Remembering winter: Toward a molecular understanding of vernalization

Annual Review of Plant Biology

Volumn 56, Issue , 2005, Pages 491-508

  Sung, Sibum ^a   Amasino, Richard M ^a  

^a UNIVERSITY OF WISCONSIN MADISON   (United States)

Author keywords

Cold acclimation; Epigenetics; Flowering; Histone modifications; Polycomb mediated gene repression

Indexed keywords

HISTONE; POLYCOMB PROTEIN, PLANT; REPRESSOR PROTEIN;

ADAPTATION; COLD; GENE EXPRESSION REGULATION; GENETICS; PHYSIOLOGY; PLANT; PLANT PHYSIOLOGY; REVIEW; SEASON;

ADAPTATION, PHYSIOLOGICAL; COLD; GENE EXPRESSION REGULATION, PLANT; HISTONES; PLANT PHYSIOLOGY; PLANTS; REPRESSOR PROTEINS; SEASONS;

ARABIDOPSIS;

EID: 20444363811     PISSN: 15435008     EISSN: None     Source Type: Book Series    
DOI: 10.1146/annurev.arplant.56.032604.144307     Document Type: Review

References (114)

1. Aasland R, Gibson TJ, Stewart AF. 1995. The PHD finger: implications for chromatin-mediated transcriptional regulation. Trends Biochem. Sci. 20:56-59
2. Abegg FA. 1936. A genetic factor for the annual habit in beets and linkage relationship. J. Argicultural Res. 53:493-511
3. Anderson BE, Ward JM, Schroeder JI. 1994. Evidence for an extracellular reception site for abscisic acid in commelina guard cells. Plant Physiol. 104:1177-83
4. Ausin I, Alonso-Blanco C, Jarillo JA, Ruiz-Garcia L, Martinez-Zapater JM. 2004. Regulation of flowering time by FVE, a retinoblastoma-associated protein. Nat. Genet. 36:162-66
5. Bannister AJ, Zegerman P, Partridge JF, Miska EA, Thomas JO, et al. 2001. Selective recognition of methylated lysine 9 on histone H3 by the HP1 chromo domain. Nature 410:120-24
6. Bastow R, Mylne JS, Lister C, Lippman Z, Martienssen RA, Dean C. 2004. Vernalization requires epigenetic silencing of FLC by histone methylation. Nature 427:164-67
7. Beisel C, Imhof A, Greene J, Kremmer E, Sauer F. 2002. Histone methylation by the Drosophila epigenetic transcriptional regulator Ash1. Nature 419:857-62
8. Berger SL. 2002. Histone modifications in transcriptional regulation. Curr. Opin. Genet. Dev. 12:142-48
9. Bernier G, Kinet J-M, Sachs RM. 1981. The Physiology of Flowering. Boca Raton, FL: CRC Press
10. Breiling A, Bonte E, Ferrari S, Becker PB, Paro R. 1999. The Drosophila polycomb protein interacts with nucleosomal core particles in vitro via its repression domain. Mol. Cell. Biol. 19:8451-60
11. Burn JE, Bagnall DJ, Metzger JD, Dennis ES, Peacock WJ. 1993. DNA methylation, vernalization, and the initiation of flowering. Proc. Natl. Acad. Sci. USA 90:287-91
12. Burn JE, Smyth DR, Peacock WJ, Dennis ES. 1993. Genes conferring late flowering in Arabidopsis thaliana. Genetica 90:147-55
13. Cao R, Wang L, Wang H, Xia L, Erdjument-Bromage H, et al. 2002. Role of histone H3 lysine 27 methylation in Polycomb-group silencing. Science 298:1039-43
14. Chinnusamy V, Ohta M, Kanrar S, Lee BH, Hong X, et al. 2003. ICE1: a regulator of cold-induced transcriptome and freezing tolerance in Arabidopsis. Genes Dev. 17:1043-54
15. Chouard P. 1960. Vernalization and its relations to dormancy. Annu. Rev. Plant Physiol. 11:191-238
16. Clarke JH, Dean C. 1994. Mapping FRI, a locus controlling flowering time and vernalization response in Arabidopsis thaliana. Mol. Gen. Genet. 242:81-89
