Arabidopsis ribonucleotide reductases are critical for cell cycle progression, DNA damage repair, and plant development

Plant Cell

Volumn 18, Issue 2, 2006, Pages 350-365

  Wang, Chunxin ^a   Liu, Zhongchi ^a  

^a Bldg 142   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BIOLOGICAL ORGANS; CATALYSIS; CELLS; DNA; GENES; PLANTS (BOTANY);

CELL CYCLE PROGRESSION; DEOXYRIBONUCLEOTIDES; GROWTH RETARDATION; RIBONUCLEOTIDE REDUCTASE;

ENZYMES;

CATALYSTS; CELLS; ENZYMES; GENES; NUCLEIC ACIDS; PLANTS;

ANIMALIA; ARABIDOPSIS; ARABIDOPSIS THALIANA; MAMMALIA;

EID: 33745441439     PISSN: 10404651     EISSN: None     Source Type: Journal    
DOI: 10.1105/tpc.105.037044     Document Type: Article

References (68)

1. Angelis, K.J., Dusinska, M., and Collins, A.R. (1999). Single cell gel electrophoresis: Detection of DNA damage at different levels of sensitivity. Electrophoresis 20, 2133-2138.
2. Bowman, J.L., Smyth, D.R., and Meyerowitz, E.M. (1989). Genes directing flower development in Arabidopsis. Plant Cell 1, 37-52.
3. Brodersen, P., Petersen, M., Pike, H.M., Olszak, B., Skov, S., Odum, N., Jorgensen, L.B., Brown, R.E., and Mundy, J. (2002). Knockout of Arabidopsis accelerated-cell-death11 encoding a sphingosine transfer protein causes activation of programmed cell death and defense. Genes Dev. 16, 490-502.
4. Bundock, P., and Hooykaas, P. (2002). Severe developmental defects, hypersensitivity to DNA-damaging agents, and lengthened telomeres in Arabidopsis MRE11 mutants. Plant Cell 14, 2451-2462.
5. Chabes, A., Domkin, V., and Thelander, L. (1999). Yeast Sml1, a protein inhibitor of ribonucleotide reductase. J. Biol. Chem. 274, 36679-36683.
6. Chabes, A., Georgieva, B., Domkin, V., Zhao, X., Rothstein, R., and Thelander, L. (2003a). Survival of DNA damage in yeast directly depends on increased dNTP levels allowed by relaxed feedback inhibition of ribonucleotide reductase. Cell 112, 391-401.
7. Chabes, A., and Thelander, L. (2003). DNA building blocks at the foundation of better survival. Cell Cycle 2, 171-173.
8. Chabes, A.L., Pfleger, C.M., Kirschner, M.W., and Thelander, L. (2003b). Mouse ribonucleotide reductase R2 protein: A new target for anaphase-promoting complex-Cdh1-mediated proteolysis. Proc. Natl. Acad. Sci. USA 100, 3925-3929.
9. Chaboute, M.E., Clement, B., and Philipps, G. (2002). S phase and meristem-specific expression of the tobacco RNR1b gene is mediated by an E2F element located in the 5′ leader sequence. J. Biol. Chem. 277, 17845-17851.
10. Chaboute, M.E., Clement, B., Sekine, M., Philipps, G., and Chaubet-Gigot, N. (2000). Cell cycle regulation of the tobacco ribonucleotide reductase small subunit gene is mediated by E2F-like elements. Plant Cell 12, 1987-2000.
11. Chaboute, M.E., Combettes, B., Clement, B., Gigot, C., and Philipps, G. (1998). Molecular characterization of tobacco ribonucleotide reductase RNR1 and RNR2 cDNAs and cell cycle-regulated expression in synchronized plant cells. Plant Mol. Biol. 38, 797-806.
12. Chen, I.P., Haehnel, U., Altschmied, L., Schubert, I., and Puchta, H. (2003). The transcriptional response of Arabidopsis to genotoxic stress-A high-density colony array study (HDCA). Plant J. 35, 771-786.
13. Chernova, O.B., Chernov, M.V., Agarwal, M.L., Taylor, W.R., and Stark, G.R. (1995). The role of p53 in regulating genomic stability when DNA and RNA synthesis are inhibited. Trends Biochem. Sci. 20, 431-434.
14. Collins, A., Dusinska, M., Franklin, M., Somorovska, M., Petrovska, H., Duthie, S., Fillion, L., Panayiotidis, M., Raslova, K., and Vaughan, N. (1997). Comet assay in human biomonitoring studies: Reliability, validation, and applications. Environ. Mol. Mutagen. 30, 139-146.
