Home LiteratureArticle Details
PMID: 21258002 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

Arabidopsis floral initiator SKB1 confers high salt tolerance by regulating transcription and pre-mRNA splicing through altering histone H4R3 and small nuclear ribonucleoprotein LSM4 methylation.

The Plant cell ·Vol. 23 ·No. 1 ·2011-01-00 ·Pages 396-411

Zhang Z, Zhang S, Zhang Y, Wang X, Li D, Li Q, Yue M, Li Q, Zhang YE, Xu Y, Xue Y, Chong K, Bao S

Abstract

Plants adapt their growth and development in response to perceived salt stress. Although DELLA-dependent growth restraint is thought to be an integration of the plant's response to salt stress, little is known about how histone modification confers salt stress and, in turn, affects development. Here, we report that floral initiator Shk1 kinase binding protein1 (SKB1) and histone4 arginine3 (H4R3) symmetric dimethylation (H4R3sme2) integrate responses to plant developmental progress and salt stress. Mutation of SKB1 results in salt hypersensitivity, late flowering, and growth retardation. SKB1 associates with chromatin and thereby increases the H4R3sme2 level to suppress the transcription of FLOWERING LOCUS C (FLC) and a number of stress-responsive genes. During salt stress, the H4R3sme2 level is reduced, as a consequence of SKB1 disassociating from chromatin to induce the expression of FLC and the stress-responsive genes but increasing the methylation of small nuclear ribonucleoprotein Sm-like4 (LSM4). Splicing defects are observed in the skb1 and lsm4 mutants, which are sensitive to salt. We propose that SKB1 mediates plant development and the salt response by altering the methylation status of H4R3sme2 and LSM4 and linking transcription to pre-mRNA splicing.

MeSH Terms
Abscisic Acid/pharmacology Arabidopsis/genetics,growth & development,metabolism Arabidopsis Proteins/genetics,metabolism Flowers/growth & development Gene Expression Profiling Gene Expression Regulation, Plant Histones/metabolism MADS Domain Proteins/metabolism Methylation Mutation Oligonucleotide Array Sequence Analysis RNA Precursors/metabolism RNA Splicing RNA, Plant/metabolism Ribonucleoproteins, Small Nuclear/genetics,metabolism Salt Tolerance Salt-Tolerant Plants/genetics,growth & development,metabolism Transcription, Genetic
Chemicals
Arabidopsis Proteins FLF protein, Arabidopsis Histones MADS Domain Proteins RNA Precursors RNA, Plant Ribonucleoproteins, Small Nuclear Abscisic Acid
Authors & Affiliations
13 authors, click to expand affiliations / ORCID
Zhang Zhaoliang
Key Laboratory of Molecular and Developmental Biology, Institute of Genetics and Developmental Biology, Chinese Academy of Sciences, Beijing 100101, China.
Zhang Shupei
Zhang Ya
Wang Xin
Li Dan
Li Qiuling
Yue Minghui
Li Qun
Zhang Yu-e
Xu Yunyuan
Xue Yongbiao
Chong Kang
Bao Shilai
References (101)
101 references, click to expand
  1. Targeting an mRNA for decapping: displacement of translation factors and association of the Lsm1p-7p complex on deadenylated yeast mRNAs.
    Mol Cell. 2001 Nov;8(5):1075-83 PMID: 11741542
  2. A genetic link between cold responses and flowering time through FVE in Arabidopsis thaliana.
    Nat Genet. 2004 Feb;36(2):167-71 PMID: 14745450
  3. Ion homeostasis during salt stress in plants.
    Curr Opin Cell Biol. 2001 Aug;13(4):399-404 PMID: 11454443
  4. Yeast caspase 1 links messenger RNA stability to apoptosis in yeast.
    EMBO Rep. 2005 Nov;6(11):1076-81 PMID: 16170310
  5. Identification and characterization of Uss1p (Sdb23p): a novel U6 snRNA-associated protein with significant similarity to core proteins of small nuclear ribonucleoproteins.
    EMBO J. 1995 May 1;14(9):2066-75 PMID: 7744012
  6. Abscisic acid inhibits type 2C protein phosphatases via the PYR/PYL family of START proteins.
    Science. 2009 May 22;324(5930):1068-71 PMID: 19407142
  7. Enhancement of abscisic acid sensitivity and reduction of water consumption in Arabidopsis by combined inactivation of the protein phosphatases type 2C ABI1 and HAB1.
