Evolutionary conservation of cold-induced antisense RNAs of FLOWERING LOCUS C in Arabidopsis thaliana perennial relatives

Nature Communications

Volumn 5, Issue , 2014, Pages

  Castaings, Loren ^a,d   Bergonzi, Sara ^a   Albani, Maria C ^a,b   Kemi, Ulla ^a,c   Savolainen, Outi ^c   Coupland, George ^a  

^a MAX PLANCK INSTITUTE FOR PLANT BREEDING RESEARCH   (Germany)

^b UNIVERSITY OF COLOGNE   (Germany)

^c UNIVERSITY OF OULU   (Finland)

^d CNRS   (France)

Author keywords

[No Author keywords available]

Indexed keywords

COMPLEMENTARY RNA; MESSENGER RNA; PERPETUAL FLOWERING 1; PROTEIN; SPACER DNA; TRANS ACTING FACTOR; UNCLASSIFIED DRUG; ARABIDOPSIS PROTEIN; FLF PROTEIN, ARABIDOPSIS; MADS DOMAIN PROTEIN;

DICOTYLEDON; EVOLUTIONARY BIOLOGY; FLOWERING; GENE EXPRESSION; RNA; TEMPERATURE EFFECT; WINTER;

ARABIDOPSIS; ARABIDOPSIS ALPINA; ARABIDOPSIS LYRATA; ARABIDOPSIS THALIANA; ARTICLE; COLD EXPOSURE; CONTROLLED STUDY; EXON; FLOWERING LOCUS C; GENE EXPRESSION; GENE LOCUS; GENE REPRESSION; GENE SEQUENCE; GENE TRANSFER; GENETIC CONSERVATION; LIFE CYCLE; NONHUMAN; NUCLEOTIDE SEQUENCE; PERENNIAL PLANT; PROMOTER REGION; VERNALIZATION; COLD; GENE EXPRESSION REGULATION; GENETICS; METABOLISM;

ARABIDOPSIS; ARABIDOPSIS PROTEINS; COLD TEMPERATURE; GENE EXPRESSION REGULATION, PLANT; MADS DOMAIN PROTEINS; RNA, ANTISENSE;

EID: 84904614824     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms5457     Document Type: Article

References (58)

