title: O-GlcNAc-mediated interaction between VER2 and TaGRP2 elicits TaVRN1 mRNA accumulation during vernalization in winter wheat.
abstract: Vernalization, sensing of prolonged cold, is important for seasonal flowering in eudicots and monocots. While vernalization silences a repressor (FLC, MADS-box transcription factor) in eudicots, it induces an activator (TaVRN1, an AP1 clade MADS-box transcription factor) in monocots. The mechanism for TaVRN1 induction during vernalization is not well understood. Here we reveal a novel mechanism for controlling TaVRN1 mRNA accumulation in response to prolonged cold sensing in wheat. The carbohydrate-binding protein VER2, a jacalin lectin, promotes TaVRN1 upregulation by physically interacting with the RNA-binding protein TaGRP2. TaGRP2 binds to TaVRN1 pre-mRNA and inhibits TaVRN1 mRNA accumulation. The physical interaction between VER2 and TaGRP2 is controlled by TaGRP2 O-GlcNAc modification, which gradually increases during vernalization. The interaction between VER2 and O-GlcNAc-TaGRP2 reduces TaGRP2 protein accumulation in the nucleus and/or promotes TaGRP2 dissociation from TaVRN1, leading to TaVRN1 mRNA accumulation. Our data reveal a new mechanism for sensing prolonged cold in temperate cereals.
authors.affiliation: 1] Key Laboratory of Plant Molecular Physiology, Institute of Botany, Chinese Academy of Sciences, Beijing 100093, China [2] University of the Chinese Academy of Sciences, Beijing 100049, China [3].
authors.forename: Jun
authors.initials: J
authors.lastname: Xiao
authors.affiliation: 1] Key Laboratory of Plant Molecular Physiology, Institute of Botany, Chinese Academy of Sciences, Beijing 100093, China [2] University of the Chinese Academy of Sciences, Beijing 100049, China [3].
authors.forename: Shujuan
authors.initials: S
authors.lastname: Xu
authors.affiliation: 1] Key Laboratory of Plant Molecular Physiology, Institute of Botany, Chinese Academy of Sciences, Beijing 100093, China [2] University of the Chinese Academy of Sciences, Beijing 100049, China [3].
authors.forename: Chunhua
authors.initials: C
authors.lastname: Li
authors.affiliation: Key Laboratory of Plant Molecular Physiology, Institute of Botany, Chinese Academy of Sciences, Beijing 100093, China.
authors.forename: Yunyuan
authors.initials: Y
authors.lastname: Xu
authors.affiliation: Key Laboratory of Plant Molecular Physiology, Institute of Botany, Chinese Academy of Sciences, Beijing 100093, China.
authors.forename: Lijing
authors.initials: L
authors.lastname: Xing
authors.affiliation: Key Laboratory of Plant Molecular Physiology, Institute of Botany, Chinese Academy of Sciences, Beijing 100093, China.
authors.forename: Yuda
authors.initials: Y
authors.lastname: Niu
authors.affiliation: 1] Key Laboratory of Plant Molecular Physiology, Institute of Botany, Chinese Academy of Sciences, Beijing 100093, China [2] University of the Chinese Academy of Sciences, Beijing 100049, China.
authors.forename: Qing
authors.initials: Q
authors.lastname: Huan
authors.affiliation: Hybrid Wheat Research Center, Beijing Academy of Agriculture and Forestry Sciences, Beijing 100089, China.
authors.forename: Yimiao
authors.initials: Y
authors.lastname: Tang
authors.affiliation: Hybrid Wheat Research Center, Beijing Academy of Agriculture and Forestry Sciences, Beijing 100089, China.
authors.forename: Changping
authors.initials: C
authors.lastname: Zhao
authors.affiliation: Department of Biology, University of Pennsylvania, Philadelphia, Pennsylvania 19104, USA.
authors.forename: Doris
authors.initials: D
authors.lastname: Wagner
authors.affiliation: Institute of Genetics and Developmental Biology, Chinese Academy of Sciences, Beijing 100101, China.
