Remembering winter: toward a molecular understanding of vernalization.

Exposure to the prolonged cold of winter is an important environmental cue that favors flowering in the spring in many types of plants. The process by which exposure to cold promotes flowering is known as vernalization. In Arabidopsis and certain cereals, the block to flowering in plants that have not been vernalized is due to the expression of flowering repressors. The promotion of flowering is due to the cold-mediated suppression of these repressors. Recent work has demonstrated that covalent modifications of histones in the chromatin of target loci are part of the molecular mechanism by which certain repressors are silenced during vernalization.

[1]  W. Peacock,et al.  Genes conferring late flowering inArabidopsis thaliana , 1993, Genetica.

[2]  R. Amasino,et al.  siRNAs targeting an intronic transposon in the regulation of natural flowering behavior in Arabidopsis. , 2004, Genes & development.

[3]  R. Amasino,et al.  PAF1-complex-mediated histone methylation of FLOWERING LOCUS C chromatin is required for the vernalization-responsive, winter-annual habit in Arabidopsis. , 2004, Genes & development.

[4]  Yi Zhang,et al.  Hierarchical recruitment of polycomb group silencing complexes. , 2004, Molecular cell.

[5]  Andrew J Link,et al.  A Protein Complex Containing the Conserved Swi2/Snf2-Related ATPase Swr1p Deposits Histone Variant H2A.Z into Euchromatin , 2004, PLoS biology.

[6]  R. Amasino,et al.  Vernalization and epigenetics: how plants remember winter. , 2004, Current opinion in plant biology.

[7]  J. A. Jarillo,et al.  Regulation of flowering time by FVE, a retinoblastoma-associated protein , 2004, Nature Genetics.

[8]  Wei-Hua Wu,et al.  ATP-Driven Exchange of Histone H2AZ Variant Catalyzed by SWR1 Chromatin Remodeling Complex , 2004, Science.

[9]  R. Martienssen,et al.  Vernalization requires epigenetic silencing of FLC by histone methylation , 2004, Nature.

[10]  R. Amasino,et al.  Vernalization in Arabidopsis thaliana is mediated by the PHD finger protein VIN3 , 2004, Nature.

[11]  S. Shirasawa,et al.  Polycomb Group Suppressor of Zeste 12 Links Heterochromatin Protein 1α and Enhancer of Zeste 2* , 2004, Journal of Biological Chemistry.

[12]  D. Laurie.  Comparative genetics of flowering time , 1997, Plant Molecular Biology.

[13]  R. Amasino,et al.  Analysis of naturally occurring late flowering in Arabidopsis thaliana , 1993, Molecular and General Genetics MGG.

[14]  R. Barg,et al.  Developmental and organ-specific expression of an ABA- and stress-induced protein in barley , 1992, Plant Molecular Biology.

[15]  R. Shapley,et al.  The Wheat VRN2 Gene Is a Flowering Repressor Down-Regulated by Vernalization , 2004 .

[16]  C. Dean,et al.  Mapping FRI, a locus controlling flowering time and vernalization response in Arabidopsis thaliana , 2004, Molecular and General Genetics MGG.

[17]  R. Amasino,et al.  Regulation of Flowering Time by Histone Acetylation in Arabidopsis , 2003, Science.

[18]  Stuart L Schreiber,et al.  Methylation of histone H3 K4 mediates association of the Isw1p ATPase with chromatin. , 2003, Molecular cell.

[19]  C. Dean,et al.  A Nuclear Protease Required for Flowering-Time Regulation in Arabidopsis Reduces the Abundance of SMALL UBIQUITIN-RELATED MODIFIER Conjugates Article, publication date, and citation information can be found at www.plantcell.org/cgi/doi/10.1105/tpc.015487. , 2003, The Plant Cell Online.

[20]  N. Ohad,et al.  From flour to flower: how Polycomb group proteins influence multiple aspects of plant development. , 2003, Trends in plant science.

[21]  R. Amasino,et al.  Attenuation of FLOWERING LOCUS C activity as a mechanism for the evolution of summer-annual flowering behavior in Arabidopsis , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[22]  Youngchang Kim,et al.  Molecular basis for the discrimination of repressive methyl-lysine marks in histone H3 by Polycomb and HP1 chromodomains. , 2003, Genes & development.

[23]  Junying Yuan,et al.  The PHD Finger of the Chromatin-Associated Protein ING2 Functions as a Nuclear Phosphoinositide Receptor , 2003, Cell.

[24]  R. Dutnall.  Cracking the histone code: one, two, three methyls, you're out! , 2003, Molecular cell.

