Seed dormancy cycling in Arabidopsis: Chromatin remodelling and regulation of DOG1 in response to seasonal environmental signals

Plant Journal

Volumn 81, Issue 3, 2015, Pages 413-425

  Footitt, Steven ^a   Müller, Kerstin ^b   Kermode, Allison R ^b   Finch Savage, William E ^a  

^a UNIVERSITY OF WARWICK   (United Kingdom)

^b SIMON FRASER UNIVERSITY   (Canada)

Author keywords

Arabidopsis; chromatin remodelling; dormancy cycling; histone acetylation; histone methylation; histone ubiquitination

Indexed keywords

ACETYLATION; ALKYLATION; GENE EXPRESSION; PLANTS (BOTANY);

ARABIDOPSIS; CHROMATIN REMODELLING; DORMANCY CYCLING; HISTONE ACETYLATION; HISTONE METHYLATION; UBIQUITINATION;

ENVIRONMENTAL REGULATIONS;

ARABIDOPSIS;

ARABIDOPSIS PROTEIN; CURLY LEAF PROTEIN, ARABIDOPSIS; DOG1 PROTEIN, ARABIDOPSIS; HISTONE; HISTONE LYSINE METHYLTRANSFERASE; HOMEODOMAIN PROTEIN; NUCLEAR PROTEIN; ROS1 PROTEIN, ARABIDOPSIS; SUVH4 PROTEIN, ARABIDOPSIS; SWINGER PROTEIN, ARABIDOPSIS; TRANSCRIPTION FACTOR;

ACETYLATION; ARABIDOPSIS; CHROMATIN ASSEMBLY AND DISASSEMBLY; DORMANCY; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; PHYSIOLOGY; SEASON; TEMPERATURE; UBIQUITINATION;

ACETYLATION; ARABIDOPSIS; ARABIDOPSIS PROTEINS; CHROMATIN ASSEMBLY AND DISASSEMBLY; GENE EXPRESSION REGULATION, PLANT; HISTONE-LYSINE N-METHYLTRANSFERASE; HISTONES; HOMEODOMAIN PROTEINS; NUCLEAR PROTEINS; PLANT DORMANCY; SEASONS; TEMPERATURE; TRANSCRIPTION FACTORS; UBIQUITINATION;

EID: 84921616375     PISSN: 09607412     EISSN: 1365313X     Source Type: Journal    
DOI: 10.1111/tpj.12735     Document Type: Article

References (48)

