A stochastic model of chromatin modification: Cell population coding of winter memory in plants

Journal of Theoretical Biology

Volumn 302, Issue , 2012, Pages 6-17

  Satake, Akiko ^a,b   Iwasa, Yoh ^c  

^a HOKKAIDO UNIVERSITY   (Japan)

^b JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

^c KYUSHU UNIVERSITY   (Japan)

Author keywords

Bistability; Cell to cell variations; Epigenetics; Flowering; Histone modification

Indexed keywords

BIOLOGICAL ANALYSIS; CELL ORGANELLE; FLOWERING; MEMORY; MODEL TEST; NUMERICAL MODEL; PROTEIN; STOCHASTICITY; TEMPERATURE EFFECT;

ANNUAL PLANT; ARTICLE; CELL DIVISION; CELL POPULATION; CHROMATIN ASSEMBLY AND DISASSEMBLY; COLD TREATMENT; COMPUTER SIMULATION; DNA REPLICATION; EPIGENETICS; FLOWERING LOCUS C GENE; GENE EXPRESSION; GENE REPRESSION; INHERITANCE; MATHEMATICAL ANALYSIS; MEMORY; NUCLEOSOME; PERENNIAL PLANT; PLANT; PLANT GENE; POSITIVE FEEDBACK; PRIORITY JOURNAL; STOCHASTIC MODEL; TRANSIENT EXPRESSION; WINTER MEMORY;

ACCLIMATIZATION; ARABIDOPSIS; ARABIDOPSIS PROTEINS; CHROMATIN; COMPUTER SIMULATION; EPIGENOMICS; FEEDBACK, PHYSIOLOGICAL; FLOWERS; GENE EXPRESSION REGULATION, PLANT; GENES, PLANT; HISTONES; MADS DOMAIN PROTEINS; MODELS, GENETIC; PLANT CELLS; PLANTS; SEASONS; STOCHASTIC PROCESSES; TEMPERATURE;

EID: 84858130419     PISSN: 00225193     EISSN: 10958541     Source Type: Journal    
DOI: 10.1016/j.jtbi.2012.02.009     Document Type: Article

References (45)

