Arabidopsis TEBICHI, with helicase and DNA polymerase domains, is required for regulated cell division and differentiation in meristems

Plant Cell

Volumn 18, Issue 4, 2006, Pages 879-892

  Inagaki, Soichi ^a   Suzuki, Takamasa ^a   Ohto, Masa Aki ^b,d   Urawa, Hiroko ^b,e   Horiuchi, Takashi ^b   Nakamura, Kenzo ^a   Morikami, Atsushi ^c  

^a NAGOYA UNIVERSITY   (Japan)

^b NATIONAL INSTITUTE FOR BASIC BIOLOGY   (Japan)

^c MEIJO UNIVERSITY   (Japan)

^d UNIVERSITY OF CALIFORNIA   (United States)

^e NATIONAL INSTITUTE OF TECHNOLOGY AND EVALUATION   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

BIODIVERSITY; CELLS; DNA; GENES; MUTAGENESIS; PLANTS (BOTANY);

MERISTEMS; POLYMERASE; TEB MUTANTS; TEBICHI (TEB) GENE;

PROTEINS;

BIODIVERSITY; CELLS; GENES; MUTAGENS; NUCLEIC ACIDS; PLANTS; PROTEINS;

ANIMALIA; ARABIDOPSIS; ARABIDOPSIS THALIANA; MAMMALIA;

EID: 33745445746     PISSN: 10404651     EISSN: None     Source Type: Journal    
DOI: 10.1105/tpc.105.036798     Document Type: Article

References (74)