    Plant Physiol. 2006 Aug;141(4):1389-99 PMID: 16798945
  8. Arabidopsis ABA response gene ABI1: features of a calcium-modulated protein phosphatase.
    Science. 1994 Jun 3;264(5164):1448-52 PMID: 7910981
  9. Cell signaling under salt, water and cold stresses.
    Curr Opin Plant Biol. 2001 Oct;4(5):401-6 PMID: 11597497
  10. Lesions in the mRNA cap-binding gene ABA HYPERSENSITIVE 1 suppress FRIGIDA-mediated delayed flowering in Arabidopsis.
    Plant J. 2004 Oct;40(1):112-9 PMID: 15361145
  11. SKB1-mediated symmetric dimethylation of histone H4R3 controls flowering time in Arabidopsis.
    EMBO J. 2007 Apr 4;26(7):1934-41 PMID: 17363895
  12. Abiotic stress and ABA-inducible Group 4 LEA from Brassica napus plays a key role in salt and drought tolerance.
    J Biotechnol. 2009 Jan 15;139(2):137-45 PMID: 19014980
  13. Abscisic acid activation of plasma membrane Ca(2+) channels in guard cells requires cytosolic NAD(P)H and is differentially disrupted upstream and downstream of reactive oxygen species production in abi1-1 and abi2-1 protein phosphatase 2C mutants.
    Plant Cell. 2001 Nov;13(11):2513-23 PMID: 11701885
  14. Regulation of ion homeostasis under salt stress.
    Curr Opin Plant Biol. 2003 Oct;6(5):441-5 PMID: 12972044
  15. Arabidopsis transcriptome analysis under drought, cold, high-salinity and ABA treatment conditions using a tiling array.
    Plant Cell Physiol. 2008 Aug;49(8):1135-49 PMID: 18625610
  16. The Arabidopsis aldehyde oxidase 3 (AAO3) gene product catalyzes the final step in abscisic acid biosynthesis in leaves.
    Proc Natl Acad Sci U S A. 2000 Nov 7;97(23):12908-13 PMID: 11050171
  17. Regulation of the ABA-sensitive Arabidopsis potassium channel gene GORK in response to water stress.
    FEBS Lett. 2003 Nov 6;554(1-2):119-26 PMID: 14596925
  18. Regulated RNA processing in the control of Arabidopsis flowering.
    Int J Dev Biol. 2005;49(5-6):773-80 PMID: 16096981
  19. Plant serine/arginine-rich proteins and their role in pre-mRNA splicing.
    Trends Plant Sci. 2004 Nov;9(11):541-7 PMID: 15501179
  20. Abscisic acid: emergence of a core signaling network.
    Annu Rev Plant Biol. 2010;61:651-79 PMID: 20192755
  21. Assisted RNP assembly: SMN and PRMT5 complexes cooperate in the formation of spliceosomal UsnRNPs.
    EMBO J. 2002 Nov 1;21(21):5853-63 PMID: 12411503
  22. A proteomic analysis of arginine-methylated protein complexes.
    Mol Cell Proteomics. 2003 Dec;2(12):1319-30 PMID: 14534352
  23. Methylation of ribosomal protein S10 by protein-arginine methyltransferase 5 regulates ribosome biogenesis.
    J Biol Chem. 2010 Apr 23;285(17):12695-705 PMID: 20159986
  24. Gain-of-function and loss-of-function phenotypes of the protein phosphatase 2C HAB1 reveal its role as a negative regulator of abscisic acid signalling.
    Plant J. 2004 Feb;37(3):354-69 PMID: 14731256
  25. Fibroblast growth factor 2 (FGF-2) is a novel substrate for arginine methylation by PRMT5.
    Biol Chem. 2009 Jan;390(1):59-65 PMID: 19086919
  26. Role of plant RNA-binding proteins in development, stress response and genome organization.
    Trends Plant Sci. 2009 Apr;14(4):229-36 PMID: 19285908
  27. PRMT5-mediated methylation of histone H4R3 recruits DNMT3A, coupling histone and DNA methylation in gene silencing.
    Nat Struct Mol Biol. 2009 Mar;16(3):304-311 PMID: 19234465
  28. The expression level of the chromatin-associated HMGB1 protein influences growth, stress tolerance, and transcriptome in Arabidopsis.
    J Mol Biol. 2008 Dec 5;384(1):9-21 PMID: 18822296
  29. 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
  30. A putative transcriptional elongation factor hIws1 is essential for mammalian cell proliferation.
    Biochem Biophys Res Commun. 2007 Feb 2;353(1):47-53 PMID: 17184735
  31. Regulation of osmotic stress-responsive gene expression by the LOS6/ABA1 locus in Arabidopsis.
    J Biol Chem. 2002 Mar 8;277(10):8588-96 PMID: 11779861
  32. Human SWI/SNF-associated PRMT5 methylates histone H3 arginine 8 and negatively regulates expression of ST7 and NM23 tumor suppressor genes.