17. Czermin B, Melfi R, McCabe D, Seitz V, Imhof A, Pirrotta V. 2002. Drosophila enhancer of Zeste/ESC complexes have a histone H3 methyltransferase activity that marks chromosomal Polycomb sites. Cell 111:185-96
18. Dubcovsky J, Luo MC, Zhong GY, Bransteitter R, Desai A, et al. 1996. Genetic map of diploid wheat, Triticum monococcum L., and its comparison with maps of Hordeum vulgare L. Genetics 143:983-99
19. Dutnall RN. 2003. Cracking the histone code: one, two, three methyls, you're out! Mol. Cell. 12:3-4
20. Erwin JE, Warner RM, Smith AG. 2002. Vernalization, photoperiod and GA3 interact to affect flowering of Japanese radish (Raphanus sativus Chinese Radish Jumbo Scarlet). Physiol. Plant 115:298-302
21. Fischle W, Wang Y, Jacobs SA, Kim Y, Allis CD, Khorasanizadeh S. 2003. Molecular basis for the discrimination of repressive methyl-lysine marks in histone H3 by Polycomb and HP1 chromodomains. Genes Dev. 17:1870-81
22. Francis NJ, Saurin AJ, Shao Z, Kingston RE. 2001. Reconstitution of a functional core polycomb repressive complex. Mol. Cell. 8:545-56
23. Gazzani S, Gendall AR, Lister C, Dean C. 2003. Analysis of the molecular basis of flowering time variation in Arabidopsis accessions. Plant Physiol. 132:1107-14
24. Gendall AR, Levy YY, Wilson A, Dean C. 2001. The VERNALIZATION 2 gene mediates the epigenetic regulation of vernalization in Arabidopsis. Cell 107:525-35
25. Gilmour S, Hajela RK, Thomashow MF. 1988. Cold acclimation in Arabidopsis thaliana. Plant Physiol. 87:745-50
26. Gilmour SJ, Zarka DG, Stockinger EJ, Salazar MP, Houghton JM, Thomashow MF. 1998. Low temperature regulation of the Arabidopsis CBF family of AP2 transcriptional activators as an early step in cold-induced COR gene expression. Plant J. 16:433-42
27. Gould A. 1997. Functions of mammalian Polycomb group and trithorax group related genes. Curr. Opin. Genet. Dev. 7:488-94
28. Gozani O, Karuman P, Jones DR, Ivanov D, Cha J, et al. 2003. The PHD finger of the chromatin-associated protein ING2 functions as a nuclear phosphoinositide receptor. Cell 114:99-111
29. Guy CL, Niemi KJ, Brambl R. 1985. Altered gene expression during cold acclimation of spinach. Proc. Natl. Acad. Sci. USA 82:3673-77
30. He Y, Doyle MD, Amasino RM. 2004. PAF1 complex-mediated histone methylation of FLOWERING LOCUS C chromatin is required for the vernalization-responsive, winter-annual habit in Arabidopsis. Genes Dev. 18:2774-84
31. He Y, Michaels SD, Amasino RM. 2003. Regulation of flowering time by histone acetylation in Arabidopsis. Science 302:1751-54
32. Hong BM, Barg R, Ho THD. 1992. Developmental and organ-specific expression of an ABA-induced and stress-induced protein in barley. Plant Mol. Biol. 18:663-74
33. Houde M, Danyluk J, Laliberte JF, Rassart E, Dhindsa RS, Sarhan F. 1992. Cloning, characterization, and expression of a carrier DNA encoding a 50-kilodalton protein specifically induced by cold acclimation in wheat. Plant Physiol. 99:1381-87
34. Hsieh TF, Hakim O, Ohad N, Fischer RL. 2003. From flour to flower: how Polycomb group proteins influence multiple aspects of plant development. Trends Plant Sci. 8:439-45
35. Ichimura K, Mizoguchi T, Yoshida R, Yuasa T, Shinozaki K. 2000. Various abiotic stresses rapidly activate Arabidopsis MAP kinases ATMPK4 and ATMPK6. Plant J. 24:655-65
36. Iizuka M, Smith MM. 2003. Functional consequences of histone modifications. Curr. Opin. Genet. Dev. 13:154-60