1. Abraham, R.T. (2001). Cell cycle checkpoint signaling through the ATM and ATR kinases. Genes Dev. 15, 2177-2196.
2. Alonso, J.M., et al. (2003). Genome-wide insertional mutagenesis of Arabidopsis thaliana. Science 301, 653-657.
3. Barbour, L., and Xiao, W. (2003). Regulation of alternative replication bypass pathways at stalled replication forks and its effects on genome stability: A yeast model. Mutat. Res. 532, 137-155.
4. Bilbao, C., Ferreiro, J.A., Comendador, M.A., and Sierra, L.M. (2002). Influence of mus201 and mus308 mutations of Drosophila melanogaster on the genotoxicity of model chemicals in somatic cells in vivo measured with the comet assay. Mutat. Res. 503, 11-19.
5. Birnbaum, K., Shasha, D.E., Wang, J.Y., Jung, J.W., Lambert, G.M., Galbraith, D.W., and Benfey, P.N. (2003). A gene expression map of the Arabidopsis root. Science 302, 1956-1960.
6. Boisnard-Lorig, C., Colon-Carmona, A., Bauch, M., Hodge, S., Doerner, P., Bancharel, E., Dumas, C., Haseloff, J., and Berger, F. (2001). Dynamic analyses of the expression of the HISTONE::YFP fusion protein in Arabidopsis show that syncytial endosperm is divided in mitotic domains. Plant Cell 13, 495-509.
7. Boyd, J.B., Sakaguchi, K., and Harris, P.V. (1990). mus308 mutants of Drosophila exhibit hypersensitivity to DNA cross-linking agents and are defective in a deoxyribonuclease. Genetics 125, 813-819.
8. Brewer, B.J., and Fangman, W.L. (1987). The localization of replication origins on ARS plasmids in S. cerevisiae. Cell 51, 463-471.
9. Britt, A.B. (1999). Molecular genetics of DNA repair in higher plants. Trends Plant Sci. 4, 20-25.
10. 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.
11. Carles, C.C., Choffnes-Inada, D., Reville, K., Lertpiriyapong, K., and Fletcher, J.C. (2005). ULTRAPETALA1 encodes a SAND domain putative transcriptional regulator that controls shoot and floral meristem activity in Arabidopsis. Development 132, 897-911.
12. Clark, S.E., Running, M.P., and Meyerowitz, M. (1995). CLAVATA3 is a specific regulator of shoot and floral meristem development affecting the same processes as CLAVATA1. Development 121, 2057-2067.
13. Colon-Carmona, A., You, R., Haimovitch-Gal, T., and Doerner, P. (1999). Technical advance. Spatio-temporal analysis of mitotic activity with a labile cyclin-GUS fusion protein. Plant J. 20, 503-508.
14. Costanzo, V., Robertson, K., Bibikova, M., Kim, E., Grieco, D., Gottesman, M., Carroll, D., and Gautier, J. (2001). Mre11 protein complex prevents double-strand break accumulation during chromosomal DNA replication. Mol. Cell 8, 137-147.
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. Deveaux, Y., Alonso, B., Pierrugues, O., Godon, C., and Kazmaier, M. (2000). Molecular cloning and developmental expression of AtGR1, a new growth-related Arabidopsis gene strongly induced by ionizing radiation. Radiat. Res. 154, 355-364.
17. Di Laurenzio, L., Wysocka-Diller, J., Malamy, J.E., Pysh, L., Helariutta, Y., Freshour, G., Hahn, M.G., Feldmann, K.A., and Benfey, P.M. (1996). The SCARECROW gene regulates an asymmetric cell division that is essential for generating the radial organization of the Arabidopsis root. Cell 86, 423-433.
18. Donnelly, P.M., Bonetta, D., Tsukaya, H., Dengler, R.E., and Dengler, N.G. (1999). Cell cycling and cell enlargement in developing leaves of Arabidopsis. Dev. Biol. 215, 407-419.
19. Enomoto, S., and Berman, J. (1998). Chromatin assembly factor I contributes to the maintenance, but not the re-establishment, of silencing at the yeast silent mating loci. Genes Dev. 12, 219-232.
20. Fletcher, J.C. (2001). The ULTRAPETALA gene controls shoot and floral meristem size in Arabidopsis. Development 128, 1323-1333.
21. Fukaki, H., Wysocka-Diller, J., Kato, T., Fujisawa, H., Benfey, P.M., and Tasaka, M. (1998). Genetic evidence that the endodermis is essential for shoot gravitropism in Arabidopsis thaliana. Plant J. 14, 425-430.
22. Garcia, V., Bruchet, H., Camescasse, D., Granier, F., Bouchez, D., and Tissier, A. (2003). AtATM is essential for meiosis and the somatic response to DNA damage in plants. Plant Cell 15, 119-132.
23. Green, K.A., Prigge, M.J., Katzman, R.B., and Clark, S.E. (2005). CORONA, a member of the class III homeodomain leucine zipper gene family in Arabidopsis, regulates stem cell specification and organogenesis. Plant Cell 17, 691-704.
24. Guyomarc'h, S., Vernoux, T., Traas, J., Zhou, D.X., and Delarue, M. (2004). MGOUN3, an Arabidopsis gene with tetratricopeptide-repeat-related motifs, regulates meristem cellular organization. J. Exp. Bot. 55, 673-684.
25. Harris, P.V., Mazina, O.M., Leonhardt, E.A., Case, R.B., Boyd, J.B., and Burtis, K.C. (1996). Molecular cloning of Drosophila mus308, a gene involved in DNA cross-link repair with homology to prokaryotic DNA polymerase I genes. Mol. Cell. Biol. 16, 5764-5771.
