Home LiteratureArticle Details
PMID: 25030056 Published · epublish English Journal Article Research Support, Non-U.S. Gov't

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

Nature communications ·Vol. 5 ·2014-07-17 ·Pages 4457

Castaings L, Bergonzi S, Albani MC, Kemi U, Savolainen O, Coupland G

Abstract

Antisense RNA (asRNA) COOLAIR is expressed at A. thaliana FLOWERING LOCUS C (FLC) in response to winter temperatures. Its contribution to cold-induced silencing of FLC was proposed but its functional and evolutionary significance remain unclear. Here we identify a highly conserved block containing the COOLAIR first exon and core promoter at the 3' end of several FLC orthologues. Furthermore, asRNAs related to COOLAIR are expressed at FLC loci in the perennials A. alpina and A. lyrata, although some splicing variants differ from A. thaliana. Study of the A. alpina orthologue, PERPETUAL FLOWERING 1 (PEP1), demonstrates that AaCOOLAIR is induced each winter of the perennial life cycle. Introduction of PEP1 into A. thaliana reveals that AaCOOLAIR cis-elements confer cold-inducibility in this heterologous species while the difference between PEP1 and FLC mRNA patterns depends on both cis-elements and species-specific trans-acting factors. Thus, expression of COOLAIR is highly conserved, supporting its importance in FLC regulation.

