The catalytic subunit of Arabidopsis DNA polymerase α ensures stable maintenance of histone modification

Development (Cambridge)

Volumn 140, Issue 1, 2013, Pages 156-166

  Hyun, Youbong ^a   Yun, Hyein ^a   Park, Kyunghyuk ^a   Ohr, Hyonhwa ^a   Lee, Okchan ^a   Kim, Dong Hwan ^b   Sung, Sibum ^b   Choi, Yeonhee ^a,c  

^a Seoul National University   (South Korea)

^b UNIVERSITY OF TEXAS AT AUSTIN   (United States)

^c Seoul National University   (South Korea)

Author keywords

Chromatin assembly; DNA polymerase ; Epigenetic maintenance

Indexed keywords

DNA DIRECTED DNA POLYMERASE ALPHA; HISTONE; LIKE HETEROCHROMATIN PROTEIN 1; MEMBRANE PROTEIN; POLYCOMB REPRESSIVE COMPLEX 1; POLYCOMB REPRESSIVE COMPLEX 2; UNCLASSIFIED DRUG;

ALLELE; ARABIDOPSIS; ARTICLE; CATALYSIS; CONTROLLED STUDY; GENE EXPRESSION; GENE REPRESSION; HISTONE MODIFICATION; IMMUNOPRECIPITATION; MISSENSE MUTATION; MITOSIS; MUTANT; NONHUMAN; PRIORITY JOURNAL; VERNALIZATION;

ARABIDOPSIS; ARABIDOPSIS PROTEINS; CATALYTIC DOMAIN; DNA POLYMERASE I; ENZYME STABILITY; EPIGENESIS, GENETIC; HISTONES; MITOSIS; MUTATION, MISSENSE; PLANTS, GENETICALLY MODIFIED; PROTEIN SUBUNITS;

ARABIDOPSIS;

EID: 84870675105     PISSN: 09501991     EISSN: 14779129     Source Type: Journal    
DOI: 10.1242/dev.084624     Document Type: Article

References (58)

