Home LiteratureArticle Details
PMID: 22892321 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

The histone methyltransferase SDG724 mediates H3K36me2/3 deposition at MADS50 and RFT1 and promotes flowering in rice.

The Plant cell ·Vol. 24 ·No. 8 ·2012-08-00 ·Pages 3235-47

Sun C, Fang J, Zhao T, Xu B, Zhang F, Liu L, Tang J, Zhang G, Deng X, Chen F, Qian Q, Cao X, Chu C

Abstract

Chromatin modifications affect flowering time in the long-day plant Arabidopsis thaliana, but the role of histone methylation in flowering time regulation of rice (Oryza sativa), a short-day plant, remains to be elucidated. We identified a late-flowering long vegetative phase1 (lvp1) mutant in rice and used map-based cloning to reveal that lvp1 affects the SET domain group protein 724 (SDG724). SDG724 functions as a histone methyltransferase in vitro and contributes to a major fraction of global histone H3 lysine 36 (H3K36) methylation in vivo. Expression analyses of flowering time genes in wild-type and lvp1 mutants revealed that Early heading date1, but not Heading date1, are misregulated in lvp1 mutants. In addition, the double mutant of lvp1 with photoperiod sensitivity5 (se5) flowered later than the se5 single mutant, indicating that lvp1 delays flowering time irrespective of photoperiod. Chromatin immunoprecipitation assays showed that lvp1 had reduced levels of H3K36me2/3 at MADS50 and RFT1. This suggests that the divergent functions of paralogs RFT1 and Hd3a, and of MADS50 and MADS51, are in part due to differential H3K36me2/3 deposition, which also correlates with higher expression levels of MADS50 and RFT1 in flowering promotion in rice.

