MIDGET unravels functions of the Arabidopsis topoisomerase VI complex in DNA endoreduplication, chromatin condensation, and transcriptional silencing

Plant Cell

Volumn 19, Issue 10, 2007, Pages 3100-3110

  Kirik, Viktor ^a,b   Schrader, Andrea ^a   Uhrig, Joachim F ^a   Hulskamp, Martin ^a  

^a UNIVERSITY OF COLOGNE   (Germany)

^b GEOPHYSICAL LABORATORY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BIOLOGICAL MATERIALS; DNA; ENZYME ACTIVITY; PROTEINS; TRANSCRIPTION;

CHROMATIN CONDENSATION; DNA ENDOREDUPLICATION; ENDOREDUPLICATION CYCLES; TRANSCRIPTIONAL SILENCING;

PLANTS (BOTANY);

ARABIDOPSIS; ARCHAEA;

EID: 37249024654     PISSN: 10404651     EISSN: 1532298X     Source Type: Journal    
DOI: 10.1105/tpc.107.054361     Document Type: Article

References (55)

1. Becker, D., Kemper, E., Schell, J., and Masterson, R. (1992). New plant binary vectors with selectable markers located proximal to the left T-DNA border. Plant Mol. Biol. 20: 1195-1197.
2. Bergerat, A., de Massy, B., Gadelle, D., Varoutas, P.C., Nicolas, A., and Forterre, P. (1997). An atypical topoisomerase II from Archaea with implications for meiotic recombination. Nature 386: 414-417.
3. Bergerat, A., Gadelle, D., and Forterre, P. (1994). Purification of a DNA topoisomerase II from the hyperthermophilic archaeon Sulfolobus shibatae. A thermostable enzyme with both bacterial and eucaryal features. J. Biol. Chem. 269: 27663-27669.
4. Bernhardt, C., Zhao, M., Gonzalez, A., Lloyd, A., and Schiefelbein, J. (2005). The bHLH genes GL3 and EGL3 participate in an intercellular regulatory circuit that controls cell patterning in the Arabidopsis root epidermis. Development 132: 291-298.
5. Bult, C.J., et al. (1996). Complete genome sequence of the methanogenic archaeon, Methanococcus jannaschii. Science 273: 1058-1073.
6. Champoux, J.J. (2001). DNA topoisomerases: Structure, function, and mechanism. Annu. Rev. Biochem. 70: 369-413.
7. Colon-Carmona, A., You, R., Haimovitch, T., and Doerner, P. (1999). Spatio-temporal analysis of mitotic activity with a labile cyclin-GUS fusion protein. Plant J. 20: 503-508.
8. Corbett, K.D., and Berger, J.M. (2003a). Structure of the topoisomerase VI-B subunit: Implications for type II topoisomerase mechanism and evolution. EMBO J. 22: 151-163.
9. Corbett, K.D., and Berger, J.M. (2003b). Emerging roles for plant topoisomerase VI. Chem. Biol. 10: 107-111.
10. Costa, S., and Shaw, P. (2006). Chromatin organization and cell fate switch respond to positional information in Arabidopsis. Nature 439: 493-496.
11. Culligan, K., Tissier, A., and Britt, A. (2004). ATR regulates a G2 phase cell-cycle checkpoint in Arabidopsis thaliana. Plant Cell 16: 1091-1104.
12. Culligan, K.M., Robertson, C.E., Foreman, J., Doerner, P., and Britt, A.B. (2006). ATR and ATM play both distinct and additive roles in response to ionizing radiation. Plant J. 48: 947-961.
13. Cuvier, O., and Hirano, T. (2003). A role of topoisomerase II in linking DNA replication to chromosome condensation. J. Cell Biol. 160: 645-655.
14. Deming, P.B., Cistulli, C.A., Zhao, H., Graves, P.R., Piwnica-Worms, H., Paules, R.S., Downes, C.S., and Kaufmann, W.K. (2001). The human decatenation checkpoint. Proc. Natl. Acad. Sci. USA 98: 12044-12049.
15. Earley, K.W., Haag, J.R., Pontes, O., Opper, K., Juehne, T., Song, K., and Pikaard, C.S. (2006). Gateway-compatible vectors for plant functional genomics and proteomics. Plant J. 45: 616-629.
16. Fransz, P., De Jong, J.H., Lysak, M., Castiglione, M.R., and Schubert, I. (2002). Interphase chromosomes in Arabidopsis are organized as well defined chromocenters from which euchromatin loops emanate. Proc. Natl. Acad. Sci. USA 99: 14584-14589.