1. Ahmed, S., Saini, S., Arora, S. and Singh, J. (2001). Chromodomain protein Swi6-mediated role of DNA polymerase alpha in establishment of silencing in fission Yeast. J. Biol. Chem. 276, 47814-47821.
2. Alabert, C. and Groth, A. (2012). Chromatin replication and epigenome maintenance. Nat. Rev. Mol. Cell Biol. 13, 153-167.
3. Angel, A., Song, J., Dean, C. and Howard, M. (2011). A Polycomb-based switch underlying quantitative epigenetic memory. Nature 476, 105-108.
4. Barrero, J. M., González-Bayón, R., del Pozo, J. C., Ponce, M. R. and Micol, J. L. (2007). INCURVATA2 encodes the catalytic subunit of DNA Polymerase alpha and interacts with genes involved in chromatin-mediated cellular memory in Arabidopsis thaliana. Plant Cell 19, 2822-2838.
5. Chabouté, M. E., Clément, 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.
6. Choi, J., Hyun, Y., Kang, M. J., In Yun, H., Yun, J. Y., Lister, C., Dean, C., Amasino, R. M., Noh, B., Noh, Y. S. et al. (2009). Resetting and regulation of Flowering Locus C expression during Arabidopsis reproductive development. Plant J. 57, 918-931.
7. De Lucia, F., Crevillen, P., Jones, A. M., Greb, T. and Dean, C. (2008). A PHDpolycomb repressive complex 2 triggers the epigenetic silencing of FLC during vernalization. Proc. Natl. Acad. Sci. USA 105, 16831-16836.
8. del Olmo, I., López-González, L., Martín-Trillo, M. M., Martínez-Zapater, J. M., Piñeiro, M. and Jarillo, J. A. (2010). EARLY IN SHORT DAYS 7 (ESD7) encodes the catalytic subunit of DNA polymerase epsilon and is required for flowering repression through a mechanism involving epigenetic gene silencing. Plant J. 61, 623-636.
9. Exner, V., Aichinger, E., Shu, H., Wildhaber, T., Alfarano, P., Caflisch, A., Gruissem, W., Köhler, C. and Hennig, L. (2009). The chromodomain of LIKE HETEROCHROMATIN PROTEIN 1 is essential for H3K27me3 binding and function during Arabidopsis development. PLoS ONE 4, e5335.
10. Finnegan, E. J. and Dennis, E. S. (2007). Vernalization-induced trimethylation of histone H3 lysine 27 at FLC is not maintained in mitotically quiescent cells. Curr. Biol. 17, 1978-1983.
11. Gendall, A. R., Levy, Y. Y., Wilson, A. and Dean, C. (2001). The VERNALIZATION 2 gene mediates the epigenetic regulation of vernalization in Arabidopsis. Cell 107, 525-535.
12. Gong, Z., Morales-Ruiz, T., Ariza, R. R., Roldán-Arjona, T., David, L. and Zhu, J. K. (2002). ROS1, a repressor of transcriptional gene silencing in Arabidopsis, encodes a DNA glycosylase/lyase. Cell 111, 803-814.
13. Hansen, K. H., Bracken, A. P., Pasini, D., Dietrich, N., Gehani, S. S., Monrad, A., Rappsilber, J., Lerdrup, M. and Helin, K. (2008). A model for transmission of the H3K27me3 epigenetic mark. Nat. Cell Biol. 10, 1291-1300.
14. Helliwell, C. A., Wood, C. C., Robertson, M., James Peacock, W. and Dennis, E. S. (2006). The Arabidopsis FLC protein interacts directly in vivo with SOC1 and FT chromatin and is part of a high-molecular-weight protein complex. Plant J. 46, 183-192.
15. Heo, J. B. and Sung, S. (2011). Vernalization-mediated epigenetic silencing by a long intronic noncoding RNA. Science 331, 76-79.
16. Ingouff, M., Rademacher, S., Holec, S., Solji, L., Xin, N., Readshaw, A., Foo, S. H., Lahouze, B., Sprunck, S. and Berger, F. (2010). Zygotic resetting of the HISTONE 3 variant repertoire participates in epigenetic reprogramming in Arabidopsis. Curr. Biol. 20, 2137-2143.
17. Jeong, C. W., Roh, H., Dang, T. V., Choi, Y. D., Fischer, R. L., Lee, J. S. and Choi, Y. (2011). An E3 ligase complex regulates SET-domain polycomb group protein activity in Arabidopsis thaliana. Proc. Natl. Acad. Sci. USA 108, 8036-8041.
18. Jiang, D., Wang, Y., Wang, Y. and He, Y. (2008). Repression of FLOWERING LOCUS C and FLOWERING LOCUS T by the Arabidopsis Polycomb repressive complex 2 components. PLoS ONE 3, e3404.
19. 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.
20. Kim, D. H., Doyle, M. R., Sung, S. and Amasino, R. M. (2009). Vernalization: winter and the timing of flowering in plants. Annu. Rev. Cell Dev. Biol. 25, 277-299.
21. 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.