37. Ishitani M, Xiong L, Lee H, Stevenson B, Zhu JK. 1998. HOS1, a genetic locus involved in cold-responsive gene expression in arabidopsis. Plant Cell 10:1151-61
38. Jacobs SA, Khorasanizadeh S. 2002. Structure of HP1 chromodomain bound to a lysine 9-methylated histone H3 tail. Science 295:2080-83
39. Jaglo-Ottosen KR, Gilmour SJ, Zarka DG, Schabenberger O, Thomashow MF. 1998. Arabidopsis CBF1 overexpression induces COR genes and enhances freezing tolerance. Science 280:104-6
40. Jenuwein T, Allis CD. 2001. Translating the histone code. Science 293:1074-80
41. Johanson U, West J, Lister C, Michaels S, Amasino R, Dean C. 2000. Molecular analysis of FRIGIDA, a major determinant of natural variation in Arabidopsis flowering time. Science 290:344-47
42. Jonak C, Kiegerl S, Ligterink W, Barker PJ, Huskisson NS, Hirt H. 1996. Stress signaling in plants: a mitogen-activated protein kinase pathway is activated by cold and drought. Proc. Natl. Acad. Sci. USA 93:11274-79
43. Kim YJ. 1998. Studies on vernlization treatment of winter barley in the 17th century that are described in Ko's "Monthly Farming Guide." Proc. Korean Soc. Cereal Res. 5:117-25
44. Knight MR, Campbell AK, Smith SM, Trewavas AJ. 1991. Transgenic plant aequorin reports the effects of touch and cold-shock and elicitors on cytoplasmic calcium. Nature 352:524-26
45. Kobor MS, Venkatasubrahmanyam S, Meneghini MD, Gin JW, Jennings JL, et al. 2004. A protein complex containing the conserved Swi2/Snf2-related ATPase Swrlp deposits histone variant H2A.Z into euchromatin. PLoS Biol. 2:587-99
46. Koornneef M, Alonso-Blanco C, Peeters AJ, Soppe W. 1998. Genetic control of flowering time in Arabidopsis. Ann. Rev. Plant Physiol. Plant Mol. Biol. 49:345-70
47. Koornneef M, Blankestijn-de Vries H, Hanhart C, Soppe W, Peeters T. 1994. The phenotype of some late-flowering mutants is enhanced by a locus on chromosome 5 that is not effective in the Landsberg erecta wild-type. Plant J. 6:911-19
48. Kouzarides T. 2002. Histone methylation in transcriptional control. Curr. Opin. Genet. Dev. 12:198-209
49. Kovtun Y, Chiu WL, Tena G, Sheen J. 2000. Functional analysis of oxidative stress-activated mitogen-activated protein kinase cascade in plants. Proc. Natl. Acad. Sci. USA 97:2940-45
50. Krishna P, Sacco M, Cherutti JF, Hill S. 1995. Cold-induced accumulation of hsp90 transcripts in Brassica napus. Plant Physiol. 107:915-23
51. Krogan NJ, Dover J, Wood A, Schneider J, Heidt J, et al. 2003. The Paf1 complex is required for histone H3 methylation by COMPASS and Dot1p: linking transcriptional elongation to histone methylation. Mol. Cell. 11:721-29
52. Kuzmichev A, Nishioka K, Erdjument-Bromage H, Tempst P, Reinberg D. 2002. Histone methyltransferase activity associated with a human multiprotein complex containing the enhancer of Zeste protein. Genes Dev. 16:2893-905
53. Lachner M, O'Carroll D, Rea S, Mechtler K, Jenuwein T. 2001. Methylation of histone H3 lysine 9 creates a binding site for HP1 proteins. Nature 410:116-20
54. Lang A. 1965. Physiology of flower initiation. In Encyclopedia of Plant Physiology, ed. W Ruhland, pp. 1371-536. Berlin: Springer-Verlag
55. Lang A. 1986. Hyoscyamus niger. In CRC Handbook of Flowering, ed. AH Halevy, pp. 144-86. Boca Raton, FL: CRC Press