MeSH Terms
Arabidopsis/genetics,metabolism Arabidopsis Proteins/genetics,metabolism Cold Temperature Gene Expression Regulation, Plant MADS Domain Proteins/genetics RNA, Antisense/genetics
Chemicals
Arabidopsis Proteins FLF protein, Arabidopsis MADS Domain Proteins RNA, Antisense
Authors & Affiliations
6 authors, click to expand affiliations / ORCID
Castaings Loren
1] Max Planck Institute for Plant Breeding Research, Carl von Linné Weg 10, D-50829 Cologne, Germany [2].
Bergonzi Sara
Max Planck Institute for Plant Breeding Research, Carl von Linné Weg 10, D-50829 Cologne, Germany.
Albani Maria C
1] Max Planck Institute for Plant Breeding Research, Carl von Linné Weg 10, D-50829 Cologne, Germany [2] Botanical Institute, University of Cologne, Zülpicher Strasse 47B, D-50674 Cologne, Germany.
Kemi Ulla
1] Max Planck Institute for Plant Breeding Research, Carl von Linné Weg 10, D-50829 Cologne, Germany [2] Department of Biology, University of Oulu, PO Box 3000, FIN-90014 Oulu, Finland.
Savolainen Outi
1] Department of Biology, University of Oulu, PO Box 3000, FIN-90014 Oulu, Finland [2] Biocenter Oulu, University of Oulu, FIN-90014 Oulu, Finland.
Coupland George
Max Planck Institute for Plant Breeding Research, Carl von Linné Weg 10, D-50829 Cologne, Germany.
References (57)
57 references, click to expand
  1. FLOWERING LOCUS C encodes a novel MADS domain protein that acts as a repressor of flowering.
    Plant Cell. 1999 May;11(5):949-56 PMID: 10330478
  2. Surveying Saccharomyces genomes to identify functional elements by comparative DNA sequence analysis.
    Genome Res. 2001 Jul;11(7):1175-86 PMID: 11435399
  3. VISTA : visualizing global DNA sequence alignments of arbitrary length.
    Bioinformatics. 2000 Nov;16(11):1046-7 PMID: 11159318
  4. Comparative genomics and regulatory evolution: conservation and function of the Chs and Apetala3 promoters.
    Mol Biol Evol. 2001 Oct;18(10):1882-91 PMID: 11557794
  5. Genic and global functions for Paf1C in chromatin modification and gene expression in Arabidopsis.
    PLoS Genet. 2008 Aug 22;4(8):e1000077 PMID: 18725930
  6. A PHD-polycomb repressive complex 2 triggers the epigenetic silencing of FLC during vernalization.
    Proc Natl Acad Sci U S A. 2008 Nov 4;105(44):16831-6 PMID: 18854416
  7. Molecular basis of age-dependent vernalization in Cardamine flexuosa.
    Science. 2013 May 31;340(6136):1097-100 PMID: 23723237
  8. Effects of genetic perturbation on seasonal life history plasticity.
    Science. 2009 Feb 13;323(5916):930-4 PMID: 19150810
  9. LHP1, the Arabidopsis homologue of HETEROCHROMATIN PROTEIN1, is required for epigenetic silencing of FLC.
    Proc Natl Acad Sci U S A. 2006 Mar 28;103(13):5012-7 PMID: 16549797
  10. The VERNALIZATION 2 gene mediates the epigenetic regulation of vernalization in Arabidopsis.
    Cell. 2001 Nov 16;107(4):525-35 PMID: 11719192
  11. Arabidopsis mutants showing an altered response to vernalization.
    Plant J. 1996 Oct;10(4):637-44 PMID: 8998499
  12. Epigenetic maintenance of the vernalized state in Arabidopsis thaliana requires LIKE HETEROCHROMATIN PROTEIN 1.
    Nat Genet. 2006 Jun;38(6):706-10 PMID: 16682972
  13. Vernalization-mediated epigenetic silencing by a long intronic noncoding RNA.
    Science. 2011 Jan 7;331(6013):76-9 PMID: 21127216
  14. The genetic basis of flowering responses to seasonal cues.
    Nat Rev Genet. 2012 Sep;13(9):627-39 PMID: 22898651
  15. The FLF MADS box gene: a repressor of flowering in Arabidopsis regulated by vernalization and methylation.
    Plant Cell. 1999 Mar;11(3):445-58 PMID: 10072403
  16. Differential regulation of FLOWERING LOCUS C expression by vernalization in cabbage and Arabidopsis.
    Plant Physiol. 2005 Mar;137(3):1037-48 PMID: 15734903
  17. GATA: a graphic alignment tool for comparative sequence analysis.
    BMC Bioinformatics. 2005 Jan 17;6:9 PMID: 15655071
  18. Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana.
    Plant J. 1998 Dec;16(6):735-43 PMID: 10069079
  19. R-loop stabilization represses antisense transcription at the Arabidopsis FLC locus.
    Science. 2013 May 3;340(6132):619-21 PMID: 23641115
  20. Vernalization-induced trimethylation of histone H3 lysine 27 at FLC is not maintained in mitotically quiescent cells.
    Curr Biol. 2007 Nov 20;17(22):1978-83 PMID: 17980595
  21. Cold-induced silencing by long antisense transcripts of an Arabidopsis Polycomb target.
    Nature. 2009 Dec 10;462(7274):799-802 PMID: 20010688
  22. Role of vernalization and of duplicated FLOWERING LOCUS C in the perennial Arabidopsis lyrata.
    New Phytol. 2013 Jan;197(1):323-335 PMID: 23106477
  23. Targeted 3' processing of antisense transcripts triggers Arabidopsis FLC chromatin silencing.
    Science. 2010 Jan 1;327(5961):94-7 PMID: 19965720
  24. Control of flowering time by FLC orthologues in Brassica napus.
    Plant J. 2001 Dec;28(5):545-53 PMID: 11849594
  25. Silencing by plant Polycomb-group genes requires dispersed trimethylation of histone H3 at lysine 27.
    EMBO J. 2006 Oct 4;25(19):4638-49 PMID: 16957776
  26. The FRIGIDA complex activates transcription of FLC, a strong flowering repressor in Arabidopsis, by recruiting chromatin modification factors.
    Plant Cell. 2011 Jan;23(1):289-303 PMID: 21282526