    Mol Cell Biol. 2004 Nov;24(21):9630-45 PMID: 15485929
  33. Regulation of flowering time by FVE, a retinoblastoma-associated protein.
    Nat Genet. 2004 Feb;36(2):162-6 PMID: 14745447
  34. Gene expression-based classification and regulatory networks of pediatric acute lymphoblastic leukemia.
    Blood. 2009 Nov 12;114(20):4486-93 PMID: 19755675
  35. Transcriptional regulatory networks in cellular responses and tolerance to dehydration and cold stresses.
    Annu Rev Plant Biol. 2006;57:781-803 PMID: 16669782
  36. Blimp1 associates with Prmt5 and directs histone arginine methylation in mouse germ cells.
    Nat Cell Biol. 2006 Jun;8(6):623-30 PMID: 16699504
  37. Methylation of SPT5 regulates its interaction with RNA polymerase II and transcriptional elongation properties.
    Mol Cell. 2003 Apr;11(4):1055-66 PMID: 12718890
  38. Histone arginine methylation is required for vernalization-induced epigenetic silencing of FLC in winter-annual Arabidopsis thaliana.
    Proc Natl Acad Sci U S A. 2008 Jan 15;105(2):411-6 PMID: 18178621
  39. Regulation of Arabidopsis cryptochrome 2 by blue-light-dependent phosphorylation.
    Nature. 2002 Jun 13;417(6890):763-7 PMID: 12066190
  40. Involvement of Arabidopsis HOS15 in histone deacetylation and cold tolerance.
    Proc Natl Acad Sci U S A. 2008 Mar 25;105(12):4945-50 PMID: 18356294
  41. Protein arginine methylation in mammals: who, what, and why.
    Mol Cell. 2009 Jan 16;33(1):1-13 PMID: 19150423
  42. Modulation of abscisic acid signal transduction and biosynthesis by an Sm-like protein in Arabidopsis.
    Dev Cell. 2001 Dec;1(6):771-81 PMID: 11740939
  43. Mutations in the Type II protein arginine methyltransferase AtPRMT5 result in pleiotropic developmental defects in Arabidopsis.
    Plant Physiol. 2007 Aug;144(4):1913-23 PMID: 17573539
  44. Cell signaling during cold, drought, and salt stress.
    Plant Cell. 2002;14 Suppl:S165-83 PMID: 12045276
  45. Sm-like proteins wRING the neck of mRNA.
    Curr Biol. 2000 Jun 29;10(13):R478-81 PMID: 10898971
  46. Role of chromatin modification in flowering-time control.
    Trends Plant Sci. 2005 Jan;10(1):30-5 PMID: 15642521
  47. Integration of plant responses to environmentally activated phytohormonal signals.
    Science. 2006 Jan 6;311(5757):91-4 PMID: 16400150
  48. Control of DNA methylation and heterochromatic silencing by histone H2B deubiquitination.
    Nature. 2007 Jun 7;447(7145):735-8 PMID: 17554311
  49. Arginine methylation mediated by the Arabidopsis homolog of PRMT5 is essential for proper pre-mRNA splicing.
    Proc Natl Acad Sci U S A. 2010 Nov 2;107(44):19114-9 PMID: 20956294
  50. Arginine methyltransferase Capsuleen is essential for methylation of spliceosomal Sm proteins and germ cell formation in Drosophila.
    Development. 2007 Jan;134(1):137-46 PMID: 17164419
  51. Molecular genetic perspectives on cross-talk and specificity in abiotic stress signalling in plants.
    J Exp Bot. 2004 Jan;55(395):225-36 PMID: 14673035
  52. Functions of Lsm proteins in mRNA degradation and splicing.
    Curr Opin Cell Biol. 2000 Jun;12(3):346-50 PMID: 10801455
  53. Control of the transition to flowering by chromatin modifications.
    Mol Plant. 2009 Jul;2(4):554-564 PMID: 19825638
  54. A protein phosphatase 2C involved in ABA signal transduction in Arabidopsis thaliana.
    Science. 1994 Jun 3;264(5164):1452-5 PMID: 8197457
  55. ROS1, a repressor of transcriptional gene silencing in Arabidopsis, encodes a DNA glycosylase/lyase.
    Cell. 2002 Dec 13;111(6):803-14 PMID: 12526807
  56. Integration of abscisic acid signalling into plant responses.
    Plant Biol (Stuttg). 2006 May;8(3):314-25 PMID: 16807823
  57. srGAP2 arginine methylation regulates cell migration and cell spreading through promoting dimerization.