15. Culligan, K., Tissier, A., and Britt, A. (2004). ATR regulates a G2-phase cell-cycle checkpoint in Arabidopsis thaliana. Plant Cell 16, 1091-1104.
16. Danon, A., and Gallois, P. (1998). UV-C radiation induces apoptotic-like changes in Arabidopsis thaliana. FEBS Lett. 437, 131-136.
17. Danon, A., Rotari, V.I., Gordon, A., Mailhac, N., and Gallois, P. (2004). Ultraviolet-C overexposure induces programmed cell death in Arabidopsis, which is mediated by caspase-like activities and which can be suppressed by caspase inhibitors, p35 and Defender against Apoptotic Death. J. Biol. Chem. 279, 779-787.
18. Dietrich, R.A., Delaney, T.P., Uknes, S.J., Ward, E.R., Ryals, J.A., and Dangl, J.L. (1994). Arabidopsis mutants simulating disease resistance response. Cell 77, 565-577.
19. Doucet-Chabeaud, G., Godon, C., Brutesco, C., de Murcia, G., and Kazmaier, M. (2001). Ionising radiation induces the expression of PARP-1 and PARP-2 genes in Arabidopsis. Mol. Genet. Genomics 265, 954-963.
20. Doutriaux, M.P., Couteau, F., Bergounioux, C., and White, C. (1998). Isolation and characterisation of the RAD51 and DMC1 homologs from Arabidopsis thaliana. Mol. Gen. Genet. 257, 283-291.
21. Downes, C.S., Bachrati, C.Z., Devlin, S.J., Tommasino, M., Cutts, T.J., Watson, J.V., Rasko, I., and Johnson, R.T. (2000). Mammalian S-phase checkpoint integrity is dependent on transformation status and purine deoxyribonucleosides. J. Cell Sci. 113, 1089-1096.
22. Elledge, S.J., Zhou, Z., and Allen, J.B. (1992). Ribonucleotide reductase: Regulation, regulation, regulation. Trends Biochem. Sci. 17, 119-123.
23. Fobert, P.R., Coen, E.S., Murphy, G.J., and Doonan, J.H. (1994). Patterns of cell division revealed by transcriptional regulation of genes during the cell cycle in plants. EMBO J. 13, 616-624.
24. Greenberg, J.T. (1996). Programmed cell death: A way of life for plants. Proc. Natl. Acad. Sci. USA 93, 12094-12097.
25. Greenberg, J.T., and Yao, N. (2004). The role and regulation of programmed cell death in plant-pathogen interactions. Cell. Microbiol. 6, 201-211.
26. Hartung, F., Angelis, K.J., Meister, A., Schubert, I., Melzer, M., and Puchta, H. (2002). An archaebacterial topoisomerase homolog not present in other eukaryotes is indispensable for cell proliferation of plants. Curr. Biol. 12, 1787-1791.
27. Hemerly, A., Bergounioux, C., Van Montagu, M., Inze, D., and Ferreira, P. (1992). Genes regulating the plant cell cycle: Isolation of a mitotic-like cyclin from Arabidopsis thaliana. Proc. Natl. Acad. Sci. USA 89, 3295-3299.
28. Hennegan, K.P., and Danna, K.J. (1998). pBIN20: an improved binary vector for Agrobacterium-mediated transformation. Plant Mol. Biol. Rep. 16, 129-131.
29. Huang, M., Zhou, Z., and Elledge, S.J. (1998). The DNA replication and damage checkpoint pathways induce transcription by inhibition of the Crt1 repressor. Cell 94, 595-605.
30. Kaya, H., Shibahara, K.I., Taoka, K.I., Iwabuchi, M., Stillman, B., and Araki, T. (2001). FASCIATA genes for chromatin assembly factor-1 in Arabidopsis maintain the cellular organization of apical meristems. Cell 104, 131-142.
31. Kimura, T., Takeda, S., Sagiya, Y., Gotoh, M., Nakamura, Y., and Arakawa, H. (2003). Impaired function of p53R2 in Rrm2b-null mice causes severe renal failure through attenuation of dNTP pools. Nat. Genet. 34, 440-445.
32. Kolberg, M., Strand, K.R., Graft, P., and Andersson, K.K. (2004). Structure, function, and mechanism of ribonucleotide reductases. Biochim. Biophys. Acta 1699, 1-34.
