Antisense COOLAIR mediates the coordinated switching of chromatin states at FLC during vernalization

Proceedings of the National Academy of Sciences of the United States of America

Volumn 111, Issue 45, 2014, Pages 16160-16165

  Csorba, Tibor ^a,b   Questa, Julia I ^a   Sun, Qianwen ^a,c   Dean, Caroline ^a  

^a JOHN INNES CENTRE   (United Kingdom)

^b National Agricultural Research and Innovation Centre   (Hungary)

^c Tsinghua University   (China)

Author keywords

Arabidopsis; Flowering; Histone modifications; Long noncoding RNA; Polycomb

Indexed keywords

COMPLEMENTARY RNA; COOLAIR; HISTONE H3; LONG UNTRANSLATED RNA; LYSINE; UNCLASSIFIED DRUG; ARABIDOPSIS PROTEIN; CHROMATIN; FLF PROTEIN, ARABIDOPSIS; HISTONE; MADS DOMAIN PROTEIN; PLANT RNA; POLYCOMB GROUP PROTEIN;

ARABIDOPSIS THALIANA; ARTICLE; CHROMATIN; COLD EXPOSURE; EPIGENETICS; FLOWERING LOCUS C GENE; GENE; GENE CONTROL; GENE SILENCING; GENETIC ANALYSIS; METHYLATION; PROMOTER REGION; REGULATORY MECHANISM; VERNALIZATION; ARABIDOPSIS; COLD; FLOWER; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; PHYSIOLOGY;

ARABIDOPSIS; ARABIDOPSIS PROTEINS; CHROMATIN; COLD TEMPERATURE; FLOWERS; GENE EXPRESSION REGULATION, PLANT; GENE SILENCING; HISTONES; MADS DOMAIN PROTEINS; METHYLATION; POLYCOMB-GROUP PROTEINS; RNA, ANTISENSE; RNA, LONG NONCODING; RNA, PLANT;

EID: 84909609618     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1419030111     Document Type: Article

References (35)