[25]  R. Amasino,et al.  PIE1, an ISWI Family Gene, Is Required for FLC Activation and Floral Repression in Arabidopsis Article, publication date, and citation information can be found at www.plantcell.org/cgi/doi/10.1105/tpc.012161. , 2003, The Plant Cell Online.

[26]  C. Lister,et al.  Analysis of the Molecular Basis of Flowering Time Variation in Arabidopsis Accessions1[w] , 2003, Plant Physiology.

[27]  L. Yan,et al.  Positional cloning of the wheat vernalization gene VRN1 , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[28]  J. Riechmann,et al.  Analysis of the Arabidopsis MADS AFFECTING FLOWERING Gene Family: MAF2 Prevents Vernalization by Short Periods of Cold Article, publication date, and citation information can be found at www.plantcell.org/cgi/doi/10.1105/tpc.009506. Online version contains Web-only data. , 2003, The Plant Cell Online.

[29]  Jian-Kang Zhu,et al.  ICE1: a regulator of cold-induced transcriptome and freezing tolerance in Arabidopsis. , 2003, Genes & development.

[30]  Masayoshi Iizuka,et al.  Functional consequences of histone modifications. , 2003, Current opinion in genetics & development.

[31]  V. Orlando.  Polycomb, Epigenomes, and Control of Cell Identity , 2003, Cell.

[32]  M. Johnston,et al.  The Paf1 complex is required for histone H3 methylation by COMPASS and Dot1p: linking transcriptional elongation to histone methylation. , 2003, Molecular cell.

[33]  Kevin Struhl,et al.  Targeted recruitment of Set1 histone methylase by elongating Pol II provides a localized mark and memory of recent transcriptional activity. , 2003, Molecular cell.

[34]  S. Schreiber,et al.  Signaling Network Model of Chromatin , 2002, Cell.

[35]  D. Kirschmann,et al.  Does heterochromatin protein 1 always follow code? , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[36]  G. Coupland,et al.  early in short days 4, a mutation in Arabidopsis that causes early flowering and reduces the mRNA abundance of the floral repressor FLC , 2002, Development.

[37]  D. Reinberg,et al.  Histone methyltransferase activity associated with a human multiprotein complex containing the Enhancer of Zeste protein. , 2002, Genes & development.

[38]  R. Amasino,et al.  Characterization and effects of the replicated flowering time gene FLC in Brassica rapa. , 2002, Genetics.

[39]  B. Turner,et al.  Cellular Memory and the Histone Code , 2002, Cell.

[40]  Christian Beisel,et al.  Histone methylation by the Drosophila epigenetic transcriptional regulator Ash1 , 2002, Nature.

[41]  V. Pirrotta,et al.  Drosophila Enhancer of Zeste/ESC Complexes Have a Histone H3 Methyltransferase Activity that Marks Chromosomal Polycomb Sites , 2002, Cell.

[42]  Brigitte Wild,et al.  Histone Methyltransferase Activity of a Drosophila Polycomb Group Repressor Complex , 2002, Cell.

[43]  Stuart L. Schreiber,et al.  Active genes are tri-methylated at K4 of histone H3 , 2002, Nature.

[44]  Hengbin Wang,et al.  Role of Histone H3 Lysine 27 Methylation in Polycomb-Group Silencing , 2002, Science.

[45]  H. Hirt,et al.  Opposite changes in membrane fluidity mimic cold and heat stress activation of distinct plant MAP kinase pathways. , 2002, The Plant journal : for cell and molecular biology.

[46]  Caroline Dean,et al.  Multiple Roles of Arabidopsis VRN1 in Vernalization and Flowering Time Control , 2002, Science.

[47]  Alan G. Smith,et al.  Vernalization, photoperiod and GA3 interact to affect flowering of Japanese radish (Raphanus sativus Chinese Radish Jumbo Scarlet). , 2002, Physiologia plantarum.

[48]  S. Poux,et al.  The Drosophila trithorax protein is a coactivator required to prevent re-establishment of polycomb silencing. , 2002, Development.

[49]  J. Simon,et al.  Programming off and on states in chromatin: mechanisms of Polycomb and trithorax group complexes. , 2002, Current opinion in genetics & development.

[50]  T. Kouzarides.  Histone methylation in transcriptional control. , 2002, Current opinion in genetics & development.

[51]  S. Berger,et al.  Histone modifications in transcriptional regulation. , 2002, Current opinion in genetics & development.