  27. Different regulatory regions are required for the vernalization-induced repression of FLOWERING LOCUS C and for the epigenetic maintenance of repression.
    Plant Cell. 2002 Oct;14(10):2527-37 PMID: 12368502
  28. Vernalization-repression of Arabidopsis FLC requires promoter sequences but not antisense transcripts.
    PLoS One. 2011;6(6):e21513 PMID: 21713009
  29. PEP1 of Arabis alpina is encoded by two overlapping genes that contribute to natural genetic variation in perennial flowering.
    PLoS Genet. 2012;8(12):e1003130 PMID: 23284298
  30. Vernalization-induced repression of FLOWERING LOCUS C stimulates flowering in Sinapis alba and enhances plant responsiveness to photoperiod.
    New Phytol. 2008;178(4):755-765 PMID: 18346112
  31. 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. 2010 Apr;186(1):228-38 PMID: 20100201
  32. The PHD finger protein VRN5 functions in the epigenetic silencing of Arabidopsis FLC.
    Curr Biol. 2007 Jan 9;17(1):73-8 PMID: 17174094
  33. The timing of flowering.
    Plant Physiol. 2010 Oct;154(2):516-20 PMID: 20921176
  34. Rapid turnover of long noncoding RNAs and the evolution of gene expression.
    PLoS Genet. 2012;8(7):e1002841 PMID: 22844254
  35. The Arabidopsis thaliana vernalization response requires a polycomb-like protein complex that also includes VERNALIZATION INSENSITIVE 3.
    Proc Natl Acad Sci U S A. 2006 Sep 26;103(39):14631-6 PMID: 16983073
  36. Flowering time control: another window to the connection between antisense RNA and chromatin.
    Trends Genet. 2012 Sep;28(9):445-53 PMID: 22785023
  37. Arabidopsis REF6 is a histone H3 lysine 27 demethylase.
    Nat Genet. 2011 Jun 05;43(7):715-9 PMID: 21642989
  38. Functional demarcation of active and silent chromatin domains in human HOX loci by noncoding RNAs.
    Cell. 2007 Jun 29;129(7):1311-23 PMID: 17604720
  39. The Arabidopsis RNA-binding protein FCA requires a lysine-specific demethylase 1 homolog to downregulate FLC.
    Mol Cell. 2007 Nov 9;28(3):398-407 PMID: 17996704
  40. A gene loop containing the floral repressor FLC is disrupted in the early phase of vernalization.
    EMBO J. 2013 Jan 9;32(1):140-8 PMID: 23222483
  41. Regulatory elements of the floral homeotic gene AGAMOUS identified by phylogenetic footprinting and shadowing.
    Plant Cell. 2003 Jun;15(6):1296-309 PMID: 12782724
  42. The spen family protein FPA controls alternative cleavage and polyadenylation of RNA.
    Dev Cell. 2010 Feb 16;18(2):203-13 PMID: 20079695
  43. Multiple roles of Arabidopsis VRN1 in vernalization and flowering time control.
    Science. 2002 Jul 12;297(5579):243-6 PMID: 12114624
  44. Independent FLC mutations as causes of flowering-time variation in Arabidopsis thaliana and Capsella rubella.
    Genetics. 2012 Oct;192(2):729-39 PMID: 22865739
  45. Long noncoding RNA as modular scaffold of histone modification complexes.
    Science. 2010 Aug 6;329(5992):689-93 PMID: 20616235
  46. Vernalization in Arabidopsis thaliana is mediated by the PHD finger protein VIN3.
    Nature. 2004 Jan 8;427(6970):159-64 PMID: 14712276
  47. LAGAN and Multi-LAGAN: efficient tools for large-scale multiple alignment of genomic DNA.
    Genome Res. 2003 Apr;13(4):721-31 PMID: 12654723
  48. PEP1 regulates perennial flowering in Arabis alpina.
    Nature. 2009 May 21;459(7245):423-7 PMID: 19369938
  49. Structural and functional differences in the long non-coding RNA hotair in mouse and human.
    PLoS Genet. 2011 May;7(5):e1002071 PMID: 21637793
  50. cis-Regulatory elements and chromatin state coordinately control temporal and spatial expression of FLOWERING LOCUS T in Arabidopsis.
    Plant Cell. 2010 May;22(5):1425-40 PMID: 20472817
  51. BAC-recombineering for studying plant gene regulation: developmental control and cellular localization of SnRK1 kinase subunits.
    Plant J. 2011 Mar;65(5):829-42 PMID: 21235649
  52. Phylogenetic shadowing of primate sequences to find functional regions of the human genome.
    Science. 2003 Feb 28;299(5611):1391-4 PMID: 12610304
  53. Robust control of the seasonal expression of the Arabidopsis FLC gene in a fluctuating environment.
    Proc Natl Acad Sci U S A. 2010 Jun 22;107(25):11632-7 PMID: 20534541
  54. Discovery of functional elements in 12 Drosophila genomes using evolutionary signatures.
    Nature. 2007 Nov 8;450(7167):219-32 PMID: 17994088
  55. A Polycomb-based switch underlying quantitative epigenetic memory.
    Nature. 2011 Jul 24;476(7358):105-8 PMID: 21785438
  56. FRIGIDA delays flowering in Arabidopsis via a cotranscriptional mechanism involving direct interaction with the nuclear cap-binding complex.
    Plant Physiol. 2009 Jul;150(3):1611-8 PMID: 19429606
  57. A PHD finger protein involved in both the vernalization and photoperiod pathways in Arabidopsis.
    Genes Dev. 2006 Dec 1;20(23):3244-8 PMID: 17114575
Article Info
Journal
Nature communications
Abbr.
Nat Commun
ISSN
2041-1723
DOI
10.1038/ncomms5457
Published
2014-07-17
Epub
2014-00-17
Pages
4457
Language
English
Region
England
NLM ID
101528555
PMCID
PMC4109010
Subset
IM
External Links
PubMed source DOI: 10.1038/ncomms5457 PMC Full Text View journal details
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: product@genelibs.com

Copyright © 2026.Genelibs Jinan Honghui Biotechnology Co., Ltd. 鲁ICP备20007159号-2