MeSH Terms
Amino Acid Sequence Chromatin Assembly and Disassembly Chromatin Immunoprecipitation Chromosome Mapping Cloning, Molecular Flowers/enzymology,genetics,physiology Gene Expression Regulation, Plant Genes, Plant Genetic Loci Genetic Vectors Genotyping Techniques Histone Methyltransferases Histone-Lysine N-Methyltransferase/genetics,metabolism Histones/genetics,metabolism Methylation Molecular Sequence Data Mutation Oryza/enzymology,genetics,physiology Photoperiod Plant Proteins/genetics,metabolism Time Factors Transformation, Genetic
Chemicals
Histones Plant Proteins Histone Methyltransferases Histone-Lysine N-Methyltransferase
Authors & Affiliations
13 authors, click to expand affiliations / ORCID
Sun Changhui
State Key Laboratory of Plant Genomics and National Center for Plant Gene Research (Beijing), Institute of Genetics and Developmental Biology, Chinese Academy of Sciences, Beijing 100101, China.
Fang Jun
Zhao Taolan
Xu Bo
Zhang Fantao
Liu Linchuan
Tang Jiuyou
Zhang Genfa
Deng Xiaojian
Chen Fan
Qian Qian
Cao Xiaofeng
Chu Chengcai
References (65)
65 references, click to expand
  1. Ehd1, a B-type response regulator in rice, confers short-day promotion of flowering and controls FT-like gene expression independently of Hd1.
    Genes Dev. 2004 Apr 15;18(8):926-36 PMID: 15078816
  2. Multiple alleles at Early flowering 1 locus making variation in the basic vegetative growth period in rice (Oryza sativa L.).
    Theor Appl Genet. 2009 Jul;119(2):315-23 PMID: 19407983
  3. A POLYCOMB group gene of rice (Oryza sativa L. subspecies indica), OsiEZ1, codes for a nuclear-localized protein expressed preferentially in young seedlings and during reproductive development.
    Gene. 2003 Sep 18;314:1-13 PMID: 14527713
  4. OsMT1a, a type 1 metallothionein, plays the pivotal role in zinc homeostasis and drought tolerance in rice.
    Plant Mol Biol. 2009 May;70(1-2):219-29 PMID: 19229638
  5. Rice Indeterminate 1 (OsId1) is necessary for the expression of Ehd1 (Early heading date 1) regardless of photoperiod.
    Plant J. 2008 Dec;56(6):1018-29 PMID: 18774969
  6. Regulation of carotenoid composition and shoot branching in Arabidopsis by a chromatin modifying histone methyltransferase, SDG8.
    Plant Cell. 2009 Jan;21(1):39-53 PMID: 19174535
  7. DWARF AND LOW-TILLERING, a new member of the GRAS family, plays positive roles in brassinosteroid signaling in rice.
    Plant J. 2009 Jun;58(5):803-16 PMID: 19220793
  8. Phytochrome mediates the external light signal to repress FT orthologs in photoperiodic flowering of rice.
    Genes Dev. 2002 Aug 1;16(15):2006-20 PMID: 12154129
  9. FT protein movement contributes to long-distance signaling in floral induction of Arabidopsis.
    Science. 2007 May 18;316(5827):1030-3 PMID: 17446353
  10. Arabidopsis histone methyltransferase SET DOMAIN GROUP8 mediates induction of the jasmonate/ethylene pathway genes in plant defense response to necrotrophic fungi.
    Plant Physiol. 2010 Nov;154(3):1403-14 PMID: 20810545
  11. SET DOMAIN GROUP25 encodes a histone methyltransferase and is involved in FLOWERING LOCUS C activation and repression of flowering.
    Plant Physiol. 2009 Nov;151(3):1476-85 PMID: 19726574
  12. Natural variation in Ghd7 is an important regulator of heading date and yield potential in rice.
    Nat Genet. 2008 Jun;40(6):761-7 PMID: 18454147
  13. 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
  14. Ehd2, a rice ortholog of the maize INDETERMINATE1 gene, promotes flowering by up-regulating Ehd1.
    Plant Physiol. 2008 Nov;148(3):1425-35 PMID: 18790997
  15. Regulation of flowering in rice: two florigen genes, a complex gene network, and natural variation.
    Curr Opin Plant Biol. 2011 Feb;14(1):45-52 PMID: 20864385
  16. OsWRKY71, a rice transcription factor, is involved in rice defense response.
    J Plant Physiol. 2007 Aug;164(8):969-79 PMID: 16919842
  17. OsMADS50 and OsMADS56 function antagonistically in regulating long day (LD)-dependent flowering in rice.