1. Michaels SD, Amasino RM (1999) FLOWERING LOCUS C encodes a novel MADS domain protein that acts as a repressor of flowering. Plant Cell 11(5):949-956.
2. 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(7):3753-3758.
3. Sheldon CC, et al. (1999) The FLF MADS box gene: A repressor of flowering in Arabidopsis regulated by vernalization and methylation. Plant Cell 11(3):445-458.
4. Gendall AR, Levy YY, Wilson A, Dean C (2001) The VERNALIZATION 2 gene mediates the epigenetic regulation of vernalization in Arabidopsis. Cell 107(4):525-535.
5. De Lucia F, Crevillen P, Jones AM, Greb T, Dean C (2008) A PHD-polycomb repressive complex 2 triggers the epigenetic silencing of FLC during vernalization. Proc Natl Acad Sci USA 105(44):16831-16836.
6. Angel A, Song J, Dean C, Howard M (2011) A Polycomb-based switch underlying quantitative epigenetic memory. Nature 476(7358):105-108.
7. Yang H, Howard M, Dean C (2014) Antagonistic roles for H3K36me3 and H3K27me3 in the cold-induced epigenetic switch at Arabidopsis FLC. Curr Biol 24(15):1793-1797.
8. Liu F, Marquardt S, Lister C, Swiezewski S, Dean C (2010) Targeted 3' processing of antisense transcripts triggers Arabidopsis FLC chromatin silencing. Science 327(5961):94-97.
9. Marquardt S, et al. (2014) Functional consequences of splicing of the antisense transcript COOLAIR on FLC transcription. Mol Cell 54(1):156-165.
10. Wang ZW, Wu Z, Raitskin O, Sun Q, Dean C (2014) Antisense-mediated FLC transcriptional repression requires the P-TEFb transcription elongation factor. Proc Natl Acad Sci USA 111(20):7468-7473.
11. Swiezewski S, Liu F, Magusin A, Dean C (2009) Cold-induced silencing by long antisense transcripts of an Arabidopsis Polycomb target. Nature 462(7274):799-802.
12. Hornyik C, Duc C, Rataj K, Terzi LC, Simpson GG (2010) Alternative polyadenylation of antisense RNAs and flowering time control. Biochem Soc Trans 38(4):1077-1081.
13. Sun Q, Csorba T, Skourti-Stathaki K, Proudfoot NJ, Dean C (2013) R-loop stabilization represses antisense transcription at the Arabidopsis FLC locus. Science 340(6132):619-621.
14. Helliwell CA, Robertson M, Finnegan EJ, Buzas DM, Dennis ES (2011) Vernalizationrepression of Arabidopsis FLC requires promoter sequences but not antisense transcripts. PLoS ONE 6(6):e21513.
15. Gutierrez RA, Ewing RM, Cherry JM, Green PJ (2002) Identification of unstable transcripts in Arabidopsis by cDNA microarray analysis: Rapid decay is associated with a group of touch- and specific clock-controlled genes. Proc Natl Acad Sci USA 99(17):11513-11518.
16. Coustham V, et al. (2012) Quantitative modulation of polycomb silencing underlies natural variation in vernalization. Science 337(6094):584-587.
17. Narsai R, et al. (2007) Genome-wide analysis of mRNA decay rates and their determinants in Arabidopsis thaliana. Plant Cell 19(11):3418-3436.
18. Batista PJ, Chang HY (2013) Long noncoding RNAs: Cellular address codes in development and disease. Cell 152(6):1298-1307.
19. Chu C, Qu K, Zhong FL, Artandi SE, Chang HY (2011) Genomic maps of long noncoding RNA occupancy reveal principles of RNA-chromatin interactions. Mol Cell 44(4):667-678.
20. Finnegan EJ, Dennis ES (2007) Vernalization-induced trimethylation of histone H3 lysine 27 at FLC is not maintained in mitotically quiescent cells. Curr Biol 17(22):1978-1983.
21. Wang D, Tyson MD, Jackson SS, Yadegari R (2006) Partially redundant functions of two SET-domain polycomb-group proteins in controlling initiation of seed development in Arabidopsis. Proc Natl Acad Sci USA 103(35):13244-13249.
22. Dodd IB, Micheelsen MA, Sneppen K, Thon G (2007) Theoretical analysis of epigenetic cell memory by nucleosome modification. Cell 129(4):813-822.
23. Greb T, et al. (2007) The PHD finger protein VRN5 functions in the epigenetic silencing of Arabidopsis FLC. Curr Biol 17(1):73-78.
24. Dong G, Ma DP, Li J (2008) The histone methyltransferase SDG8 regulates shoot branching in Arabidopsis. Biochem Biophys Res Commun 373(4):659-664.
25. Kim SY, et al. (2005) Establishment of the vernalization-responsive, winter-annual habit in Arabidopsis requires a putative histone H3 methyl transferase. Plant Cell 17(12):3301-3310.
26. Xu L, et al. (2008) Di- and tri-but not monomethylation on histone H3 lysine 36 marks active transcription of genes involved in flowering time regulation and other processes in Arabidopsis thaliana. Mol Cell Biol 28(4):1348-1360.
27. Yuan W, et al. (2011) H3K36 methylation antagonizes PRC2-mediated H3K27 methylation. J Biol Chem 286(10):7983-7989.
28. Tanaka Y, Katagiri Z, Kawahashi K, Kioussis D, Kitajima S (2007) Trithorax-group protein ASH1 methylates histone H3 lysine 36. Gene 397(1-2):161-168.
29. Cartagena JA, et al. (2008) The Arabidopsis SDG4 contributes to the regulation of pollen tube growth by methylation of histone H3 lysines 4 and 36 in mature pollen. Dev Biol 315(2):355-368.
30. Zhao Z, Yu Y, Meyer D, Wu C, Shen WH (2005) Prevention of early flowering by expression of FLOWERING LOCUS C requires methylation of histone H3 K36. Nat Cell Biol 7(12):1256-1260.
31. Pedersen MT, Helin K (2010) Histone demethylases in development and disease. Trends Cell Biol 20(11):662-671.
32. Wang KC, Chang HY (2011) Molecular mechanisms of long noncoding RNAs. Mol Cell 43(6):904-914.
33. Keller C, Kulasegaran-Shylini R, Shimada Y, Hotz HR, Bühler M (2013) Noncoding RNAs prevent spreading of a repressive histone mark. Nat Struct Mol Biol 20(8):994-1000.
34. Sheldon CC, Conn AB, Dennis ES, Peacock WJ (2002) Different regulatory regions are required for the vernalization-induced repression of FLOWERING LOCUS C and for the epigenetic maintenance of repression. Plant Cell 14(10):2527-2537.
35. Seeley KA, Byrne DH, Colbert JT (1992) Red light-independent instability of oat phytochrome mRNA in vivo. Plant Cell 4(1):29-38.