1. Agius, F., Kapoor, A., and, Zhu, J.K., (2006) Role of the Arabidopsis DNA glycosylase/lyase ROS1 in active DNA demethylation. Proc. Natl Acad. Sci. USA, 103, 11796-11801.
2. Baskin, C.C., and, Baskin, J.M., (2006) The natural history of soil seed banks of arable land. Weed Sci. 54, 549-557.
3. Bentsink, L., Jowett, J., Hanhart, C.J., and, Koornneef, M., (2006) Cloning of DOG1, a quantitative trait locus controlling seed dormancy in Arabidopsis. Proc. Natl Acad. Sci. USA, 103, 17042-17047.
4. Berr, A., Shafiq, S., and, Shen, W.H., (2011) Histone modifications in transcriptional activation during plant development. Biochim. Biophys. Acta, 1809, 567-576.
5. Bouyer, D., Roudier, F., Heese, M., et al. (2012) Polycomb repressive complex 2 controls the embryo-to-seedling phase transition. PLoS Genet. 7, e1002014.
6. Cadman, C.S.C., Toorop, P.E., Hilhorst, H.W.M., and, Finch-Savage, W.E., (2006) Gene expression profiles of Arabidopsis Cvi seeds during dormancy cycling indicate a common underlying dormancy control mechanism. Plant J. 46, 805-822.
7. Calonje, M., (2014) PRC1 marks the difference in plant PcG repression. Mol. Plant, 7, 459-471.
8. Cao, Y., Dai, Y., Cui, S.J., and, Ma, L.G., (2008) Histone H2B Monoubiquitination in the chromatin of FLOWERING LOCUS C regulates flowering time in Arabidopsis. Plant Cell, 20, 2586-2602.
9. Chiang, G.C.K., Bartsch, M., Barua, D., Nakabayashi, K., Debieu, M., Kronholm, I., Koornneef, M., Soppe, W.J.J., Donohue, K., and, de Meaux, J., (2011) DOG1 expression is predicted by the seed-maturation environment and contributes to geographical variation in germination in Arabidopsis thaliana. Mol. Ecol. 20, 3336-3349.
10. Chinnusamy, V., and, Zhu, J.K., (2009) Epigenetic regulation of stress responses in plants. Curr. Opin. Plant Biol. 12, 133-139.
11. Colville, A., Alhattab, R., Hu, M., Labbe, H., Xing, T., and, Miki, B., (2011) Role of HD2 genes in seed germination and early seedling growth in Arabidopsis. Plant Cell Rep. 30, 1969-1979.
12. Du, H.N., (2012) Transcription, DNA damage and beyond: the roles of histone ubiquitination and deubiquitination. Curr. Protein Pept. Sci. 13, 447-466.
13. Earley, K.W., Shook, M.S., Brower-Toland, B., Hicks, L., and, Pikaard, C.S., (2007) In vitro specificities of Arabidopsis co-activator histone acetyltransferases: implications for histone hyperacetylation in gene activation. Plant J. 52, 615-626.
14. Engelhorn, J., Blanvillain, R., and, Carles, C.C., (2014) Gene activation and cell fate control in plants: a chromatin perspective. Cell. Mol. Life Sci. 71, 3119-3137.
15. Evans, M.E.K., and, Dennehy, J.J., (2005) Germ banking: bet-hedging and variable release from egg and seed dormancy. Q. Rev. Biol. 80, 431-451.
16. Finch-Savage, W.E., and, Footitt, S., (2012) To germinate or not to germinate: a question of dormancy relief not germination stimulation. Seed Sci. Res. 22, 243-248.
17. Finch-Savage, W.E., and, Leubner-Metzger, G., (2006) Seed dormancy and the control of germination. New Phytol. 171, 501-523.
18. Finch-Savage, W.E., Cadman, C.S.C., Toorop, P.E., Lynn, J.R., and, Hilhorst, H.W.M., (2007) Seed dormancy release in Arabidopsis Cvi by dry after-ripening, low temperature, nitrate and light shows common quantitative patterns of gene expression directed by environmentally specific sensing. Plant J. 51, 60-78.
19. Footitt, S., Douterelo-Soler, I., Clay, H., and, Finch-Savage, W.E., (2011) Dormancy cycling in Arabidopsis seeds is controlled by seasonally distinct hormone-signaling pathways. Proc. Natl Acad. Sci. USA, 108, 20236-20241.
20. Footitt, S., Huang, Z.Y., Clay, H.A., Mead, A., and, Finch-Savage, W.E., (2013) Temperature, light and nitrate sensing coordinate Arabidopsis seed dormancy cycling, resulting in winter and summer annual phenotypes. Plant J. 74, 1003-1015.
21. Footitt, S., Clay, H.A., Dent, K., and, Finch-Savage, W.E., (2014) Environment sensing in spring-dispersed seeds of a winter annual Arabidopsis influences the regulation of dormancy to align germination potential with seasonal changes. New Phytol. 202, 929-939.
22. Furner, I.J., and, Matzke, M., (2011) Methylation and demethylation of the Arabidopsis genome. Curr. Opin. Plant Biol. 14, 137-141.
23. Graeber, K., Nakabayashi, K., Miatton, E., Leubner-Metzger, G., and, Soppe, W.J.J., (2012) Molecular mechanisms of seed dormancy. Plant Cell Environ. 35, 769-1786.
24. Himanen, K., Woloszynska, M., Boccardi, T.M., Groeve, S., Nelissen, H., Bruno, L., Vuylsteke, M., and, Lijsebettens, M., (2012) Histone H2B monoubiquitination is required to reach maximal transcript levels of circadian clock genes in Arabidopsis. Plant J. 72, 249-260.
25. Jackson, J.P., Lindroth, A.M., Cao, X., and, Jacobsen, S.E., (2002) Control of CpNpG DNA methylation by the KRYPTONITE histone H3 methyltransferase. Nature, 416, 556-560.
