Encoding memory of winter by noncoding RNAs

In some plant species, prolonged exposure to low temperature during the winter season is necessary to acquire the competence to flower in the following spring. This process, known as vernalization, is an epigenetic change in that a mitotically stable change of the developmental potential of the meristem (competence to flower) is maintained even in the absence of the inducing signal (prolonged cold exposure). In Arabidopsis, vernalization results in stable epigenetic repression of a potent floral repressor, FLOWERING LOCUS C (FLC). Increased enrichment of Polycomb Repressive Complex 2 (PRC2) and trimethylated Histone H3 Lys 27 (H3K27me3) at FLC chromatin is necessary for the stable maintenance of FLC repression by vernalization. Recent recognition of long noncoding RNAs (ncRNAs) in vernalization response indicates that long ncRNAs are evolutionarily conserved components for PRC2-mediated repression in eukaryotes.

[1]  J. Komorowski,et al.  Kcnq1ot1 antisense noncoding RNA mediates lineage-specific transcriptional silencing through chromatin-level regulation. , 2008, Molecular cell.

[2]  Toshiro K. Ohsumi,et al.  Genome-wide identification of polycomb-associated RNAs by RIP-seq. , 2010, Molecular cell.

[3]  J. Dubcovsky,et al.  Genetic and Molecular Characterization of the VRN2 Loci in Tetraploid Wheat1[W][OA] , 2008, Plant Physiology.

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

[5]  Danhua Jiang,et al.  Repression of FLOWERING LOCUS C and FLOWERING LOCUS T by the Arabidopsis Polycomb Repressive Complex 2 Components , 2008, PloS one.

[6]  Sibum Sung,et al.  Vernalization-Mediated Epigenetic Silencing by a Long Intronic Noncoding RNA , 2011, Science.

[7]  Alexandra M. E. Jones,et al.  A PHD-Polycomb Repressive Complex 2 triggers the epigenetic silencing of FLC during vernalization , 2008, Proceedings of the National Academy of Sciences.

[8]  R. Amasino,et al.  Vernalization: winter and the timing of flowering in plants. , 2009, Annual review of cell and developmental biology.

[9]  M. Robertson,et al.  The Arabidopsis thaliana vernalization response requires a polycomb-like protein complex that also includes VERNALIZATION INSENSITIVE 3 , 2006, Proceedings of the National Academy of Sciences.

[10]  Donna M Bond,et al.  Polycomb proteins regulate the quantitative induction of VERNALIZATION INSENSITIVE 3 in response to low temperatures. , 2011, The Plant journal : for cell and molecular biology.

[11]  Richard A Young,et al.  Short RNAs are transcribed from repressed polycomb target genes and interact with polycomb repressive complex-2. , 2010, Molecular cell.

[12]  Howard Y. Chang,et al.  Functional Demarcation of Active and Silent Chromatin Domains in Human HOX Loci by Noncoding RNAs , 2007, Cell.

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

[14]  Antoine H. F. M. Peters,et al.  Polycomb group proteins Ezh2 and Rnf2 direct genomic contraction and imprinted repression in early mouse embryos. , 2008, Developmental cell.

[15]  Jennifer A. Mitchell,et al.  The Air Noncoding RNA Epigenetically Silences Transcription by Targeting G9a to Chromatin , 2008, Science.

[16]  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.

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

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

[19]  Peter Fraser,et al.  Kcnq1ot1/Lit1 Noncoding RNA Mediates Transcriptional Silencing by Targeting to the Perinucleolar Region , 2008, Molecular and Cellular Biology.

[20]  Olivier Voinnet,et al.  The long and the short of noncoding RNAs. , 2009, Current opinion in cell biology.

[21]  R. Amasino,et al.  Arabidopsis Relatives of the Human Lysine-Specific Demethylase1 Repress the Expression of FWA and FLOWERING LOCUS C and Thus Promote the Floral Transition[W] , 2007, The Plant Cell Online.

[22]  O. Nilsson,et al.  An Antagonistic Pair of FT Homologs Mediates the Control of Flowering Time in Sugar Beet , 2010, Science.

[23]  J. Mellor.  It Takes a PHD to Read the Histone Code , 2006, Cell.

[24]  W. Reik,et al.  The long noncoding RNA Kcnq1ot1 organises a lineage-specific nuclear domain for epigenetic gene silencing , 2009, Development.

[25]  I. Henderson,et al.  The need for winter in the switch to flowering. , 2003, Annual review of genetics.

[26]  Robert J. Schmitz,et al.  Vernalization: a model for investigating epigenetics and eukaryotic gene regulation in plants. , 2007, Biochimica et biophysica acta.

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

[28]  G. Kreiman,et al.  Widespread transcription at neuronal activity-regulated enhancers , 2010, Nature.

[29]  T. Derrien,et al.  Long Noncoding RNAs with Enhancer-like Function in Human Cells , 2010, Cell.

[30]  Robert J. Schmitz,et al.  DICER-LIKE 1 and DICER-LIKE 3 Redundantly Act to Promote Flowering via Repression of FLOWERING LOCUS C in Arabidopsis thaliana , 2007, Genetics.

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

[32]  G. Simpson,et al.  The spen family protein FPA controls alternative cleavage and polyadenylation of RNA. , 2010, Developmental cell.

[33]  C. Dean,et al.  Cold-induced silencing by long antisense transcripts of an Arabidopsis Polycomb target , 2009, Nature.

[34]  T. Jenuwein,et al.  Silencing by plant Polycomb‐group genes requires dispersed trimethylation of histone H3 at lysine 27 , 2006, The EMBO journal.

[35]  J. Ecker,et al.  Small RNA-mediated chromatin silencing directed to the 3′ region of the Arabidopsis gene encoding the developmental regulator, FLC , 2007, Proceedings of the National Academy of Sciences.

[36]  Howard Y. Chang,et al.  Long Noncoding RNA as Modular Scaffold of Histone Modification Complexes , 2010, Science.

[37]  Jeannie T. Lee,et al.  Polycomb Proteins Targeted by a Short Repeat RNA to the Mouse X Chromosome , 2008, Science.

[38]  J. Mattick,et al.  Long non-coding RNAs: insights into functions , 2009, Nature Reviews Genetics.

[39]  W. Peacock,et al.  Different Regulatory Regions Are Required for the Vernalization-Induced Repression of FLOWERING LOCUS C and for the Epigenetic Maintenance of Repression Article, publication date, and citation information can be found at www.plantcell.org/cgi/doi/10.1105/tpc.004564. , 2002, The Plant Cell Online.

[40]  Xuemei Chen,et al.  Small RNAs and their roles in plant development. , 2009, Annual review of cell and developmental biology.

[41]  R. Amasino,et al.  Epigenetic maintenance of the vernalized state in Arabidopsis thaliana requires LIKE HETEROCHROMATIN PROTEIN 1 , 2006, Nature Genetics.