17. Gasser, S.M., Laroche, T., Falquet, J., Boy de la Tour, E., and Laemmli, U.K. (1986). Metaphase chromosome structure. Involvement of topoisomerase II. J. Mol. Biol. 188: 613-629.
18. Gimenez-Abian, J.F., Weingartner, M., Binarova, P., Clarke, D.J., Anthony, R.G., Calderini, O., Heberle-Bors, E., Moreno Diaz de la Espina, S., Bogre, L., and De la Torre, C. (2002). A topoisomerase II-dependent checkpoint in G2-phase plant cells can be bypassed by ectopic expression of mitotic cyclin B2. Cell Cycle 1: 187-192.
19. Grebenok, R.J., Pierson, E., Lambert, G.M., Gong, F.C., Afonso, C.L., Haldeman-Cahill, R., Carrington, J.C., and Galbraith, D.W. (1997). Green-fluorescent protein fusions for efficient characterization of nuclear targeting. Plant J. 11: 573-586.
20. Grelon, M., Vezon, D., Gendrot, G., and Pelletier, G. (2001). AtSPO11-1 is necessary for efficient meiotic recombination in plants. EMBO J. 20: 589-600.
21. 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.
22. Hartung, F., and Puchta, H. (2000). Molecular characterisation of two paralogous SPO11 homologues in Arabidopsis thaliana. Nucleic Acids Res. 28: 1548-1554.
23. Hartung, F., and Puchta, H. (2001). Molecular characterization of homologues of both subunits A (SPO11) and B of the archaebacterial topoisomerase 6 in plants. Gene 271: 81-86.
24. Hefner, E., Huefner, N., and Britt, A.B. (2006). Tissue-specific regulation of cell-cycle responses to DNA damage in Arabidopsis seedlings. DNA Repair (Amst.) 5: 102-110.
25. Hulskamp, M., Misera, S., and Jürgens, G. (1994). Genetic dissection of trichome cell development in Arabidopsis. Cell 76: 555-566.
26. Jones, M.A., Shen, J.J., Fu, Y., Yang, Z., and Grierson, C.S. (2002). The Arabidopsis Rop2 GTPase is a positive regulator of both root hair initiation and tip growth. Plant Cell 14: 763-776.
27. Kirik, A., Pecinka, A., Wendeler, E., and Reiss, B. (2006). The chromatin assembly factor subunit FASCIATA1 is involved in homologous recombination in plants. Plant Cell 18: 2431-2442.
28. Kurz, E.U., and Lees-Miller, S.P. (2004). DNA damage-induced activation of ATM and ATM-dependent signaling pathways. DNA Repair (Amst.) 3: 889-900.
29. Larkin, J.C., Walker, J.D., Bolognesi-Winfield, A.C., Gray, J.C., and Walker, A.R. (1999). Allele-specific interactions between ttg and gl1 during trichome development in Arabidopsis thaliana. Genetics 151: 1591-1604.
30. Lee, M.M., and Schiefelbein, J. (2002). Cell patterning in the Arabidopsis root epidermis determined by lateral inhibition with feedback. Plant Cell 14: 611-618.
31. LeRoy, G., Loyola, A., Lane, W.S., and Reinberg, D. (2000). Purification and characterization of a human factor that assembles and remodels chromatin. J. Biol. Chem. 275: 14787-14790.
32. Letunic, I., Copley, R.R., Pils, B., Pinkert, S., Schultz, J., and Bork, P. (2006). SMART 5: Domains in the context of genomes and networks. Nucleic Acids Res. 34: D257-D260.
33. Liu, L.F., and Wang, J.C. (1987). Supercoiling of the DNA template during transcription. Proc. Natl. Acad. Sci. USA 84: 7024-7027.
34. Mathur, J., and Koncz, C. (1998). PEG-mediated protoplast transformation with naked DNA. Methods Mol. Biol. 82: 267-276.
35. Nichols, M.D., DeAngelis, K., Keck, J.L., and Berger, J.M. (1999). Structure and function of an archaeal topoisomerase VI subunit with homology to the meiotic recombination factor Spo11. EMBO J. 18: 6177-6188.
36. Perazza, D., Herzog, M., Hulskamp, M., Brown, S., Dorne, A., and Bonneville, J. (1999). Trichome cell growth in Arabidopsis thaliana can be depressed by mutations in at least five genes. Genetics 152: 461-476.