22. Ko, J. H., Mitina, I., Tamada, Y., Hyun, Y., Choi, Y., Amasino, R. M., Noh, B. and Noh, Y. S. (2010). Growth habit determination by the balance of histone methylation activities in Arabidopsis. EMBO J. 29, 3208-3215.
23. Kotogány, E., Dudits, D., Horváth, G. V. and Ayaydin, F. (2010). A rapid and robust assay for detection of S-phase cell cycle progression in plant cells and tissues by using ethynyl deoxyuridine. Plant Methods 6, 5.
24. Kunkel, T. A. and Burgers, P. M. (2008). Dividing the workload at a eukaryotic replication fork. Trends Cell Biol. 18, 521-527.
25. Lindroth, A. M., Shultis, D., Jasencakova, Z., Fuchs, J., Johnson, L., Schubert, D., Patnaik, D., Pradhan, S., Goodrich, J., Schubert, I. et al. (2004). Dual histone H3 methylation marks at lysines 9 and 27 required for interaction with CHROMOMETHYLASE3. EMBO J. 23, 4146-4155.
26. Liu, J., Ren, X., Yin, H., Wang, Y., Xia, R., Wang, Y. and Gong, Z. (2010a). Mutation in the catalytic subunit of DNA polymerase alpha influences transcriptional gene silencing and homologous recombination in Arabidopsis. Plant J. 61, 36-45.
27. Liu, Q., Wang, J., Miki, D., Xia, R., Yu, W., He, J., Zheng, Z., Zhu, J. K. and Gong, Z. (2010b). DNA replication factor C1 mediates genomic stability and transcriptional gene silencing in Arabidopsis. Plant Cell 22, 2336-2352.
28. Lu, F., Cui, X., Zhang, S., Jenuwein, T. and Cao, X. (2011). Arabidopsis REF6 is a histone H3 lysine 27 demethylase. Nat. Genet. 43, 715-719.
29. Majka, J. and Burgers, P. M. (2004). The PCNA-RFC families of DNA clamps and clamp loaders. Prog. Nucleic Acid Res. Mol. Biol. 78, 227-260.
30. Margueron, R. and Reinberg, D. (2010). Chromatin structure and the inheritance of epigenetic information. Nat. Rev. Genet. 11, 285-296.
31. Margueron, R., Justin, N., Ohno, K., Sharpe, M. L., Son, J., Drury, W. J., 3rd, Voigt, P., Martin, S. R., Taylor, W. R., De Marco, V. et al. (2009). Role of the polycomb protein EED in the propagation of repressive histone marks. Nature 461, 762-767.
32. Michaels, S. D., Himelblau, E., Kim, S. Y., Schomburg, F. M. and Amasino, R. M. (2005). Integration of flowering signals in winter-annual Arabidopsis. Plant Physiol. 137, 149-156.
33. Mylne, J. S., Barrett, L., Tessadori, F., Mesnage, S., Johnson, L., Bernatavichute, Y. V., Jacobsen, S. E., Fransz, P. and Dean, C. (2006). LHP1, the Arabidopsis homologue of HETEROCHROMATIN PROTEIN1, is required for epigenetic silencing of FLC. Proc. Natl. Acad. Sci. USA 103, 5012-5017.
34. Nakayama, J., Allshire, R. C., Klar, A. J. and Grewal, S. I. (2001). A role for DNA polymerase alpha in epigenetic control of transcriptional silencing in fission yeast. EMBO J. 20, 2857-2866.
35. O'Donnell, L., Panier, S., Wildenhain, J., Tkach, J. M., Al-Hakim, A., Landry, M. C., Escribano-Diaz, C., Szilard, R. K., Young, J. T., Munro, M. et al. (2010). The MMS22L-TONSL complex mediates recovery from replication stress and homologous recombination. Mol. Cell 40, 619-631.
36. Ono, T., Kaya, H., Takeda, S., Abe, M., Ogawa, Y., Kato, M., Kakutani, T., Mittelsten Scheid, O., Araki, T. and Shibahara, K. (2006). Chromatin assembly factor 1 ensures the stable maintenance of silent chromatin states in Arabidopsis. Genes Cells 11, 153-162.
37. Petruk, S., Sedkov, Y., Johnston, D. M., Hodgson, J. W., Black, K. L., Kovermann, S. K., Beck, S., Canaani, E., Brock, H. W. and Mazo, A. (2012). TrxG and PcG proteins but not methylated histones remain associated with DNA through replication. Cell 150, 922-933.
38. Pien, S., Fleury, D., Mylne, J. S., Crevillen, P., Inzé, D., Avramova, Z., Dean, C. and Grossniklaus, U. (2008). ARABIDOPSIS TRITHORAX1 dynamically regulates FLOWERING LOCUS C activation via histone 3 lysine 4 trimethylation. Plant Cell 20, 580-588.
39. Ransom, M., Dennehey, B. K. and Tyler, J. K. (2010). Chaperoning histones during DNA replication and repair. Cell 140, 183-195.
40. Satake, A. and Iwasa, Y. (2012). A stochastic model of chromatin modification: cell population coding of winter memory in plants. J. Theor. Biol. 302, 6-17.
41. Schubert, D., Primavesi, L., Bishopp, A., Roberts, G., Doonan, J., Jenuwein, T. and Goodrich, J. (2006). Silencing by plant Polycomb-group genes requires dispersed trimethylation of histone H3 at lysine 27. EMBO J. 25, 4638-4649.