26. Jackson, J.P., Johnson, L., Jasencakova, Z., Zhang, X., PerezBurgos, L., Singh, P.B., Cheng, X.D., Schubert, I., Jenuwein, T., and, Jacobsen, S.E., (2004) Dimethylation of histone H3 lysine 9 is a critical mark for DNA methylation and gene silencing in Arabidopsis thaliana. Chromosoma, 112, 308-315.
27. Karmodiya, K., Krebs, A.R., Oulad-Abdelghani, M., Kimura, H., and, Tora, L., (2012) H3K9 and H3K14 acetylation co-occur at many gene regulatory elements, while H3K14ac marks a subset of inactive inducible promoters in mouse embryonic stem cells. BMC Genom. 13, 424.
28. Krichevsky, A., Zaltsman, A., Lacroix, B., and, Citovsky, V., (2011) Involvement of KDM1C histone demethylase-OTLD1 otubain-like histone deubiquitinase complexes in plant gene repression. Proc. Natl Acad. Sci. USA, 108, 11157-11162.
29. Kucera, B., Cohn, M.A., and, Leubner-Metzger, G., (2005) Plant hormone interactions during seed dormancy release and germination. Seed Sci. Res. 15, 281-307.
30. Liu, Y., Koornneef, M., and, Soppe, W.J.J., (2007) The absence of histone H2B monoubiquitination in the Arabidopsis hub1 (rdo4) mutant reveals a role for chromatin remodeling in seed dormancy. Plant Cell, 19, 433-444.
31. McEwen, K.R., and, Ferguson-Smith, A.C., (2010) Distinguishing epigenetic marks of developmental and imprinting regulation. Epigenetics Chromatin, 3, 2.
32. Molitor, A.M., Bu, Z., Yu, Y., and, Shen, W.-H., (2014) Arabidopsis AL PHD-PRC1 complexes promote seed germination through H3K4me3-to-H3K27me3 chromatin state switch in repression of seed developmental genes. PLoS Genet. 10, e1004091.
33. Muller, K., Bouyer, D., Schnittger, A., and, Kermode, A.R., (2012) Evolutionarily conserved histone methylation dynamics during seed life-cycle transitions. PLoS One, 7, e51532.
34. Nakabayashi, K., Bartscha, M., Xianga, Y., Miattona, E., Pellengahra, S., Yanob, R., Seob, M., and, Soppe, W.J.J., (2012) The time required for dormancy release in Arabidopsis is determined by DELAY OF GERMINATION1 protein levels in freshly harvested seeds. Plant Cell, 24, 2826-2838.
35. Nambara, E., Okamoto, M., Tatematsu, K., Yano, R., Seo, M., and, Kamiya, Y., (2010) Abscisic acid and the control of seed dormancy and germination. Seed Sci. Res. 20, 55-67.
36. Pons, T.L., (1989) Breaking of seed dormancy by nitrate as a gap detection mechanism. Ann. Bot. 63, 139-143.
37. Roudier, F., Ahmed, I., Berard, C., et al. (2011) Integrative epigenomic mapping defines four main chromatin states in Arabidopsis. EMBO J. 30, 1928-1938.
38. Saatkamp, A., Affre, L., Baumberger, T., Dumas, P.J., Gasmi, A., Gachet, S., and, Arene, F., (2011a) Soil depth detection by seeds and diurnally fluctuating temperatures: different dynamics in 10 annual plants. Plant Soil, 349, 331-340.
39. Saatkamp, A., Affre, L., Dutoit, T., and, Poschlod, P., (2011b) Germination traits explain soil seed persistence across species: the case of Mediterranean annual plants in cereal fields. Ann. Bot. 107, 415-426.
40. Sridhar, V.V., Kapoor, A., Zhang, K.L., Zhu, J.J., Zhou, T., Hasegawa, P.M., Bressan, R.A., and, Zhu, J.K., (2007) Control of DNA methylation and heterochromatic silencing by histone H2B deubiquitination. Nature, 447, 735-738.
41. Sun, Z.W., and, Allis, C.D., (2002) Ubiquitination of histone H2B regulates H3 methylation and gene silencing in yeast. Nature, 418, 104-108.
42. Walck, J.L., Hidayati, S.N., Dixon, K.W., Thompson, K., and, Poschlod, P., (2011) Climate change and plant regeneration from seed. Glob. Change Biol. 17, 2145-2161.
43. Wang, Z., Cao, H., Sun, Y.Z., et al. (2013) Arabidopsis paired amphipathic helix proteins SNL1 and SNL2 redundantly regulate primary seed dormancy via abscisic acid-ethylene antagonism mediated by histone deacetylation. Plant Cell, 25, 149-166.
44. Wright, D.E., Wang, C.Y., and, Kao, C.F., (2011) Flickin' the ubiquitin switch: the role of H2B ubiquitylation in development. Epigenetics, 6, 1165-1175.
45. Yang, C., Bratzel, F., Hohmann, N., Koch, M., Turck, F., and, Calonje, M., (2013) VAL-and AtBMI1-Mediated H2Aub initiate the switch from embryonic to postgerminative growth in Arabidopsis. Curr. Biol. 23, 1324-1329.
46. Yano, A., Kodama, Y., Koike, A., Shinya, T., Kim, H.J., Matsumoto, M., Ogita, S., Wada, Y., Ohad, N., and, Sano, H., (2006) Interaction between methyl CpG-binding protein and Ran GTPase during cell division in tobacco cultured cells. Ann. Bot. 98, 1179-1187.
47. Yano, R., Takebayashi, Y., Nambara, E., Kamiya, Y., and, Seo, M., (2013) Combining association mapping and transcriptomics identify HD2B histone deacetylase as a genetic factor associated with seed dormancy in Arabidopsis thaliana. Plant J. 74, 815-828.
48. Zheng, J., Chen, F.Y., Wang, Z., Cao, H., Li, X.Y., Deng, X., Soppe, W.J.J., Li, Y., and, Liu, Y.X., (2012) A novel role for histone methyltransferase KYP/SUVH4 in the control of Arabidopsis primary seed dormancy. New Phytol. 193, 605-616.