33. Kressel, M., and Groscurth, P. (1994). Distinction of apoptotic and necrotic cell death by in situ labelling of fragmented DNA. Cell Tissue Res. 278, 549-556.
34. Kuriyama, H., and Fukuda, H. (2002). Developmental programmed cell death in plants. Curr. Opin. Plant Biol. 5, 568-573.
35. Levin, J.Z., Fletcher, J.C., Chen, X., and Meyerowitz, E.M. (1998). A genetic screen for modifiers of UFO meristem activity identifies three novel FUSED FLORAL ORGANS genes required for early flower development in Arabidopsis. Genetics 149, 579-595.
36. Lincker, F., Philipps, G., and Chaboute, M.E. (2004). UV-C response of the ribonucleotide reductase large subunit involves both E2F-mediated gene transcriptional regulation and protein subcellular relocalization in tobacco cells. Nucleic Acids Res. 32, 1430-1438.
37. Liu, C., Powell, K.A., Mundt, K., Wu, L., Carr, A.M., and Caspari, T. (2003). Cop9/signalosome subunits and Pcu4 regulate ribonucleotide reductase by both checkpoint-dependent and -independent mechanisms. Genes Dev. 17, 1130-1140.
38. Liu, Z., Franks, R.G., and Klink, V.P. (2000). Regulation of gynoecium marginal tissue formation by LEUNIG and AINTEGUMENTA. Plant Cell 12, 1879-1892.
39. Liu, Z., and Meyerowitz, E.M. (1995). LEUNIG regulates AGAMOUS expression in Arabidopsis flowers. Development 121, 975-991.
40. Liu, Z., Running, M.P., and Meyerowitz, E.M. (1997). TSO1 functions in cell division during Arabidopsis flower development. Development 124, 665-672.
41. Mayer, K.F., School, H., Haecker, A., Lenhard, M., Jurgens, G., and Laux, T. (1998). Role of WUSCHEL in regulating stem cell fate in the Arabidopsis shoot meristem. Cell 95, 805-815.
42. McCallum, C.M., Comai, L., Greene, E.A., and Henikoff, S. (2000). Targeting induced local lesions in genomes (TILLING) for plant functional genomics. Plant Physiol. 123, 439-442.
43. Miller, J.D., Arteca, R.N., and Pell, E.J. (1999). Senescence-associated gene expression during ozone-induced leaf senescence in Arabidopsis. Plant Physiol. 120, 1015-1024.
44. Oliver, F.J., Collins, M.K., and Lopez-Rivas, A. (1996). dNTP pools imbalance as a signal to initiate apoptosis. Experientia 52, 995-1000.
45. Osakabe, K., Yoshioka, T., Ichikawa, H., and Toki, S. (2002). Molecular cloning and characterization of RAD51-like genes from Arabidopsis thaliana. Plant Mol. Biol. 50, 71-81.
46. Parcy, F., Nilsson, O., Busch, M.A., Lee, I., and Weigel, D. (1998). A genetic framework for floral patterning. Nature 395, 561-566.
47. Philipps, G., Clement, B., and Gigot, C. (1995). Molecular characterization and cell cycle-regulated expression of a cDNA clone from Arabidopsis thaliana homologous to the small subunit of ribonucleotide reductase. FEBS Lett. 358, 67-70.
48. Pontier, D., Gan, S., Amasino, R.M., Roby, D., and Lam, E. (1999). Markers for hypersensitive response and senescence show distinct patterns of expression. Plant Mol. Biol. 39, 1243-1255.
49. Rate, D.N., Cuenca, J.V., Bowman, G.R., Guttman, D.S., and Greenberg, J.T. (1999). The gain-of-function Arabidopsis acd6 mutant reveals novel regulation and function of the salicylic acid signaling pathway in controlling cell death, defenses, and cell growth. Plant Cell 11, 1695-1708.
50. Reichard, P. (1988). Interactions between deoxyribonucleotide and DNA synthesis. Annu. Rev. Biochem. 57, 349-374.
51. Riha, K., McKnight, T.D., Griffing, L.R., and Shippen, D.E. (2001). Living with genome instability: Plant responses to telomere dysfunction. Science 291, 1797-1800.