56. Laurie DA. 1997. Comparative genetics of flowering time. Plant Mol. Biol. 35:167-77
57. Lee H, Xiong L, Gong Z, Ishitani M, Stevenson B, Zhu JK. 2001. The Arabidopsis HOS1 gene negatively regulates cold signal transduction and encodes a RING finger protein that displays cold-regulated nucleo-cytoplasmic partitioning. Genes Dev. 15:912-24
58. Lee I, Amasino RM. 1995. Effect of vernalization, photoperiod and light quality on the flowering phenotype of Arabidopsis plants containing the FRIGIDA gene. Plant Physiol. 108:157-62
59. Lee I, Bleecker A, Amasino R. 1993. Analysis of naturally occurring late flowering in Arabidopsis thaliana. Mol. Gen. Genet. 237:171-76
60. Lee I, Michaels SD, Masshardt AS, Amasino RM. 1994. The late-flowering phenotype of FRIGIDA and LUMINIDEPENDENS is suppressed in the Landsberg erecta strain of Arabidopsis. Plant J. 6:903-9
61. Levy YY, Mesnage S, Mylne JS, Gendall AR, Dean C. 2002. Multiple roles of Arabidopsis VRN1 in vernalization and flowering time control. Science 297:243-46
62. Li Y, Kirschmann DA, Wallrath LL. 2002. Does heterochromatin protein 1 always follow code? Proc. Natl. Acad. Sci. USA 99(Suppl.)4:16462-69
63. Lin CT, Thomashow MF. 1992. A cold-regulated Arabidopsis gene encodes a polypeptide having potent cryoprotective activity. Biochem. Biophys. Res. Commun. 183:1103-8
64. Liu J, Gilmour SJ, Thomashow MF, Van Nocker S. 2002. Cold signalling associated with vernalization in Arabidopsis thaliana does not involve CBF1 or abscisic acid. Physiol. Plant 114:125-34
65. Liu J, He Y, Amasino RM, Chen X. 2004. siRNA targeting an intronic transposon in the regulation of natural flowering behavior in Arabidopsis. Genes Dev. 18:2873-78
66. McClintock B. 1950. The origin and behavior of mutable loci in Maize. Proc. Natl. Acad. Sci. USA 36:344-55
67. Medina J, Bargues M, Terol J, Perez-Alonso M, Salinas J. 1999. The Arabidopsis CBF gene family is composed of three genes encoding AP2 domain-containing proteins whose expression is regulated by low temperature but not by abscisic acid or dehydration. Plant Physiol. 119:463-70
68. Michaels S, Amasino R. 2000. Memories of winter: vernalization and the competence to flower. Plant Cell Environ. 23:1145-54
69. Michaels SD, Amasino RM. 1999. FLOWERING LOCUS C encodes a novel MADS domain protein that acts as a repressor of flowering. Plant Cell 11:949-56
70. Michaels SD, Amasino RM. 2001. Loss of FLOWERING LOCUS C activity eliminates the late-flowering phenotype of FRIGIDA and autonomous pathway mutations but not responsiveness to vernalization. Plant Cell 13:935-41
71. Michaels SD, He Y, Scortecci KC, Amasino RM. 2003. Attenuation of FLOWERING LOCUS C activity as a mechanism for the evolution of summer-annual flowering behavior in Arabidopsis. Proc. Natl. Acad. Sci. USA 100:10102-7
72. Mizoguchi T, Irie K, Hirayama T, Hayashida N, Yamaguchi-Shinozaki K, et al. 1996. A gene encoding a mitogen-activated protein kinase kinase kinase is induced simultaneously with genes for a mitogen-activated protein kinase and an S6 ribosomal protein kinase by touch, cold, and water stress in Arabidopsis thaliana. Proc. Natl. Acad. Sci. USA 93:765-69
73. Mizuguchi G, Shen X, Landry J, Wu WH, Sen S, Wu C. 2004. ATP-driven exchange of histone H2AZ variant catalyzed by SWR1 chromatin remodeling complex. Science 303:343-48