1. Amasino, R. M. & Michaels, S. D. The timing of flowering. Plant Physiol. 154, 516-520 (2010).
2. Andres, F. & Coupland, G. The genetic basis of flowering responses to seasonal cues. Nat. Rev. Genet. 13, 627-639 (2012).
3. Michaels, S. D. & Amasino, R. M. FLOWERING LOCUS C encodes a novel MADS domain protein that acts as a repressor of flowering. Plant Cell 11, 949-956 (1999).
4. Sheldon, C. C. et al. The FLF MADS box gene: a repressor of flowering in Arabidopsis regulated by vernalization and methylation. Plant Cell 11, 445-458 (1999).
5. Angel, A., Song, J., Dean, C. & Howard, M. A Polycomb-based switch underlying quantitative epigenetic memory. Nature 476, 105 (2011).
6. Finnegan, E. J. & Dennis, E. S. Vernal ization-induced trimethylation of histone H3 lysine 27 at FLC is not maintainedin mitotically quiescent cells. Curr. Biol. 17, 1978-1983 (2007). (Pubitemid 350088488)
7. Sung, S. B. & Amasino, R. M. Vernalization in Arabidopsis thaliana is mediated by the PHD finger protein VIN3. Nature 427, 159-164 (2004). (Pubitemid 38094956)
8. Wood, C. C. et al. The Arabidopsis thaliana vernalization response requires a polycomb-like protein complex that also includes VERNALIZATION INSENSITIVE 3. Proc. Natl Acad. Sci. USA 103, 14631-14636 (2006). (Pubitemid 44484801)
9. De Lucia, F., Crevillen, P., Jones, A. M. E., Greb, T. & Dean, C. A PHDPolycomb Repressive Complex 2 triggers the epigenetic silencing of FLC during vernalization. Proc. Natl Acad. Sci. USA 105, 16831-16836 (2008).
10. Gendall, A. R., Levy, Y. Y., Wilson, A. & Dean, C. The VERNALIZATIO 2 gene mediates the epigenetic regulation of vernalization in Arabidopsis. Cell 107, 525-535 (2001). (Pubitemid 33152787)
11. Ietswaart, R., Wu, Z. & Dean, C. Flowering time control: another window to the connection between antisense RNA and chromatin. Trends Genet. 28, 445-453 (2012).
12. Heo, J. B. & Sung, S. Vernalization-mediated epigenetic silencing by a long intronic noncoding RNA. Science 331, 76-79 (2011).
13. Sung, S. B. et al. Epigenetic maintenance of the vernalized state in Arabidopsis thaliana requires LIKE HETEROCHROMATIN PROTEIN 1. Nat. Genet. 38, 706-710 (2006).
14. Sheldon, C. C., Conn, A. B., Dennis, E. S. & Peacock, W. J. Different regulatory regions are required for the vernalization-induced repression of FLOWERING LOCUS C and for the epigenetic maintenance of repression. Plant Cell 14, 2527-2537 (2002). (Pubitemid 35224847)
15. Swiezewski, S., Liu, F. Q., Magusin, A. & Dean, C. Cold-induced silencing by long antisense transcripts of an Arabidopsis Polycomb target. Nature 462, 799-U122 (2009).
16. Hornyik, C., Terzi, L. C. & Simpson, G. G. The Spen family protein FPA controls alternative cleavage and polyadenylation of RNA. Dev. Cell 18, 203-213 (2010).
17. Liu, F. Q., Marquardt, S., Lister, C., Swiezewski, S. & Dean, C. Targeted 30 processing of antisense transcripts triggers Arabidopsis FLC chromatin silencing. Science 327, 94-97 (2010).
18. Liu, F. et al. The Arabidopsis RNA-binding protein FCA requires a lysinespecific demethylase 1 homolog to downregulate FLC. Mol. Cell 28, 398-407 (2007). (Pubitemid 350030571)
19. Helliwell, C. A., Robertson, M., Finnegan, E. J., Buzas, D. M. & Dennis, E. S. Vernalization-repression of Arabidopsis FLC requires promoter sequences but not antisense transcripts. PLoS ONE 6, e21513 (2011).
20. Sun, Q., Csorba, T., Skourti-Stathaki, K., Proudfoot, N. J. & Dean, C. R-loop stabilization represses antisense transcription at the Arabidopsis FLC locus. Science 340, 619-621 (2013).
21. Wang, R. H. et al. PEP1 regulates perennial flowering in Arabis alpina. Nature 459, 423-427 (2009).
22. Lin, S. I. et al. Differential regulation of expression by vernalization FLOWERING LOCUS C in cabbage and Arabidopsis. Plant Physiol. 137, 1037-1048 (2005).
23. Tadege, M. et al. Control of flowering time by FLC orthologues in Brassica napus. Plant J. 28, 545-553 (2001). (Pubitemid 34039234)
24. Aikawa, S., Kobayashi, 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 107, 11632-11637 (2010).
25. D'Aloia, M., Tocquin, P. & Perilleux, C. Vernalization-induced repression of FLOWERING LOCUS C stimulates flowering in Sinapis alba and enhances plant responsiveness to photoperiod. New Phytol. 178, 755-765 (2008). (Pubitemid 351670095)
26. Kemi, U. et al. Role of vernalization and of duplicated FLOWERING LOCUS C in the perennial Arabidopsis lyrata. New Phytol. 197, 323-335 (2013).
27. Guo, Y. L., Todesco, M., Hagmann, J., Das, S. & Weigel, D. Independent FLC mutations as causes of flowering time variation in Arabidopsis thaliana and Capsella rubella. Genetics 192, 729-739 (2012).
28. Zhou, C. M. et al. Molecular basis of age-dependent vernalization in Cardamine flexuosa. Science 340, 1097-1100 (2013).
29. Boffelli, D. et al. Phylogenetic shadowing of primate sequences to find functional regions of the human genome. Science 299, 1391-1394 (2003). (Pubitemid 36254651)