26. Helariutta, Y., Fukaki, H., Wysocka-Diller, J., Nakajima, K., Jung, J., Sena, G., Hauser, M.T., and Benfey, P.M. (2000). The SHORT-ROOT gene controls radial patterning of the Arabidopsis root, through radial signaling. Cell 101, 555-567.
27. Jenik, P.D., Jurkuta, R.E., and Barton, M.K. (2005). Interactions between the cell cycle and embryonic patterning in Arabidopsis uncovered by a mutation in DNA polymerase ε. Plant Cell 17, 3362-3377.
28. Jurgens, G., and Mayer, U. (1994). Arabidopsis. In A Color Atlas of Developing Embryos, J. Bard, ed (London: Wolfe Publishing), pp. 7-21.
29. 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.
30. Keil, R.L., and Roeder, G.S. (1984). Cis-acting, recombination- stimulating activity in a fragment of the ribosomal DNA of S. cerevisiae. Cell 39, 377-386.
31. Klimyuk, V.I., and Jones, J.D. (1997). AtDMC1, the Arabidopsis homologue of the yeast DMC1 gene: Characterization, transposon-induced allelic variation and meiosis-associated expression. Plant J. 11, 1-14.
32. Kobayashi, T., Hidaka, M., Nishizawa, M., and Horiuchi, T. (1992). Identification of a site required for DNA replication fork blocking activity in the rRNA gene cluster in Saccharomyces cerevisiae. Mol. Gen. Genet. 233, 355-362.
33. Lafarge, S., and Montane, M.H. (2003). Characterization of Arabidopsis thaliana ortholog of the human breast cancer susceptibility gene 1: AtBRCA1, strongly induced by gamma rays. Nucleic Acids Res. 31, 1148-1155.
34. Laufs, P., Dockx, J., Kronenberger, J., and Traas, J. (1998). MGOUN1 and MGOUN2: Two genes required for primordium initiation at the shoot apical and floral meristems in Arabidopsis thaliana. Development 125, 1253-1260.
35. Laux, T., Mayer, K.F., Berger, J., and Jurgens, G. (1996). The WUSCHEL gene is required for shoot and floral meristem integrity in Arabidopsis. Development 122, 87-96.
36. Leonhardt, E.A., Henderson, D.S., Rinehart, J.E., and Boyd, J.B. (1993). Characterization of the mus308 gene in Drosophila melanogaster. Genetics 133, 87-96.
37. Leyser, H.M.O., and Furner, I.J. (1992). Characterisation of three shoot apical meristem mutants of Arabidopsis thaliana. Development 116, 397-403.
38. Lupo, R., Breiling, A., Bianchi, M.E., and Orlando, V. (2001). Drosophila chromosome condensation proteins Topoisomerase II and Barren colocalize with Polycomb and maintain Fab-7 PRE silencing. Mol. Cell 7, 127-136.
39. Marini, F., Kim, N., Schuffert, A., and Wood, R.D. (2003). POLN, a nuclear PolA family DNA polymerase homologous to the DNA cross-link sensitivity protein Mus308. J. Biol. Chem. 278, 32014-32019.
40. Mayer, K.F., Schoof, 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.
41. Menges, M., Hennig, L., Gruissem, W., and Murray, J.A. (2002). Cell cycle-regulated gene expression in Arabidopsis. J. Biol. Chem. 277, 41987-42002.
42. Monson, E.K., de Bruin, D., and Zakian, V.A. (1997). The yeast Cac1 protein is required for the stable inheritance of transcriptionally repressed chromatin at telomeres. Proc. Natl. Acad. Sci. USA 94, 13081-13086.
43. Murashige, T., and Skoog, F. (1962). A revised medium for growth and bioassays with tobacco cell cultures. Physiol. Plant. 15, 473-497.
44. Nakajima, K., Sena, G., Nawy, T., and Benfey, P.M. (2001). Intercellular movement of the putative transcription factor SHR in root patterning. Nature 413, 307-311.
45. Oshige, M., Aoyagi, N., Harris, P.V., Burtis, K.C., and Sakaguchi, K. (1999). A new DNA polymerase species from Drosophila melanogaster. A probable mus308 gene product. Mutat. Res. 433, 183-192.
46. Prigge, M.J., Otsuga, D., Alonso, J.M., Ecker, J.R., Drews, G.N., and Clark, S.E. (2005). Class III homeodomain-leucine zipper gene family members have overlapping, antagonistic, and distinct roles in Arabidopsis development. Plant Cell 17, 61-76.
47. Sabatini, S., Beis, D., Wolkenfelt, H., Murfett, J., Guilfoyle, T., Malamy, J., Benfey, P., Leyser, O., Bechtold, N., Weisbeek, P., and Scheres, B. (1999). An auxin-dependent distal organizer of pattern and polarity in the Arabidopsis root. Cell 99, 463-472.
48. Saze, H., Scheid, O.M., and Paszkowski, J. (2003). Maintenance of CpG methylation is essential for epigenetic inheritance during plant gametogenesis. Nat. Genet. 34, 65-69.
49. Scheres, B., Laurenzio, L.D., Willemsen, V., Hauser, M.T., Janmaat, K., Wisbeek, P., and Benfey, P.M. (1995). Mutations affecting the radial organization of the Arabidopsis root display specific defects throughout the embryonic axis. Development 121, 53-62.