authors.forename: Caixia
authors.initials: C
authors.lastname: Gao
authors.affiliation: 1] Key Laboratory of Plant Molecular Physiology, Institute of Botany, Chinese Academy of Sciences, Beijing 100093, China [2] National Center for Plant Gene Research, Beijing 100093, China.
authors.forename: Kang
authors.initials: K
authors.lastname: Chong
mesh_terms: D000117:Acetylglucosamine / Q000378:metabolism*; D000818:Animals; D002467:Cell Nucleus / Q000378:metabolism; D002736:Chloroplasts / Q000378:metabolism; D018506:Gene Expression Regulation, Plant; D017343:Genes, Plant; D047468:Immunoprecipitation; D037102:Lectins / Q000502:physiology*; D051379:Mice; D008957:Models, Genetic; D016297:Mutagenesis, Site-Directed; D010641:Phenotype; D018515:Plant Leaves / Q000502:physiology; D010940:Plant Proteins / Q000235:genetics* / Q000502:physiology; D012333:RNA, Messenger / Q000378:metabolism*; D012621:Seasons; D014157:Transcription Factors / Q000235:genetics* / Q000378:metabolism; D014908:Triticum / Q000235:genetics / Q000378:metabolism*
chemical_list: D037102:Lectins; D010940:Plant Proteins; D012333:RNA, Messenger; D014157:Transcription Factors; D000117:Acetylglucosamine
references.citation: Plant Cell. 1999 May;11(5):949-56
references.pmid: 10330478
references.citation: Nucleic Acids Res. 2012 Dec;40(22):11240-55
references.pmid: 23042250
references.citation: Plant Physiol. 2003 Aug;132(4):1849-60
references.pmid: 12913142
references.citation: Nat Protoc. 2007;2(7):1565-72
references.pmid: 17585298
references.citation: Plant Physiol. 2011 Mar;155(3):1091-102
references.pmid: 21224338
references.citation: Mol Cells. 2010 Mar;29(3):283-90
references.pmid: 20387034
references.citation: Plant Cell Rep. 2005 Mar;23(10-11):751-8
references.pmid: 15503032
references.citation: Plant Cell. 1993 Aug;5(8):887-96
references.pmid: 8400871
references.citation: Curr Protoc Mol Biol. 2006 Aug;Chapter 27:Unit 27.4
references.pmid: 18265380
references.citation: Planta. 2006 Jul;224(2):360-6
references.pmid: 16440213
references.citation: Tsitol Genet. 2007 May-Jun;41(3):13-22
references.pmid: 17649620
references.citation: Plant Physiol. 1968 Oct;43(10):1696-8
references.pmid: 16656956
references.citation: Plant Physiol. 1966 Feb;41(2):277-81
references.pmid: 16656251
references.citation: Plant Cell. 2004 Jun;16(6):1550-63
references.pmid: 15155885
references.citation: Oncogene. 2010 May 13;29(19):2831-42
references.pmid: 20190804
references.citation: Science. 2011 Jan 7;331(6013):76-9
references.pmid: 21127216
references.citation: Plant J. 2008 Aug;55(3):455-66
references.pmid: 18410480
references.citation: Planta. 2003 Jun;217(2):261-70
references.pmid: 12783334
references.citation: BMC Plant Biol. 2013 Dec 11;13:209
references.pmid: 24330651
references.citation: J Biol Chem. 1984 Mar 10;259(5):3308-17
references.pmid: 6421821
references.citation: Plant Cell. 1995 Sep;7(9):1459-71
references.pmid: 8589629
references.citation: Biochim Biophys Acta. 2006 May-Jun;1761(5-6):599-617
references.pmid: 16781888
references.citation: PLoS Genet. 2012;8(12):e1003134
references.pmid: 23271982
references.citation: Mol Genet Genomics. 2005 Mar;273(1):54-65
references.pmid: 15690172
references.citation: Mol Cell. 2004 Feb 27;13(4):599-609
references.pmid: 14992728