    J Biol Chem. 2010 Nov 5;285(45):35133-41 PMID: 20810653
  58. Regulation of flowering time by the protein arginine methyltransferase AtPRMT10.
    EMBO Rep. 2007 Dec;8(12):1190-5 PMID: 18007657
  59. The highly conserved protein methyltransferase, Skb1, is a mediator of hyperosmotic stress response in the fission yeast Schizosaccharomyces pombe.
    J Biol Chem. 2001 May 4;276(18):14549-52 PMID: 11278267
  60. Arginine methylation an emerging regulator of protein function.
    Mol Cell. 2005 Apr 29;18(3):263-72 PMID: 15866169
  61. A thermosensory pathway controlling flowering time in Arabidopsis thaliana.
    Nat Genet. 2003 Feb;33(2):168-71 PMID: 12548286
  62. Xenopus LSm proteins bind U8 snoRNA via an internal evolutionarily conserved octamer sequence.
    Mol Cell Biol. 2002 Jun;22(12):4101-12 PMID: 12024024
  63. Uncoupling the effects of abscisic acid on plant growth and water relations. Analysis of sto1/nced3, an abscisic acid-deficient but salt stress-tolerant mutant in Arabidopsis.
    Plant Physiol. 2004 Oct;136(2):3134-47 PMID: 15466233
  64. Chromatin techniques for plant cells.
    Plant J. 2004 Sep;39(5):776-89 PMID: 15315638
  65. Regulation of flowering time by RNA processing.
    Curr Top Microbiol Immunol. 2008;326:201-18 PMID: 18630754
  66. PRMT5 regulates Golgi apparatus structure through methylation of the golgin GM130.
    Cell Res. 2010 Sep;20(9):1023-33 PMID: 20421892
  67. The Arabidopsis LOS5/ABA3 locus encodes a molybdenum cofactor sulfurase and modulates cold stress- and osmotic stress-responsive gene expression.
    Plant Cell. 2001 Sep;13(9):2063-83 PMID: 11549764
  68. Mechanisms of salinity tolerance.
    Annu Rev Plant Biol. 2008;59:651-81 PMID: 18444910
  69. Salt tolerance conferred by overexpression of a vacuolar Na+/H+ antiport in Arabidopsis.
    Science. 1999 Aug 20;285(5431):1256-8 PMID: 10455050
  70. Arabidopsis abi1-1 and abi2-1 phosphatase mutations reduce abscisic acid-induced cytoplasmic calcium rises in guard cells.
    Plant Cell. 1999 Sep;11(9):1785-98 PMID: 10488243
  71. Arginine methylation at a glance.
    J Cell Sci. 2007 Dec 15;120(Pt 24):4243-6 PMID: 18057026
  72. RNA-Seq: a revolutionary tool for transcriptomics.
    Nat Rev Genet. 2009 Jan;10(1):57-63 PMID: 19015660
  73. Modulation of ethylene responses affects plant salt-stress responses.
    Plant Physiol. 2007 Feb;143(2):707-19 PMID: 17189334
  74. Analysis of celery (Apium graveolens) mannitol dehydrogenase (Mtd) promoter regulation in Arabidopsis suggests roles for MTD in key environmental and metabolic responses.
    Plant Mol Biol. 2001 Nov;47(5):621-31 PMID: 11725947
  75. Alternative splicing of pre-mRNAs of Arabidopsis serine/arginine-rich proteins: regulation by hormones and stresses.
    Plant J. 2007 Mar;49(6):1091-107 PMID: 17319848
  76. mSin3A/histone deacetylase 2- and PRMT5-containing Brg1 complex is involved in transcriptional repression of the Myc target gene cad.
    Mol Cell Biol. 2003 Nov;23(21):7475-87 PMID: 14559996
  77. Salt and drought stress signal transduction in plants.
    Annu Rev Plant Biol. 2002;53:247-73 PMID: 12221975
  78. Calcium- and salt-stress signaling in plants: shedding light on SOS pathway.
    Arch Biochem Biophys. 2008 Mar 15;471(2):146-58 PMID: 18241665
  79. The Arabidopsis ABSCISIC ACID-INSENSITIVE2 (ABI2) and ABI1 genes encode homologous protein phosphatases 2C involved in abscisic acid signal transduction.