52. Roy, B., Beuneu, C., Roux, P., Buc, H., Lemaire, G., and Lepoivre, M. (1999). Simultaneous determination of pyrimidine or purine deoxyribonucleoside triphosphates using a polymerase assay. Anal. Biochem. 269, 403-409.
53. Russell, D.A., Wong, D.M.L., and Sachs, M.M. (1990). The anaerobic response of soybean. Plant Physiol. 92, 401-407.
54. Saada, A., Shaag, A., Mandel, H., Nevo, Y., Eriksson, S., and Elpeleg, O. (2001). Mutant mitochondrial thymidine kinase in mitochondrial DNA depletion myopathy. Nat. Genet. 29, 342-344.
55. Saitoh, S., Chabes, A., McDonald, W.H., Thelander, L., Yates, J.R., and Russell, P. (2002). Cid13 is a cytoplasmic poly(A) polymerase that regulates ribonucleotide reductase mRNA. Cell 109, 563-573.
56. Schmid, M., Davison, T.S., Henz, S.R., Pape, U.J., Demar, M., Vingron, M., Scholkopf, B., Weigel, D., and Lohmann, J.U. (2005). A gene expression map of Arabidopsis thaliana development. Nat. Genet. 37, 501-506.
57. Siddiqui, N.U., Stronghill, P.E., Dangler, R.E., Hasenkampf, C.A., and Riggs, C.D. (2003). Mutations in Arabidopsis condensin genes disrupt embryogenesis, meristem organization and segregation of homologous chromosomes during meiosis. Development 130, 3283-3295.
58. Steimer, A., Amedeo, P., Afsar, K., Fransz, P., Scheid, O.M., and Paszkowski, J. (2000). Endogenous targets of transcriptional gene silencing in Arabidopsis. Plant Cell 12, 1165-1178.
59. Takeda, S., Tadele, Z., Hofmann, I., Probst, A.V., Angelis, K.J., Kaya, H., Araki, T., Mengiste, T., Scheid, O.M., Shibahara, K., Scheel, D., and Paszkowski, J. (2004). BRU1, a novel link between responses to DNA damage and epigenetic gene silencing in Arabidopsis. Genes Dev. 18, 782-793.
60. Tanaka, H., Arakawa, H., Yamaguchi, T., Shiraishi, K., Fukuda, S., Matsui, K., Takei, Y., and Nakamura, Y. (2000). A ribonucleotide reductase gene involved in a p53-dependent cell-cycle checkpoint for DNA damage. Nature 404, 42-49.
61. 2 accumulation in papillae and hypersensitive response during the barley-powdery mildew interaction. Plant J. 11, 1187-1194.
62. Vogelstein, B., Lane, D., and Levine, A.J. (2000). Surfing the p53 network. Nature 408, 307-310.
63. West, C.E., Waterworth, W.M., Story, G.W., Sunderland, P.A., Jiang, Q., and Bray, C.M. (2002). Disruption of the Arabidopsis AtKu80 gene demonstrates an essential role for AtKu80 protein in efficient repair of DNA double-strand breaks in vivo. Plant J. 31, 517-528.
64. Whittle, C.A., Beardmore, T., and Johnston, M.O. (2001). Is G1 arrest in plant seeds induced by a p53-related pathway? Trends Plant Sci. 6, 248-251.
65. Yao, R., Zhang, Z., An, X., Bucci, B., Perlstein, D.L., Stubbe, J., and Huang, M. (2003). Subcellular localization of yeast ribonucleotide reductase regulated by the DNA replication and damage checkpoint pathways. Proc. Natl. Acad. Sci. USA 100, 6628-6633.
66. Zhao, X., Chabes, A., Domkin, V., Thelander, L., and Rothstein, R. (2001). The ribonucleotide reductase inhibitor Sml1 is a new target of the Mec1/Rad53 kinase cascade during growth and in response to DNA damage. EMBO J. 20, 3544-3553.
67. Zhao, X., Georgieva, B., Chabes, A., Domkin, V., Ippel, J.H., Schleucher, J., Wijmenga, S., Thelander, L., and Rothstein, R. (2000). Mutational and structural analyses of the ribonucleotide reductase inhibitor Sml1 define its Rnr1 interaction domain whose inactivation allows suppression of mec1 and rad53 lethality. Mol. Cell. Biol. 20, 9076-9083.
68. Zhao, X., Muller, E.G., and Rothstein, R. (1998). A suppressor of two essential checkpoint genes identifies a novel protein that negatively affects dNTP pools. Mol. Cell 2, 329-340.