74. Monroy AF, Castonguay Y, Laberge S, Sarhan F, Vezina LP, Dhindsa RS. 1993. A new cold-induced alfalfa gene is associated with enhanced hardening at subzero temperature. Plant Physiol. 102:873-79
75. Muller J, Hart CM, Francis NJ, Vargas ML, Sengupta A, et al. 2002. Histone methyltransferase activity of a Drosophila Polycomb group repressor complex. Cell 111:197-208
76. Murfet IC. 1989. Flowering genes in Pisum. In Plant Reproduction: From Floral Induction to Pollination, ed. E Lord, G Bernier, pp. 10-18. Rockville, MD: Am. Soc. Plant Physiol.
77. Murtas G, Reeves PH, Fu YF, Bancroft I, Dean C, Coupland G. 2003. A nuclear protease required for flowering-time regulation in Arabidopsis reduces the abundance of SMALL UBIQUITIN-RELATED MODIFIER conjugates. Plant Cell 15:2308-19
78. Napp-Zinn K. 1987. Vernalization: environmental and genetic regulation. In Manipulation of Flowering, ed. JG Atherton, pp. 123-32. London: Butterworths
79. Ng HH, Robert F, Young RA, Strahl K. 2003. Targeted recruitment of Set1 histone methylase by elongating Pol II provides a localized mark and memory of recent transcriptional activity. Mol. Cell. 11:709-19
80. Noh YS, Amasino RM. 2003. PIE1, an ISWI family gene, is required for FLC activation and floral repression in Arabidopsis. Plant Cell 15:1671-82
81. Orlando V. 2003. Polycomb, epigenomes, and control of cell identity. Cell 112:599-606
82. Orvar BL, Sangwan V, Omann F, Dhindsa RS. 2000. Early steps in cold sensing by plant cells: the role of actin cytoskeleton and membrane fluidity. Plant J. 23:785-94
83. Osborn TC, Kole C, Parkin IAP, Sharpe AG, Kuiper M, et al. 1997. Comparison of flowering time genes in Brassica rapa, B. napus and Arabidopsis thaliana. Genet. Soc. Am. 146:1123-29
84. Pirrotta V. 1997. PcG complexes and chromatin silencing. Curr. Opin. Genet. Dev. 7:249-58
85. Plieth C, Hansen UP, Knight H, Knight MR. 1999. Temperature sensing by plants: the primary characteristics of signal perception and calcium response. Plant J. 18:491-97
86. Poux S, Horard B, Sigrist CJ, Pirrotta V. 2002. The Drosophila trithorax protein is a coactivator required to prevent re-establishment of polycomb silencing. Development 129:2483-93
87. Ratcliffe OJ, Kumimoto RW, Wong BJ, Riechmann JL. 2003. Analysis of the Arabidopsis MADS AFFECTING FLOWERING gene family: MAF2 prevents vernalization by short periods of cold. Plant Cell 15:1159-69
88. Ratcliffe OJ, Nadzan GC, Reuber TL, Riechmann JL. 2001. Regulation of flowering in Arabidopsis by an FLC homologue. Plant Physiol. 126:122-32
89. Reeves PH, Murtas G, Dash S, Coupland G. 2002. Early in short days 4, a mutation in Arabidopsis that causes early flowering and reduces the mRNA abundance of the floral repressor FLC. Development 129:5349-61
90. Reid JB, Murfet IC. 1975. Flowering in Pisum: the sites and possible mechanisms of the vernalization response. J. Exp. Bot. 26:860-67
91. Sangwan V, Orvar BL, Beyerly J, Hirt H, Dhindsa RS. 2002. Opposite changes in membrane fluidity mimic cold and heat stress activation of distinct plant MAP kinase pathways. Plant J. 31:629-38
92. Santos-Rosa H, Schneider R, Bannister AJ, Sherriff J, Bernstein BE, et al. 2002. Active genes are tri-methylated at K4 of histone H3. Nature 419:407-11
93. Santos-Rosa H, Schneider R, Bernstein BE, Karabetsou N, Morillon A, et al. 2003. Methylation of histone H3 K4 mediates association of the Iswlp ATPase with chromatin. Mol. Cell. 12:1325-32