50. Scheres, B., Wolkenfelt, H., Willemsen, V., Terlouw, M., Lawson, E., Dean, C., and Weisbeek, P. (1994). Embryonic origin of the Arabidopsis primary root and root meristem initials. Development 120, 2475-2487.
51. Schoof, H., Lenhard, M., Haecker, A., Mayer, K.F., Jurgens, G., and Laux, T. (2000). The stem cell population of Arabidopsis shoot meristems is maintained by a regulatory loop between the CLAVATA and WUSCHEL genes. Cell 100, 635-644.
52. Segers, G., Gadisseur, I., Bergounioux, C., de Almeida Engler, J., Jacqmard, A., Van Montagu, M., and Inze, D. (1996). The Arabidopsis cyclin-dependent kinase gene cdc2bAt is preferentially expressed during S and G2 phases of the cell cycle. Plant J. 10, 601-612.
53. Seki, M., Marini, F., and Wood, R.D. (2003). POLQ (Pol θ), a DNA polymerase and DNA-dependent ATPase in human cells. Nucleic Acids Res. 31, 6117-6126.
54. Shiloh, Y. (2003). ATM and related protein kinases: Safeguarding genome integrity. Nat. Rev. Cancer 3, 155-168.
55. Shima, N., Hartford, S.A., Duffy, T., Wilson, L.A., Schimenti, K.J., and Schimenti, J.C. (2003). Phenotype-based identification of mouse chromosome instability mutants. Genetics 163, 1031-1040.
56. Siddiqui, N.U., Stronghill, P.E., Dengler, 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.
57. Smith, S., and Stillman, B. (1989). Purification and characterization of CAF-I, a human cell factor required for chromatin assembly during DNA replication in vitro. Cell 58, 15-25.
58. Sorrell, D.A., Marchbank, A., McMahon, K., Dickinson, J.R., Rogers, H.J., and Francis, D. (2002). A WEE1 homologue from Arabidopsis thaliana. Planta 215, 518-522.
59. 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.
60. Suzuki, T., Inagaki, S., Nakajima, S., Akashi, T., Ohto, M.A., Kobayashi, M., Seki, M., Shinozaki, K., Kato, T., Tabata, S., Nakamura, K., and Morikami, A. (2004). A novel Arabidopsis gene TONSOKU is required for proper cell arrangement in root and shoot apical meristems. Plant J. 38, 673-684.
61. Suzuki, T., Nakajima, S., Inagaki, S., Hirano-Nakakita, M., Matsuoka, K., Demura, T., Fukuda, H., Morikami, A., and Nakamura, K. (2005a). TONSOKU is expressed in S phase of the cell cycle and its defect delays cell cycle progression in Arabidopsis. Plant Cell Physiol. 46, 736-742.
62. Suzuki, T., Nakajima, S., Morikami, A., and Nakamura, K. (2005b). An Arabidopsis protein with a novel calcium-binding repeat sequence interacts with TONSOKU/MGOUN3/BRUSHY1 involved in meristem maintenance. Plant Cell Physiol. 46, 1452-1461.
63. 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.
64. Tuteja, N., and Tuteja, R. (2004). Unraveling DNA helicases. Motif, structure, mechanism and function. Eur. J. Biochem. 271, 1849-1863.
65. Ulmasov, T., Murfett, J., Hagen, G., and Guilfoyle, T.J. (1997). Aux/IAA proteins repress expression of reporter genes containing natural and highly active synthetic auxin response elements. Plant Cell 9, 1963-1971.
66. Umeda, M., Umeda-Hara, C., Yamaguchi, M., Hashimoto, J., and Uchimiya, H. (1999). Differential expression of genes for cyclin-dependent protein kinases in rice plants. Plant Physiol. 119, 31-40.
67. Urawa, H., Hidaka, M., Ishiguro, S., Okada, K., and Horiuchi, T. (2001). Enhanced homologous recombination caused by the non-transcribed spacer of the rDNA in Arabidopsis. Mol. Genet. Genomics 266, 546-555.
68. Weigmann, K., and Lehner, C.F. (1995). Cell fate specification by even-stopped expression in the Drosophila nervous system is coupled to cell cycle progression. Development 121, 3713-3721.
69. Williams, L., Grigg, S.P., Xie, M., Christensen, S., and Fletcher, J.C. (2005). Regulation of Arabidopsis shoot apical meristem and lateral organ formation by microRNA miR166g and its AtHD-ZIP target genes. Development 132, 3657-3668.
70. Wysocka-Diller, J.W., Helariutta, Y., Fukaki, H., Malamy, J.E., and Benfey, P.M. (2000). Molecular analysis of SCARECROW function reveals a radial patterning mechanism common to root and shoot. Development 127, 595-603.
71. Ye, X., Franco, A.A., Santos, H., Nelson, D.M., Kaufman, P.D., and Adams, P.D. (2003). Defective S phase chromatin assembly causes DNA damage, activation of the S phase checkpoint, and S phase arrest. Mol. Cell 11, 341-351.
72. Yu, Y., Steinmetz, A., Meyer, D., Brown, S., and Shen, W.H. (2003). The tobacco A-type cyclin, Nicta;CYCA3;2, at the nexus of cell division and differentiation. Plant Cell 15, 2763-2777.
73. Zhang, Z., Shibahara, K., and Stillman, B. (2000). PCNA connects DNA replication to epigenetic inheritance in yeast. Nature 408, 221-225.
74. Zhong, R., and Ye, Z.H. (2004). amphivasal vascular bundle 1, a gain-of-function mutation of the IFL1/REV gene, is associated with alterations in the polarity of leaves, stems and carpels. Plant Cell Physiol. 45, 369-385.