42. Searle, I., He, Y., Turck, F., Vincent, C., Fornara, F., Kröber, S., Amasino, R. A. and Coupland, G. (2006). The transcription factor FLC confers a flowering response to vernalization by repressing meristem competence and systemic signaling in Arabidopsis. Genes Dev. 20, 898-912.
43. Serrano-Cartagena, J., Candela, H., Robles, P., Ponce, M. R., Pérez-Pérez, J. M., Piqueras, P. and Micol, J. L. (2000). Genetic analysis of incurvata mutants reveals three independent genetic operations at work in Arabidopsis leaf morphogenesis. Genetics 156, 1363-1377.
44. Sheldon, C. C., Hills, M. J., Lister, C., Dean, C., Dennis, E. S. and Peacock, W. J. (2008). Resetting of FLOWERING LOCUS C expression after epigenetic repression by vernalization. Proc. Natl. Acad. Sci. USA 105, 2214-2219.
45. Shindo, C., Aranzana, M. J., Lister, C., Baxter, C., Nicholls, C., Nordborg, M. and Dean, C. (2005). Role of FRIGIDA and FLOWERING LOCUS C in determining variation in flowering time of Arabidopsis. Plant Physiol. 138, 1163-1173.
46. Smith, D. J. and Whitehouse, I. (2012). Intrinsic coupling of lagging-strand synthesis to chromatin assembly. Nature 483, 434-438.
47. Stroud, H., Otero, S., Desvoyes, B., Ramírez-Parra, E., Jacobsen, S. E. and Gutierrez, C. (2012). Genome-wide analysis of histone H3.1 and H3.3 variants in Arabidopsis thaliana. Proc. Natl. Acad. Sci. USA 109, 5370-5375.
48. Sung, S. and Amasino, R. M. (2004). Vernalization in Arabidopsis thaliana is mediated by the PHD finger protein VIN3. Nature 427, 159-164.
49. Sung, S., He, Y., Eshoo, T. W., Tamada, Y., Johnson, L., Nakahigashi, K., Goto, K., Jacobsen, S. E. and Amasino, R. M. (2006). Epigenetic maintenance of the vernalized state in Arabidopsis thaliana requires LIKE HETEROCHROMATIN PROTEIN 1. Nat. Genet. 38, 706-710.
50. Takeda, S., Tadele, Z., Hofmann, I., Probst, A. V., Angelis, K. J., Kaya, H., Araki, T., Mengiste, T., Mittelsten Scheid, O., Shibahara, K. et al. (2004). BRU1, a novel link between responses to DNA damage and epigenetic gene silencing in Arabidopsis. Genes Dev. 18, 782-793.
51. Tamada, Y., Yun, J. Y., Woo, S. C. and Amasino, R. M. (2009). ARABIDOPSIS TRITHORAX-RELATED7 is required for methylation of lysine 4 of histone H3 and for transcriptional activation of FLOWERING LOCUS C. Plant Cell 21, 3257-3269.
52. Turck, F., Roudier, F., Farrona, S., Martin-Magniette, M. L., Guillaume, E., Buisine, N., Gagnot, S., Martienssen, R. A., Coupland, G. and Colot, V. (2007). Arabidopsis TFL2/LHP1 specifically associates with genes marked by trimethylation of histone H3 lysine 27. PLoS Genet. 3, e86.
53. Wittmeyer, J. and Formosa, T. (1997). The Saccharomyces cerevisiae DNA polymerase alpha catalytic subunit interacts with Cdc68/Spt16 and with Pob3, a protein similar to an HMG1-like protein. Mol. Cell. Biol. 17, 4178-4190.
54. Wood, C. C., Robertson, M., Tanner, G., Peacock, W. J., Dennis, E. S. and Helliwell, C. A. (2006). The Arabidopsis thaliana vernalization response requires a polycomb-like protein complex that also includes VERNALIZATION INSENSITIVE 3. Proc. Natl. Acad. Sci. USA 103, 14631-14636.
55. Xia, R., Wang, J., Liu, C., Wang, Y., Wang, Y., Zhai, J., Liu, J., Hong, X., Cao, X., Zhu, J. K. et al. (2006). ROR1/RPA2A, a putative replication protein A2, functions in epigenetic gene silencing and in regulation of meristem development in Arabidopsis. Plant Cell 18, 85-103.
56. Yin, H., Zhang, X., Liu, J., Wang, Y., He, J., Yang, T., Hong, X., Yang, Q. and Gong, Z. (2009). Epigenetic regulation, somatic homologous recombination, and abscisic acid signaling are influenced by DNA polymerase epsilon mutation in Arabidopsis. Plant Cell 21, 386-402.
57. Yoo, S. D., Cho, Y. H. and Sheen, J. (2007). Arabidopsis mesophyll protoplasts: a versatile cell system for transient gene expression analysis. Nat. Protoc. 2, 1565-1572.
58. Zhang, X., Germann, S., Blus, B. J., Khorasanizadeh, S., Gaudin, V. and Jacobsen, S. E. (2007). The Arabidopsis LHP1 protein colocalizes with histone H3 Lys27 trimethylation. Nat. Struct. Mol. Biol. 14, 869-871.