1. Aikawa S., Kobayachi M.J., Satake A., Shimizu K.K., Kudoh H. Robust control of the seasonal expression of the Arabidopsis FLC gene in a fluctuating environment. Proc. Natl. Acad. Sci. USA 2010, 107:11632-11637.
2. Angel, A., Song, J., Dean, C., Howard, M., 2011. A polycomb-based switch underlying quantitative epigenetic memory. Nature. doi:10.1038.
3. Barrett R.M., Wood M.A. Beyond transcription factors: the role of chromatin modifying enzymes in regulating transcription required for memory. Learn. Mem. 2008, 15:460-467.
4. Bastow R., Mylne J.S., Lister C., Lippman Z., Martienssen R.A., Dean C. Vernalization requires epigenetic silencing of FLC by histone methylation. Nature 2004, 427:164-167.
5. Burrill D.R., Silver P.A. Making cellular memories. Cell 2010, 140:13-18.
6. Cao R., Wang L., Wang H., Xia L., Erdjument-Bromage H., Tempst P., Jones R.S., Zhang Y. Role of histone H3 lysine 27 methylation in Polycomb-group silencing. Science 2002, 298:1039-1043.
7. De Lucia F., Crevillen P., Jones A.M., Greb T., Dean C. A PHD-polycomb repressive complex 2 triggers the epigenetic silencing of FLC during vernalization. Proc. Natl. Acad. Sci. USA 2008, 105:16831-16836.
8. Dennis E.S., Peacock W.J. Epigenetic regulation of flowering. Curr. Opin. Plant Biol. 2007, 10:520-527.
9. Dodd I.B., Micheelsen M.A., Sneppen K., Thon G. Theoretical analysis of epigenetic cell memory by nucleosome modification. Cell 2007, 129:813-822.
10. Feller W. An Introduction to Probability Theory and its Applications 1968, John Wiley & Sons, New York.
11. Finnegan E.J., Dennis E. Vernalization-induced trimethylation of histone H3 lysine 27 at FLC is not maintained in mitotically quiescent cells. Curr. Biol. 2007, 16:1978-1983.
12. Gardner T., Cantor C.R., Collins J.J. Construction of a genetic toggle switch in Escherichia coli. Nature 2000, 403:339-342.
13. He Y. Control of the transition to flowering by chromatin modifications. Mol. Plant 2009, 2:554-564.
14. Helliwell C.A., Wood C.C., Robertson M., James Peacock W., Dennis E.S. 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. 2006, 46:183-192.
15. Hepworth S.R., Valverde F., Ravenscroft D., Mouradov A., Coupland G. Antagonistic regulation of flowering-time gene SOC1 by CONSTANS and FLC via separate promoter motifs. EMBO J. 2002, 21:4327-4337.
16. Hirose S. Crucial roles for chromatin dynamics in cellular memory. J. Biochem. 2007, 141:615-619.
17. Karlin S., Taylor H.W. A First Course in Stochastic Processes 1975, Academic Press, New York.
18. Kim D.H., Doyle M.R., Sung S., Amasino R.M. Vernalization: winter and the timing of flowering in plants. Annu. Rev. Cell. Div. Biol. 2009, 25:277-299.
19. Kuroda S., Schweighofer N., Kawato M. Exploration of signal transduction pathways in cerebellar long-term depression by kinetic simulation. J. Neurosci. 2001, 21:5693-5702.
20. Lang A. Physiology of flower initiation. Encyclopedia of Plant Physiology 1965, 1380-1536. Springer-Verlag, Berlin. W. Ruhland (Ed.).
21. Lee H., Suh S.S., Park E., Cho E., Ahn J.H., Kim S.G., Lee L.S., Kwon Y.M., Lee L. The AGAMOUS-LIKE 20 MADS domain protein integrates floral inductive pathways in Arabidopsis. Genes Dev. 2000, 14:2366-2376.
22. Levy Y.Y., Mesnage S., Mylne J.S., Gendall A.R., Dean C. Multiple roles of Arabidopsis VRN1 in vernalization and flowering time control. Science 2002, 297:243-246.
23. Lunyak V.V. Epigenetic regulation of stem cell fate. Hum. Mol. Gen. 2008, 17:R28-R36.
24. Michaels S.D., Amasino R.M. FLOWERING LOCUS C encodes a novel MADS domain protein that acts as a repressor of flowering. Plant Cell 1999, 11:949-956.
25. Mylne J.S., Barrett L., Tessadori F., Mesnage S., Johnson L., Bernatavichute Y.V., Jacobsen S.E., Fransz P., Dean C. LHP1, the Arabidopsis homologue of HETEROCHROMATIN PROTEIN1, is required for epigenetic silencing of FLC. Proc. Natl. Acad. Sci. USA 2006, 103:5012-5017.
26. Novak B., Tyson J.J. Numerical analysis of a comprehensive model of M-phase control in Xenopus oocyte extracts and intact embryos. J. Cell Sci. 1993, 106:1153-1168.
27. Ozbudak E.M., Thattai M., Kurtser I., Grossman A.D., van Oudenaarden A. Regulation of noise in the expression of a single gene. Nat. Genet. 2002, 31:69-73.
28. Ramsey S., Ozinsky A., Clark A., Smith K.D., de Atauri P., Thorsson V., Orrell D., Bolouri H. Transcriptional noise and cellular heterogeneity in mammalian macrophages. Philos. Trans. R. Soc. London B-Biol. Sci. 2006, 361:495-506.
29. Satake A. Diversity of plant life cycles is generated by dynamic epigenetic regulation in response to vernalization. J. Theor. Biol. 2010, 266:595-605.
30. Schubert D., Clarenz O., Goodrich J. Epigenetic control of plant development by polycomb-group proteins. Curr. Opin. Plant Biol. 2005, 8:553-561.
31. Searle I., He Y., Turck F., Vincent C., Fornara F., et al. The transcription factor FLC confers a flowering response to vernalization by repressing meristem competence and systemic signaling in Arabidopsis. Genes Dev. 2006, 20:898-912.
32. Sheldon C.C., Burn J.E., Perez P.P., Metzger J., Edwards J.A., Peacock W.J., Dennis E.S. The FLF MADS box gene: a repressor of flowering in Arabidopsis regulated by vernalization and methylation. Plant Cell 1999, 11:445-458.
33. Sheldon C.C., Hills M.J., Lister C., Dean C., Dennis E.S., Peacock W.J. Resetting of FLOWERING LOCUS C expression after epigenetic repression by vernalization. Proc. Natl. Acad. Sci. USA 2008, 105:2214-2219.
34. Sheldon C.C., Rouse D.T., Finnegan E.J., Peacock W.J., Dennis E.S. The molecular basis of vernalization: the central role of FLOWERING LOCUS C (FLC). Proc. Natl. Acad. Sci. USA 2000, 97:3753-3758.
35. Shindo C., Lister C., Crevilenn P., Nordborg M., Dean C. Variation in the epigenetic silencing of FLC contributes to natural variation in Arabidopsis vernalization response. Gene Dev. 2006, 20:3079-3083.
36. Sung S., Amasino R.M. Vernalization in Arabidopsis thaliana is mediated by the PHD finger protein VIN3. Nature 2004, 427:159-164.
37. Sung S., Amasino R.M. Remembering winter: towards a molecular understanding of Vernalization. Annu. Rev. Plant Biol. 2005, 56:491-508.
38. Swain P.S., Elowitz M.B., Siggia E.D. Intrinsic and extrinsic contributions to stochasticity in gene expression. Proc. Natl. Acad. Sci. USA 2002, 99:12795-12800.
39. Tanaka K., Augustine G.J. A positive feedback signal transduction loop determines timing of cerebellar long-term depression. Neuron 2008, 59:608-620.
40. Turck F., Roudier F., Farrona S., Martin-Magniette M.L., Guillaume E., Buisine N., Gagnot S., Martienssen R.A., Coupland G., Colot V. Arabidopsis TFL2/LHP1 specifically associates with genes marked by trimethylation of histone H3 Lysine 27. PLos Genet. 2007, 3:e86.
41. Turner B.M. Cellular memory and the histone code. Cell 2002, 111:285-291.
42. Wang R., Farrona S., Vincent C., Joecker A., Schoof H., Turck F., Alonso-Blanco C., Coupland G., Albani M.C. PEP1 regulates perennial flowering in Arabis alpina. Nature 2009, 459:423-427.
43. Wood C.C., Robertson M., Tanner G., Peacock W.J., Dennis E.S., Helliwell C.A. The Arabidopsis thaliana vernalization response requires a polycomb-like protein complex that also includes VERNALIZATION INSENSITIVE 3. Proc. Natl. Acad. Sci. USA 2006, 103:14631-14636.
44. Xiong W., Ferrell J.E. A positive-feedback-based bistable "memory module" that governs a cell fate decision. Nature 2003, 428:460-465.
45. Zhang X., Germann S., Blus B.J., Khorasanizadeh S., Gaudin V., Jacobsen S.E. The Arabidopsis LHP1 protein colocalizes with histone H3 Lys27 trimethylation. Nat. Struct. Mol. Biol. 2007, 14:869-871.