references.citation: Am J Physiol Endocrinol Metab. 2008 Jul;295(1):E17-28
references.pmid: 18445751
references.citation: J Exp Bot. 2006;57(4):865-75
references.pmid: 16473894
references.citation: Plant J. 2003 Jan;33(2):361-71
references.pmid: 12535349
references.citation: Plant J. 2008 Oct;56(2):239-250
references.pmid: 18573194
references.citation: Plant Mol Biol. 2013 Aug 20;:
references.pmid: 23959941
references.citation: Proc Natl Acad Sci U S A. 2009 May 19;106(20):8386-91
references.pmid: 19416817
references.citation: J Biol Chem. 2009 Aug 7;284(32):21327-37
references.pmid: 19506079
references.citation: Proc Natl Acad Sci U S A. 2003 May 13;100(10):6263-8
references.pmid: 12730378
references.citation: Plant J. 2004 Sep;39(5):776-89
references.pmid: 15315638
references.citation: Curr Opin Plant Biol. 2009 Apr;12(2):178-84
references.pmid: 19195924
references.citation: PLoS One. 2009;4(3):e4854
references.pmid: 19287503
references.citation: PLoS One. 2011;6(12):e29456
references.pmid: 22242122
references.citation: Nature. 1990 Aug 30;346(6287):818-22
references.pmid: 1697402
references.citation: J Exp Bot. 2012 Feb;63(3):1329-39
references.pmid: 22090442
references.citation: Ann Bot. 2009 Jun;103(8):1165-72
references.pmid: 19304997
references.citation: J Exp Bot. 2013 May;64(8):2413-22
references.pmid: 23580755
references.citation: Plant Physiol. 2005 Aug;138(4):2364-73
references.pmid: 16055679
references.citation: Proc Natl Acad Sci U S A. 2003 Oct 28;100(22):13099-104
references.pmid: 14557548
references.citation: Am J Physiol Endocrinol Metab. 2003 Feb;284(2):E424-34
references.pmid: 12397027
references.citation: Nature. 2007 Apr 26;446(7139):1017-22
references.pmid: 17460662
references.citation: J Cell Sci. 2012 Aug 15;125(Pt 16):3723-31
references.pmid: 22935652
references.citation: Cold Spring Harb Symp Quant Biol. 2012;77:105-15
references.pmid: 23619014
references.citation: Nature. 2013 Apr 4;496(7443):91-5
references.pmid: 23535592
references.citation: J Biol Chem. 1997 Apr 4;272(14):9308-15
references.pmid: 9083067
references.citation: Proc Natl Acad Sci U S A. 2002 Dec 24;99(26):16899-903
references.pmid: 12477932
references.citation: Plant Cell Physiol. 2007 Aug;48(8):1192-206
references.pmid: 17623742
references.citation: Genetics. 2002 Jul;161(3):1279-91
references.pmid: 12136030
references.citation: Plant Cell. 2012 Jan;24(1):96-108
references.pmid: 22267487
references.citation: J Hered. 2009 May-Jun;100(3):355-64
references.pmid: 19251764
references.citation: Endocr Rev. 2004 Oct;25(5):807-30
references.pmid: 15466941
references.citation: Plant Methods. 2006 Jun 29;2:13
references.pmid: 16808845
references.citation: Mol Genet Genomics. 2009 Aug;282(2):107-17
references.pmid: 19404679
references.citation: Mol Genet Genomics. 2012 Jul;287(7):575-90
references.pmid: 22684814
references.citation: PLoS One. 2011 Apr 19;6(4):e18959
references.pmid: 21526146
references.citation: Biochim Biophys Acta. 2004 Jul 6;1673(1-2):13-28
references.pmid: 15238246
references.citation: Nucleic Acids Res. 2009 Jul;37(Web Server issue):W202-8
references.pmid: 19458158
references.citation: Plant Signal Behav. 2010 Feb;5(2):99-104
references.pmid: 20009520
references.citation: Physiol Plant. 1998 Jan;102(1):87-92
references.pmid: 35359125