    Plant Cell. 1997 May;9(5):759-71 PMID: 9165752
  80. Caenorhabditis elegans protein arginine methyltransferase PRMT-5 negatively regulates DNA damage-induced apoptosis.
    PLoS Genet. 2009 Jun;5(6):e1000514 PMID: 19521535
  81. Organization and expression of two Arabidopsis DREB2 genes encoding DRE-binding proteins involved in dehydration- and high-salinity-responsive gene expression.
    Plant Mol Biol. 2000 Mar;42(4):657-65 PMID: 10809011
  82. Arginine methylation regulates the p53 response.
    Nat Cell Biol. 2008 Dec;10(12):1431-9 PMID: 19011621
  83. Multiple functional interactions between components of the Lsm2-Lsm8 complex, U6 snRNA, and the yeast La protein.
    Genetics. 2001 May;158(1):187-96 PMID: 11333229
  84. Protein arginine methylation: Cellular functions and methods of analysis.
    Biochim Biophys Acta. 2006 Dec;1764(12):1890-903 PMID: 17010682
  85. VERNALIZATION INSENSITIVE 3 (VIN3) is required for the response of Arabidopsis thaliana seedlings exposed to low oxygen conditions.
    Plant J. 2009 Aug;59(4):576-87 PMID: 19392705
  86. Widespread role for the flowering-time regulators FCA and FPA in RNA-mediated chromatin silencing.
    Science. 2007 Oct 5;318(5847):109-12 PMID: 17916737
  87. Regulation of flowering time by histone acetylation in Arabidopsis.
    Science. 2003 Dec 5;302(5651):1751-4 PMID: 14593187
  88. Two novel GPCR-type G proteins are abscisic acid receptors in Arabidopsis.
    Cell. 2009 Jan 9;136(1):136-48 PMID: 19135895
  89. The histone-binding protein COPR5 is required for nuclear functions of the protein arginine methyltransferase PRMT5.
    EMBO Rep. 2008 May;9(5):452-8 PMID: 18404153
  90. The Sm-protein methyltransferase, dart5, is essential for germ-cell specification and maintenance.
    Curr Biol. 2006 Jun 6;16(11):1077-89 PMID: 16753561
  91. An assembly chaperone collaborates with the SMN complex to generate spliceosomal SnRNPs.
    Cell. 2008 Oct 31;135(3):497-509 PMID: 18984161
  92. Yeast Sm-like proteins function in mRNA decapping and decay.
    Nature. 2000 Mar 30;404(6777):515-8 PMID: 10761922
  93. SCABP8/CBL10, a putative calcium sensor, interacts with the protein kinase SOS2 to protect Arabidopsis shoots from salt stress.
    Plant Cell. 2007 Apr;19(4):1415-31 PMID: 17449811
  94. H2A.Z-containing nucleosomes mediate the thermosensory response in Arabidopsis.
    Cell. 2010 Jan 8;140(1):136-47 PMID: 20079334
  95. The methylosome, a 20S complex containing JBP1 and pICln, produces dimethylarginine-modified Sm proteins.
    Mol Cell Biol. 2001 Dec;21(24):8289-300 PMID: 11713266
  96. A methyl transferase links the circadian clock to the regulation of alternative splicing.
    Nature. 2010 Nov 4;468(7320):112-6 PMID: 20962777
  97. Methylation of histone H3 and H4 by PRMT5 regulates ribosomal RNA gene transcription.
    J Cell Biochem. 2010 Feb 15;109(3):553-63 PMID: 19998411
  98. The LIM protein AJUBA recruits protein arginine methyltransferase 5 to mediate SNAIL-dependent transcriptional repression.
    Mol Cell Biol. 2008 May;28(10):3198-207 PMID: 18347060
  99. ABI1 protein phosphatase 2C is a negative regulator of abscisic acid signaling.
    Plant Cell. 1999 Oct;11(10):1897-910 PMID: 10521520
  100. GOEAST: a web-based software toolkit for Gene Ontology enrichment analysis.
    Nucleic Acids Res. 2008 Jul 1;36(Web Server issue):W358-63 PMID: 18487275
  101. Negative regulation of transcription by the type II arginine methyltransferase PRMT5.
    EMBO Rep. 2002 Jul;3(7):641-5 PMID: 12101096
Article Info
Journal
The Plant cell
Abbr.
Plant Cell
ISSN
1532-298X
Published
2011-01-00
Epub
2011-00-21
Pages
396-411
Language
English
Region
England
NLM ID
9208688
PMCID
PMC3051234
Subset
IM
Databases
GEO
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