    Plant Cell Environ. 2009 Oct;32(10):1412-27 PMID: 19558411
  18. Genetic regulation of time to flower in Arabidopsis thaliana.
    Annu Rev Plant Biol. 2004;55:521-35 PMID: 15377230
  19. Hd3a protein is a mobile flowering signal in rice.
    Science. 2007 May 18;316(5827):1033-6 PMID: 17446351
  20. Plant SET domain-containing proteins: structure, function and regulation.
    Biochim Biophys Acta. 2007 May-Jun;1769(5-6):316-29 PMID: 17512990
  21. Diversification in flowering time due to tandem FT-like gene duplication, generating novel Mendelian factors in wild and cultivated rice.
    Mol Ecol. 2009 Apr;18(7):1537-49 PMID: 19298266
  22. Hd1, a major photoperiod sensitivity quantitative trait locus in rice, is closely related to the Arabidopsis flowering time gene CONSTANS.
    Plant Cell. 2000 Dec;12(12):2473-2484 PMID: 11148291
  23. Analysis of PHOTOPERIOD SENSITIVITY5 sheds light on the role of phytochromes in photoperiodic flowering in rice.
    Plant Physiol. 2009 Oct;151(2):681-90 PMID: 19675157
  24. OsMADS51 is a short-day flowering promoter that functions upstream of Ehd1, OsMADS14, and Hd3a.
    Plant Physiol. 2007 Dec;145(4):1484-94 PMID: 17951465
  25. Redundant requirement for a pair of PROTEIN ARGININE METHYLTRANSFERASE4 homologs for the proper regulation of Arabidopsis flowering time.
    Plant Physiol. 2008 Sep;148(1):490-503 PMID: 18660432
  26. Daylength measurements by rice plants in photoperiodic short-day flowering.
    Int Rev Cytol. 2007;256:191-222 PMID: 17241908
  27. Histone methylation in higher plants.
    Annu Rev Plant Biol. 2010;61:395-420 PMID: 20192747
  28. Histone modifications in transcriptional activation during plant development.
    Biochim Biophys Acta. 2011 Oct;1809(10):567-76 PMID: 21777708
  29. Phylogenomic analysis of the PEBP gene family in cereals.
    J Mol Evol. 2005 Nov;61(5):579-90 PMID: 16170456
  30. SET domain proteins in plant development.
    Biochim Biophys Acta. 2011 Aug;1809(8):407-20 PMID: 21664308
  31. Prevention of early flowering by expression of FLOWERING LOCUS C requires methylation of histone H3 K36.
    Nat Cell Biol. 2005 Dec;7(12):1256-60 PMID: 16299497
  32. ATXR5 and ATXR6 are H3K27 monomethyltransferases required for chromatin structure and gene silencing.
    Nat Struct Mol Biol. 2009 Jul;16(7):763-8 PMID: 19503079
  33. Establishment of the vernalization-responsive, winter-annual habit in Arabidopsis requires a putative histone H3 methyl transferase.
    Plant Cell. 2005 Dec;17(12):3301-10 PMID: 16258034
  34. The structure of NSD1 reveals an autoregulatory mechanism underlying histone H3K36 methylation.
    J Biol Chem. 2011 Mar 11;286(10):8361-8368 PMID: 21196496
  35. SDG714, a histone H3K9 methyltransferase, is involved in Tos17 DNA methylation and transposition in rice.
    Plant Cell. 2007 Jan;19(1):9-22 PMID: 17259261
  36. Role of chromatin modification in flowering-time control.
    Trends Plant Sci. 2005 Jan;10(1):30-5 PMID: 15642521
  37. Control of the transition to flowering by chromatin modifications.
    Mol Plant. 2009 Jul;2(4):554-564 PMID: 19825638
  38. Adaptation of photoperiodic control pathways produces short-day flowering in rice.
    Nature. 2003 Apr 17;422(6933):719-22 PMID: 12700762
  39. Promoting gene expression in plants by permissive histone lysine methylation.
    Plant Signal Behav. 2009 Jun;4(6):484-8 PMID: 19816124
  40. Functional analyses of the flowering time gene OsMADS50, the putative SUPPRESSOR OF OVEREXPRESSION OF CO 1/AGAMOUS-LIKE 20 (SOC1/AGL20) ortholog in rice.
    Plant J. 2004 Jun;38(5):754-64 PMID: 15144377
  41. RID1, encoding a Cys2/His2-type zinc finger transcription factor, acts as a master switch from vegetative to floral development in rice.
    Proc Natl Acad Sci U S A. 2008 Sep 2;105(35):12915-20 PMID: 18725639
  42. SET DOMAIN GROUP2 is the major histone H3 lysine [corrected] 4 trimethyltransferase in Arabidopsis.