37. Robbins, J., Dilworth, S.M., Laskey, R.A., and Dingwall, C. (1991). Two interdependent basic domains in nucleoplasmin nuclear targeting sequence: Identification of a class of bipartite nuclear targeting sequence. Cell 64: 615-623.
38. Sancar, A., Lindsey-Boltz, L.A., Unsal-Kacmaz, K., and Linn, S. (2004). Molecular mechanisms of mammalian DNA repair and the DNA damage checkpoints. Annu. Rev. Biochem. 73: 39-85.
39. Schnittger, A., Schobinger, U., Stierhof, Y.D., and Hulskamp, M. (2002). Ectopic B-type cyclin expression induces mitotic cycles in endoreduplicating Arabidopsis trichomes. Curr. Biol. 12: 415-420.
40. Schultz, J., Milpetz, F., Bork, P., and Ponting, C.P. (1998). SMART, a simple modular architecture research tool: identification of signaling domains. Proc. Natl. Acad. Sci. USA 95: 5857-5864.
41. Shechter, D., Costanzo, V., and Gautier, J. (2004). Regulation of DNA replication by ATR: Signaling in response to DNA intermediates. DNA Repair (Amst.) 3: 901-908.
42. Soellick, T.R., and Uhrig, J.F. (2001). Development of an optimized interaction-mating protocol for large-scale yeast two-hybrid analyses. Genome Biol. 2: RESEARCH0052.
43. Stacey, N.J., Kuromori, T., Azumi, Y., Roberts, G., Breuer, C., Wada, T., Maxwell, A., Roberts, K., and Sugimoto-Shirasu, K. (2006). Arabidopsis SPO11-2 functions with SPO11-1 in meiotic recombination. Plant J. 48: 206-216.
44. Steimer, A., Amedeo, P., Afsar, K., Fransz, P., Mittelsten Scheid, O., and Paszkowski, J. (2000). Endogenous targets of transcriptional gene silencing in Arabidopsis. Plant Cell 12: 1165-1178.
45. Sugimoto-Shirasu, K., Roberts, G.R., Stacey, N.J., McCann, M.C., Maxwell, A., and Roberts, K. (2005). RHL1 is an essential component of the plant DNA topoisomerase VI complex and is required for ploidy-dependent cell growth. Proc. Natl. Acad. Sci. USA 102: 18736-18741.
46. Sugimoto-Shirasu, K., Stacey, N.J., Corsar, J., Roberts, K., and McCann, M.C. (2002). DNA Topoisomerase VI is essential for endoreduplication in Arabidopsis. Curr. Biol. 12: 1782-1786.
47. Uemura, T., Ohkura, H., Adachi, Y., Morino, K., Shiozaki, K., and Yanagida, M. (1987). DNA topoisomerase II is required for condensation and separation of mitotic chromosomes in S. pombe. Cell 50: 917-925.
48. Varga-Weisz, P.D., Wilm, M., Bonte, E., Dumas, K., Mann, M., and Becker, P.B. (1997). Chromatin remodelling factor CHRAC contains the ATPases ISWI and topoisomerase II. Nature 388: 598-602.
49. Vroemen, C.W., Langeveld, S., Mayer, U., Ripper, G., Jürgens, G., Kammen, A.V., and Vries, S.C.D. (1996). Pattern formation in the Arabidopsis embryo revealed by position-specific lipid transfer protein gene expression. Plant Cell 8: 783-791.
50. Walker, J.D., Oppenheimer, D.G., Concienne, J., and Larkin, J.C. (2000). SIAMESE, a gene controlling the endoreduplication cell cycle in Arabidopsis thaliana trichomes. Development 127: 3931-3940.
51. Walter, M., Chaban, C., Schutze, K., Batistic, O., Weckermann, K., Nake, C., Blazevic, D., Grefen, C., Schumacher, K., Oecking, C., Harter, K., and Kudla, J. (2004). Visualization of protein interactions in living plant cells using bimolecular fluorescence complementation. Plant J. 40: 428-438.
52. Wang, J.C. (2002). Cellular roles of DNA topoisomerases: A molecular perspective. Nat. Rev. Mol. Cell Biol. 3: 430-440.
53. Weigel, D., et al. (2000). Activation tagging in Arabidopsis. Plant Physiol. 122: 1003-1013.
54. Xie, S., and Lam, E. (1994). Abundance of nuclear DNA topoisomerase II is correlated with proliferation in Arabidopsis thaliana. Nucleic Acids Res. 22: 5729-5736.
55. Yin, Y., Cheong, H., Friedrichsen, D., Zhao, Y., Hu, J., Mora-Garcia, S., and Chory, J. (2002). A crucial role for the putative Arabidopsis topoisomerase VI in plant growth and development. Proc. Natl. Acad. Sci. USA 99: 10191-10196.