[52]  Stephen Rea,et al.  Central role of Drosophila SU(VAR)3–9 in histone H3‐K9 methylation and heterochromatic gene silencing , 2002, The EMBO journal.

[53]  S. Jacobs,et al.  Structure of HP1 Chromodomain Bound to a Lysine 9-Methylated Histone H3 Tail , 2002, Science.

[54]  S. J. Gilmour,et al.  Cold signalling associated with vernalization in Arabidopsis thaliana does not involve CBF1 or abscisic acid. , 2002, Physiologia plantarum.

[55]  Allison K. Wilson,et al.  The VERNALIZATION 2 Gene Mediates the Epigenetic Regulation of Vernalization in Arabidopsis , 2001, Cell.

[56]  R. Kingston,et al.  Reconstitution of a functional core polycomb repressive complex. , 2001, Molecular cell.

[57]  C. Allis,et al.  Translating the Histone Code , 2001, Science.

[58]  J. Riechmann,et al.  Regulation of flowering in Arabidopsis by an FLC homologue. , 2001, Plant physiology.

[59]  R. Amasino,et al.  Loss of FLOWERING LOCUS C Activity Eliminates the Late-Flowering Phenotype of FRIGIDA and Autonomous Pathway Mutations but Not Responsiveness to Vernalization , 2001, Plant Cell.

[60]  R. Amasino,et al.  Identification of a MADS-box gene, FLOWERING LOCUS M, that represses flowering. , 2001, The Plant journal : for cell and molecular biology.

[61]  M. Ishitani,et al.  The Arabidopsis HOS1 gene negatively regulates cold signal transduction and encodes a RING finger protein that displays cold-regulated nucleo--cytoplasmic partitioning. , 2001, Genes & development.

[62]  Karl Mechtler,et al.  Methylation of histone H3 lysine 9 creates a binding site for HP1 proteins , 2001, Nature.

[63]  Andrew J. Bannister,et al.  Selective recognition of methylated lysine 9 on histone H3 by the HP1 chromo domain , 2001, Nature.

[64]  M. Thomashow.  So what's new in the field of plant cold acclimation? Lots! , 2001, Plant physiology.

[65]  K. Shinozaki,et al.  Various abiotic stresses rapidly activate Arabidopsis MAP kinases ATMPK4 and ATMPK6. , 2000, The Plant journal : for cell and molecular biology.

[66]  R. Amasino,et al.  Memories of winter: vernalization and the competence to flower , 2000 .

[67]  R. Amasino,et al.  Molecular analysis of FRIGIDA, a major determinant of natural variation in Arabidopsis flowering time. , 2000, Science.

[68]  R. Dhindsa,et al.  Early steps in cold sensing by plant cells: the role of actin cytoskeleton and membrane fluidity. , 2000, The Plant journal : for cell and molecular biology.

[69]  J. Dubcovsky,et al.  Epistatic interaction between vernalization genes Vrn-Am1 and Vrn-Am2 in diploid wheat. , 2000, The Journal of heredity.

[70]  G. Tena,et al.  Functional analysis of oxidative stress-activated mitogen-activated protein kinase cascade in plants. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[71]  E. Finnegan,et al.  The molecular basis of vernalization: the central role of FLOWERING LOCUS C (FLC). , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[72]  R. Paro,et al.  The Drosophila Polycomb Protein Interacts with Nucleosomal Core Particles In Vitro via Its Repression Domain , 1999, Molecular and Cellular Biology.

[73]  M. Koornneef,et al.  The early-flowering mutant efs is involved in the autonomous promotion pathway of Arabidopsis thaliana. , 1999, Development.

[74]  Michael F. Thomashow,et al.  PLANT COLD ACCLIMATION: Freezing Tolerance Genes and Regulatory Mechanisms. , 1999, Annual review of plant physiology and plant molecular biology.

[75]  Heather Knight,et al.  Temperature sensing by plants: the primary characteristics of signal perception and calcium response. , 1999, The Plant journal : for cell and molecular biology.

[76]  R. Amasino,et al.  FLOWERING LOCUS C Encodes a Novel MADS Domain Protein That Acts as a Repressor of Flowering , 1999, Plant Cell.

[77]  W. Peacock,et al.  The FLF MADS Box Gene: A Repressor of Flowering in Arabidopsis Regulated by Vernalization and Methylation , 1999, Plant Cell.

[78]  J. Terol,et al.  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. , 1999, Plant physiology.

[79]  E. Stockinger,et al.  Low temperature regulation of the Arabidopsis CBF family of AP2 transcriptional activators as an early step in cold-induced COR gene expression. , 1998, The Plant journal : for cell and molecular biology.

