors for plant transformation. Plant Biotechnol. 26, 275-284.
22. Nezames, C.D., Sjogren, C.A., Barajas, J.F. & Larsen, P.B. (2012) The Arabidopsis cell cycle checkpoint regulators TANMEI/ALT2 and ATR mediate the active process of aluminum-dependent root growth inhibition. Plant Cell 24, 608-621.
23. Owusu-Ansah, E. & Banerjee, U. (2009) Reactive oxygen species prime Drosophila haematopoietic progenitors for differentiation. Nature 461, 537-541.
24. Perilli, S., Moubayidin, L. & Sabatini, S. (2010) The molecular basis of cytokinin function. Curr. Opin. Plant Biol. 13, 21-26.
25. Potocky, M., Jones, M.A., Bezvoda, R., Smirnoff, N. & Zarsky, V. (2007) Reactive oxygen species produced by NADPH oxidase are involved in pollen tube growth. New Phytol. 174, 742-751.
26. Ranjan, P., Anathy, V., Burch, P.M., Weirather, K., Lambeth, J.D. & Heintz, N.H. (2006) Redox-dependent expression of cyclin D1 and cell proliferation by Nox1 in mouse lung epithelial cells. Antioxid. Redox Signal. 8, 1447-1459.
27. + flux. Nature 416, 291-297.
28. Riballo, E., Kühne, M., Rief, N., Doherty, A., Smith, G.C., Recio, M.J. & Löbrich, M. (2004) A pathway of double-strand break rejoining dependent upon ATM, Artemis, and proteins locating to γ-H2AX foci. Mol. Cell 16, 715-724.
29. Riley, T., Sontag, E., Chen, P. & Levine, A. (2008) Transcriptional control of human p53-regulated genes. Nat. Rev. Mol. Cell Biol. 5, 402-412.
30. Roldán-Arjona, T. & Ariza, R.R. (2009) Repair and tolerance of oxidative DNA damage in plants. Mutat. Res. 681, 169-179.
31. Sakamoto, T., Inui, Y.T., Uraguchi, S., Yoshizumi, T., Matsunaga, S., Mastui, M., Umeda, M., Fukui, K. & Fujiwara, T. (2011) Condensin II alleviates DNA damage and is essential for tolerance of boron overload stress in Arabidopsis. Plant Cell 23, 3533-3546.
32. Saleh, A., Alvarez-Venegas, R. & Avramova, Z. (2008) An efficient chromatin immunoprecipitation (ChIP) protocol for studying histone modifications in Arabidopsis plants. Nat. Protoc. 3, 1018-1025.
33. Schneider, C.A., Rasband, W.S. & Eliceiri, K.W. (2012) NIH image to ImageJ: 25 years of image analysis. Nat. Methods 9, 671-675.
34. Shiotani, B. & Zou, L. (2009) Single-stranded DNA orchestrates an ATM-to-ATR switch at DNA breaks. Mol. Cell 33, 547-558.
35. Siddens, L.K., Krueger, S.K., Henderson, M.C. & Williams, D.E. (2014) Mammalian flavin-containing monooxygenase (FMO) as a source of hydrogen peroxide. Biochem. Pharmacol. 89, 141-147.
36. Takahashi, N., Kajihara, T., Okamura, C., Kim, Y., Katagiri, Y., Okushima, Y. & Umeda, M. (2013) Cytokinins control endocycle onset by promoting the expression of an APC/C activator in Arabidopsis roots. Curr. Biol. 23, 1812-1817.
37. Takatsuka, H. & Umeda, M. (2014) Hormonal control of cell division and elongation along differentiation trajectories in roots. J. Exp. Bot. 65, 2633-2643.
38. Takeda, S., Gapper, C., Kaya, H., Bell, E., Kuchitsu, K. & Dolan, L. (2008) Local positive feedback regulation determines cell shape in root hair cells. Science 319, 1241-1244.
39. Tanaka, T., Halicka, H.D., Huang, X., Traganos, F. & Darzynkiewicz, Z. (2006) Constitutive histone H2AX phosphorylation and ATM activation, the reporters of DNA damage by endogenous oxidants. Cell Cycle 5, 1940-1945.
40. phox homologues AtrbohD and AtrbohF are required for accumulation of reactive oxygen intermediates in the plant defense response. Proc. Natl Acad. Sci. USA 99, 517-522.
41. Truernit, E. & Haseloff, J. (2008) A simple way to identify non-viable cells within living plant tissue using confocal microscopy. Plant Methods 4, 15.
42. Tsukagoshi, H. (2012) Defective root growth triggered by oxidative stress is controlled through the expression of cell cycle-related genes. Plant Sci. 197, 30-39.
43. Tsukagoshi, H., Busch, W. & Benfey, P.N. (2010) Transcriptional regulation of ROS controls transition from proliferation to differentiation in the root. Cell 143, 606-616.
44. Tynes, R.E., Sabourin, P.J., Hodgson, E. & Philpot, R.M. (1986) Formation of hydrogen peroxide and N-hydroxylated amines catalyzed by pulmonary flavin-containing monooxygenases in the presence of primary alkylamines. Arch. Biochem. Biophys. 251, 654-664.
45. Wang, S., Durrant, W.E., Song, J., Spivey, N.W. & Dong, X. (2010) Arabidopsis BRCA2 and RAD51 proteins are specifically involved in defense gene transcription during plant immune responses. Proc. Natl Acad. Sci. USA 107, 22716-22721.
46. Yan, S., Wang, W., Marqués, J., Mohan, R., Saleh, A., Durrant, W.E. & Dong, X. (2013) Salicylic acid activates DNA damage responses to potentiate plant immunity. Mol. Cell 52, 602-610.
47. Yi, D., Kamei, C.L.A., Cools, T., Vanderauwera, S., Takahashi, N., Okushima, Y., Eekhout, T., Yoshiyama, K.O., Larkin, J., Van den Daele, H., Conklin, P., Britt, A., Umeda, M. & De Veylder, L. (2014) The Arabidopsis SIAMESE-RELATED cyclin-dependent kinase inhibitors SMR5 and SMR7 regulate the DNA damage checkpoint in response to reactive oxygen species. Plant Cell 26, 296-309.
48. Yoshiyama, K., Conklin, P.A., Huefner, N.D. & Britt, A.B. (2009) Suppressor of gamma response 1 (SOG1) encodes a putative transcription factor governing multiple responses to DNA damage. Proc. Natl Acad. Sci. USA 106, 12843-12848.
49. Yoshiyama, K.O., Kobayashi, J., Ogita, N., Ueda, M., Kimura, S., Maki, H. & Umeda, M. (2013) ATM-mediated phosphorylation of SOG1 is essential for the DNA damage response in Arabidopsis. EMBO Rep. 14, 817-822.
50. Zeier, J., Pink, B., Mueller, M.J. & Berger, S. (2004) Light conditions influence specific defence responses in incompatible plant-pathogen interactions: uncoupling systemic resistance from salicylic acid and PR-1 accumulation. Planta 219, 673-683.
51. Zhou, B.B. & Elledge, S.J. (2000) The DNA damage response: putting checkpoints in perspective. Nature 408, 433-439.