94. Schotta G, Ebert A, Krauss V, Fischer A, Hoffmann J, et al. 2002. Central role of Drosophila SU(VAR)3-9 in histone H3-K9 methylation and heterochromatic gene silencing. EMBO J. 21:1121-31
95. Schranz ME, Quijada P, Sung SB, Lukens L, Amasino R, Osborn TC. 2002. Characterization and effects of the replicated flowering time gene FLC in Brassica rapa. Genetics 162:1457-68
96. Schreiber SL, Bernstein BE. 2002. Signaling network model of chromatin. Cell 111:771-78
97. Scortecci KC, Michaels SD, Amasino RM. 2001. Identification of a MADS-box gene, FLOWERING LOCUS M, that represses flowering. Plant J. 26:229-36
98. Sheldon CC, Burn JE, Perez PP, Metzger J, Edwards JA, et al. 1999. The FLF MADS box gene: a repressor of flowering in arabidopsis regulated by vernalization and methylation. Plant Cell 11:445-58
99. Sheldon CC, Rouse DT, Finnegan EJ, Peacock WJ, Dennis ES. 2000. The molecular basis of vernalization: the central role of FLOWERING LOCUS C (FLC). Proc. Natl. Acad. Sci. USA 97:3753-58
100. Simon JA, Tamkun JW. 2002. Programming off and on states in chromatin: mechanisms of Polycomb and trithorax group complexes. Curr. Opin. Genet. Dev. 12:210-18
101. Soppe WJ, Bentsink L, Koornneef M. 1999. The early-flowering mutant efs is involved in the autonomous promotion pathway of Arabidopsis thaliana. Development 126:4763-70
102. Sung S, Amasino RM. 2004. Vernalization and epigenetics: how plants remember winter. Curr. Opin. Plant Biol. 7:4-10
103. Sung S, Amasino RM. 2004. Vernalization in Arabidopsis thaliana is mediated by the PHD finger protein VIN3. Nature 427:159-64
104. Thomashow MF. 1999. PLANT COLD ACCLIMATION: freezing tolerance genes and regulatory mechanisms. Annu. Rev. Plant Physiol. Plant Mol. Biol. 50:571-99
105. Thomashow MF. 2001. So what's new in the field of plant cold acclimation? Lots! Plant Physiol. 125:89-93
106. Tranquilli G, Dubcovsky J. 2000. Epistatic interaction between vernalization genes Vrn-Am1 and Vrn-Am2 in diploid wheat. J. Hered. 91:304-6
107. Turner BM. 2002. Cellular memory and the histone code. Cell 111:285-91
108. Vigh L, Los DA, Horvath I, Murata N. 1993. The primary signal in the biological perception of temperature: Pd-catalyzed hydrogenation of membrane lipids stimulated the expression of the desA gene in Synechocystis PCC6803. Proc. Natl. Acad. Sci. USA 90:9090-94
109. Wang L, Brown JL, Cao R, Zhang Y, Kassis JA, Jones RS. 2004. Hierarchical recruitment of polycomb group silencing complexes. Mol. Cell. 14:637-46
110. Wellensiek SJ. 1962. Dividing cells as the locus for vernalization. Nature 195:307-8
111. Wellensiek SJ. 1964. Dividing cells as the prerequisite for vernalization. Plant Physiol. 39:832-35
112. Yamamoto K, Sonoda M, Inokuchi J, Shirasawa S, Sasazuki T. 2004. Polycomb group suppressor of zeste 12 links heterochromatin protein 1alpha and enhancer of zeste 2. J. Biol. Chem. 279:401-6
113. Yan L, Loukoianov A, Blechl A, Tranquilli G, Ramakrishna W, et al. 2004. The wheat VRN2 gene is a flowering repressor down-regulated by vernalization. Science 303:1640-44
114. Yan L, Loukoianov A, Tranquilli G, Helguera M, Fahima T, Dubcovsky J. 2003. Positional cloning of the wheat vernalization gene VRN1. Proc. Natl. Acad. Sci. USA 100:6263-68