30. Cliften, P. F. et al. Surveying Saccharomyces genomes to identify functional elements by comparative DNA sequence analysis. Genome Res. 11, 1175-1186 (2001). (Pubitemid 32677291)
31. Stark, A. et al. Discovery of functional elements in 12 Drosophila genomes using evolutionary signatures. Nature 450, 219-232 (2007). (Pubitemid 350100553)
32. Adrian, J. et al. cis-Regulatory elements and chromatin state coordinately control temporal and spatial expression of FLOWERING LOCUS T in Arabidopsis. Plant Cell 22, 1425-1440 (2010).
33. Hong, R. L., Hamaguchi, L., Busch, M. A. & Weigel, D. Regulatory elements of the floral homeotic gene AGAMOUS identified by phylogenetic footprinting and shadowing. Plant Cell 15, 1296-1309 (2003). (Pubitemid 36715173)
34. Koch, M. A., Weisshaar, B., Kroymann, J., Haubold, B. & Mitchell-Olds, T. Comparative genomics and regulatory evolution: conservation and function of the Chs and Apetala3 promoters. Mol. Biol. Evol. 18, 1882-1891 (2001). (Pubitemid 32916640)
35. Kutter, C. et al. Rapid turnover of long noncoding RNAs and the evolution of gene expression. PLoS Genet. 8, e1002841 (2012).
36. Schorderet, P. & Duboule, D. Structural and functional differences in the long non-coding RNA hotair in mouse and human. PLoS Genet. 7, e1002071 (2011).
37. Albani, M. et al. PEP1 of Arabis alpina is encoded by two overlapping genes that contribute to natural genetic variation in perennial flowering. PLoS Genet. 8, e1003130 (2012).
38. Nah, G. & Chen, Z. J. Tandem duplication of the FLC locus and the origin of a new gene in Arabidopsis related species and their functional implications in allopolyploids. New Phytol. 186, 228-238 (2010).
39. Greb, T. et al. The PHD finger protein VRN5 functions in the epigenetic silencing of Arabidopsis FLC. Curr. Biol. 17, 73-78 (2007). (Pubitemid 46027584)
40. Sung, S. B., Schmitz, R. J. & Amasino, R. M. A PHD finger protein involved in both the vernalization and photoperiod pathways in Arabidopsis. Gene Dev. 20, 3244-3248 (2006). (Pubitemid 44904846)
41. Schubert, D. et al. Silencing by plant Polycomb-group genes requires dispersed trimethylation of histone H3 at lysine 27. EMBO J. 25, 4638-4649 (2006). (Pubitemid 44498136)
42. 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 297, 243-246 (2002). (Pubitemid 34761284)
43. Mylne, J. S. et al. LHP1, the Arabidopsis homologue of HETEROCHROMATIN PROTEIN1, is required for epigenetic silencing of FLC. Proc. Natl Acad. Sci. USA 103, 5012-5017 (2006).
44. Lu, F. L., Cui, X., Zhang, S. B., Jenuwein, T. & Cao, X. F. Arabidopsis REF6 is a histone H3 lysine 27 demethylase. Nat. Genet. 43, 715-U144 (2011).
45. Oh, S., Park, S. & van Nocker, S. Genic and global functions for Paf1C in chromatin modification and gene expression in Arabidopsis. PLoS Genet. 4, e1000077 (2008).
46. Geraldo, N., Baurle, I., Kidou, S., Hu, X. & Dean, C. FRIGIDA delays flowering in Arabidopsis via a cotranscriptional mechanism involving direct interaction with the nuclear cap-binding complex. Plant Physiol. 150, 1611-1618 (2009).
47. Choi, K. et al. The FRIGIDA complex activates transcription of FLC, a strong flowering repressor in Arabidopsis, by recruiting chromatin modification factors. Plant Cell 23, 289-303 (2011).
48. Rinn, J. L. et al. Functional demarcation of active and silent chromatin domains in human HOX loci by noncoding RNAs. Cell 129, 1311-1323 (2007). (Pubitemid 46962090)
49. Tsai, M. C. et al. Long noncoding RNA as modular scaffold of histone modification complexes. Science 329, 689-693 (2010).
50. Wilczek, A. M. et al. Effects of genetic perturbation on seasonal life history plasticity. Science 323, 930-934 (2009).
51. Crevillen, P., Sonmez, C., Wu, Z. & Dean, C. A gene loop containing the floral repressor FLC is disrupted in the early phase of vernalization. EMBO J. 32, 140-148 (2013).
52. Hackett, W. P. Juvenility, maturation, and rejuvenation in woody plants. Hortic. Rev. 7, 109-155 (1985).
53. Brudno, M. et al. LAGAN and Multi-LAGAN: efficient tools for large-scale multiple alignment of genomic DNA. Genome Res. 13, 721-731 (2003). (Pubitemid 36511930)
54. Mayor, C. et al. VISTA: visualizing global DNA sequence alignments of arbitrary length. Bioinformatics 16, 1046-1047 (2000). (Pubitemid 32051021)
55. Nix, D. A. & Eisen, M. B. GATA: a graphic alignment tool for comparative sequence analysis. BMC Bioinformatics 6, 9 (2005).
56. Clough, S. J. & Bent, A. F. Floral dip: a simplified method for Agrobacteriummediated transformation of Arabidopsis thaliana. Plant J. 16, 735-743 (1998).
57. Chandler, J., Wilson, A. & Dean, C. Arabidopsis mutants showing an altered response to vernalization. Plant J. 10, 637-644 (1996). (Pubitemid 27103017)
58. Bitrian, M., Roodbarkelari, F., Horvath, M. & Koncz, C. BAC-recombineering for studying plant gene regulation: developmental control and cellular localization of SnRK1 kinase subunits. Plant J. 65, 829-842 (2011).