[80]  M. Ishitani,et al.  HOS1, a Genetic Locus Involved in Cold-Responsive Gene Expression in Arabidopsis , 1998, Plant Cell.

[81]  A. Peeters,et al.  GENETIC CONTROL OF FLOWERING TIME IN ARABIDOPSIS. , 1998, Annual review of plant physiology and plant molecular biology.

[82]  O. Schabenberger,et al.  Arabidopsis CBF1 overexpression induces COR genes and enhances freezing tolerance. , 1998, Science.

[83]  A. Gould.  Functions of mammalian Polycomb group and trithorax group related genes. , 1997, Current opinion in genetics & development.

[84]  M. Trick,et al.  Comparison of flowering time genes in Brassica rapa, B. napus and Arabidopsis thaliana. , 1997, Genetics.

[85]  V. Pirrotta,et al.  PcG complexes and chromatin silencing. , 1997, Current opinion in genetics & development.

[86]  H. Hirt,et al.  Stress signaling in plants: a mitogen-activated protein kinase pathway is activated by cold and drought. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[87]  Jan Dvorak,et al.  Genetic map of diploid wheat, Triticum monococcum L., and its comparison with maps of Hordeum vulgare L. , 1996, Genetics.

[88]  K. Irie,et al.  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. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[89]  R. Amasino,et al.  Effect of Vernalization, Photoperiod, and Light Quality on the Flowering Phenotype of Arabidopsis Plants Containing the FRIGIDA Gene , 1995, Plant physiology.

[90]  S. Hill,et al.  Cold-Induced Accumulation of hsp90 Transcripts in Brassica napus , 1995, Plant physiology.

[91]  T. Gibson,et al.  The PHD finger: implications for chromatin-mediated transcriptional regulation. , 1995, Trends in biochemical sciences.

[92]  R. Amasino,et al.  The late-flowering phenotype of FRIGIDA and mutations in LUMINIDEPENDENS is suppressed in the Landsberg erecta strain of Arabidopsis , 1994 .

[93]  M. Koornneef,et al.  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 , 1994 .

[94]  J. Ward,et al.  Evidence for an Extracellular Reception Site for Abscisic Acid in Commelina Guard Cells , 1994, Plant physiology.

[95]  I. Horváth,et al.  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. , 1993, Proceedings of the National Academy of Sciences of the United States of America.

[96]  L. Vézina,et al.  A New Cold-Induced Alfalfa Gene Is Associated with Enhanced Hardening at Subzero Temperature , 1993, Plant physiology.

[97]  W. Peacock,et al.  DNA methylation, vernalization, and the initiation of flowering. , 1993, Proceedings of the National Academy of Sciences of the United States of America.

[98]  E. Rassart,et al.  Cloning, characterization, and expression of a cDNA encoding a 50-kilodalton protein specifically induced by cold acclimation in wheat. , 1992, Plant physiology.

[99]  M. Thomashow,et al.  A cold-regulated Arabidopsis gene encodes a polypeptide having potent cryoprotective activity. , 1992, Biochemical and biophysical research communications.

[100]  A. Campbell,et al.  Transgenic plant aequorin reports the effects of touch and cold-shock and elicitors on cytoplasmic calcium , 1991, Nature.

[101]  S. J. Gilmour,et al.  Cold Acclimation in Arabidopsis thaliana. , 1988, Plant physiology.

[102]  J. G. Atherton,et al.  9 – VERNALIZATION—ENVIRONMENTAL AND GENETIC REGULATION , 1987 .

[103]  C. Guy,et al.  Altered gene expression during cold acclimation of spinach. , 1985, Proceedings of the National Academy of Sciences of the United States of America.

[104]  J. B. Reid,et al.  Flowering in Pisum: the Sites and Possible Mechanisms of the Vernalization Response , 1975 .

[105]  A. Lang.  Physiology of flower initiation , 1965 .

[106]  S. Wellensiek.  Dividing Cells as the Prerequisite for Vernalization. , 1964, Plant physiology.

[107]  S. Wellensiek.  Dividing Cells as the Locus for Vernalization , 1962, Nature.

[108]  W. Hillman.  The physiology of flowering , 1962 .

[109]  P. Chouard.  Vernalization and its Relations to Dormancy , 1960 .

[110]  B. Mcclintock.  The origin and behavior of mutable loci in maize , 1950, Proceedings of the National Academy of Sciences.

[111]  R. Maclagan.  On Hyoscyamus niger , 1860 .