    Proc Natl Acad Sci U S A. 2010 Oct 26;107(43):18557-62 PMID: 20937886
  43. Adaptation of flowering-time by natural and artificial selection in Arabidopsis and rice.
    J Exp Bot. 2007;58(12):3091-7 PMID: 17693414
  44. Comparative analysis of SET domain proteins in maize and Arabidopsis reveals multiple duplications preceding the divergence of monocots and dicots.
    Plant Physiol. 2003 Jun;132(2):907-25 PMID: 12805620
  45. Identification of a novel gene ef7 conferring an extremely long basic vegetative growth phase in rice.
    Theor Appl Genet. 2009 Aug;119(4):675-84 PMID: 19495721
  46. 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. 2008 Feb;28(4):1348-60 PMID: 18070919
  47. ARABIDOPSIS TRITHORAX-RELATED7 is required for methylation of lysine 4 of histone H3 and for transcriptional activation of FLOWERING LOCUS C.
    Plant Cell. 2009 Oct;21(10):3257-69 PMID: 19855050
  48. Understanding the words of chromatin regulation.
    Cell. 2009 Jan 23;136(2):200-6 PMID: 19167321
  49. Epigenetic modifications in plants: an evolutionary perspective.
    Curr Opin Plant Biol. 2011 Apr;14(2):179-86 PMID: 21233005
  50. A pair of floral regulators sets critical day length for Hd3a florigen expression in rice.
    Nat Genet. 2010 Jul;42(7):635-8 PMID: 20543848
  51. Hd3a, a rice ortholog of the Arabidopsis FT gene, promotes transition to flowering downstream of Hd1 under short-day conditions.
    Plant Cell Physiol. 2002 Oct;43(10):1096-105 PMID: 12407188
  52. Growth habit determination by the balance of histone methylation activities in Arabidopsis.
    EMBO J. 2010 Sep 15;29(18):3208-15 PMID: 20711170
  53. Hd3a and RFT1 are essential for flowering in rice.
    Development. 2008 Feb;135(4):767-74 PMID: 18223202
  54. The ASH1 HOMOLOG 2 (ASHH2) histone H3 methyltransferase is required for ovule and anther development in Arabidopsis.
    PLoS One. 2009 Nov 12;4(11):e7817 PMID: 19915673
  55. A gene network for long-day flowering activates RFT1 encoding a mobile flowering signal in rice.
    Development. 2009 Oct;136(20):3443-50 PMID: 19762423
  56. The histone methyltransferase SDG8 regulates shoot branching in Arabidopsis.
    Biochem Biophys Res Commun. 2008 Sep 5;373(4):659-64 PMID: 18602372
  57. Rice SUVH histone methyltransferase genes display specific functions in chromatin modification and retrotransposon repression.
    Mol Plant. 2010 Jul;3(4):773-82 PMID: 20566579
  58. Phytochromes confer the photoperiodic control of flowering in rice (a short-day plant).
    Plant J. 2000 Jun;22(5):391-9 PMID: 10849355
  59. OsSET1, a novel SET-domain-containing gene from rice.
    J Exp Bot. 2003 Aug;54(389):1995-6 PMID: 12815033
  60. H3K36 methylation is critical for brassinosteroid-regulated plant growth and development in rice.
    Plant J. 2012 Apr;70(2):340-7 PMID: 22136623
  61. Isolation of rice genes possibly involved in the photoperiodic control of flowering by a fluorescent differential display method.
    Plant Cell Physiol. 2002 May;43(5):494-504 PMID: 12040096
  62. Arabidopsis SET DOMAIN GROUP2 is required for H3K4 trimethylation and is crucial for both sporophyte and gametophyte development.
    Plant Cell. 2010 Oct;22(10):3232-48 PMID: 21037105
  63. Molecular analysis of rice plants harboring a multi-functional T-DNA tagging system.
    J Genet Genomics. 2009 May;36(5):267-76 PMID: 19447374
  64. 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. 2008 Mar 15;315(2):355-68 PMID: 18252252
  65. Histone variants and modifications in plant gene regulation.
    Curr Opin Plant Biol. 2011 Apr;14(2):116-22 PMID: 21159547
Article Info
Journal
The Plant cell
Abbr.
Plant Cell
ISSN
1532-298X
DOI
10.1105/tpc.112.101436
Published
2012-08-00
Epub
2012-00-14
Pages
3235-47
Language
English
Region
England
NLM ID
9208688
PMCID
PMC3462628
Subset
IM
External Links
PubMed source DOI: 10.1105/tpc.112.101436 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: [email protected]

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