Home LiteratureArticle Details
PMID: 17526749 Published · ppublish English Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't

An SNF2 protein associated with nuclear RNA silencing and the spread of a silencing signal between cells in Arabidopsis.

The Plant cell ·Vol. 19 ·No. 5 ·2007-05-00 ·Pages 1507-21

Smith LM, Pontes O, Searle I, Yelina N, Yousafzai FK, Herr AJ, Pikaard CS, Baulcombe DC

Abstract

The silencing phenotype in Arabidopsis thaliana lines with an inverted repeat transgene under the control of a phloem-specific promoter was manifested in regions around veins due to a mobile signal of silencing. Genetic analysis implicates RNA-DEPENDENT RNA POLYMERASE2 (RDR2) and an RNA polymerase IVa subunit gene (NRPD1a) in the signaling mechanism. We also identified an SNF2 domain-containing protein (CLASSY1) that acts together with RDR2 and NRPD1a in the spread of transgene silencing and in the production of endogenous 24-nucleotide short interfering RNAs (siRNAs). Cytochemical analysis indicates that CLASSY1 may act in the nucleus with NRPD1a and RDR2 in the upstream part of RNA silencing pathways that generate a double-stranded RNA substrate for Dicer-like (DCL) nucleases. DCL3 and ARGONAUTE4 act in a downstream part of the pathway, leading to endogenous 24-nucleotide siRNA production, but are not required for intercellular signaling. From genetic analysis, we conclude that another downstream part of the pathway associated with intercellular signaling requires DCL4 and at least one other protein required for 21-nucleotide trans-acting siRNAs. We interpret the effect of polymerase IVa and trans-acting siRNA pathway mutations in terms of a modular property of RNA silencing pathways.

MeSH Terms
Alleles Amino Acid Sequence Arabidopsis/cytology,enzymology,genetics,metabolism Arabidopsis Proteins/chemistry,genetics,metabolism Cell Nucleus/metabolism DNA Polymerase beta/metabolism Gene Expression Regulation, Plant Genes, Reporter Intracellular Signaling Peptides and Proteins/chemistry,genetics,metabolism MicroRNAs/metabolism Models, Biological Molecular Sequence Data Mutagenesis Mutation/genetics Phenotype Plants, Genetically Modified Protein Structure, Secondary Protein Structure, Tertiary Protein Transport RNA Interference RNA, Small Interfering/metabolism RNA-Dependent RNA Polymerase/metabolism Signal Transduction Subcellular Fractions/metabolism
Chemicals
Arabidopsis Proteins CLASSY1 protein, Arabidopsis Intracellular Signaling Peptides and Proteins MicroRNAs RNA, Small Interfering RDR2 protein, Arabidopsis RNA-Dependent RNA Polymerase DNA Polymerase beta
Authors & Affiliations
8 authors, click to expand affiliations / ORCID
Smith Lisa M
Sainsbury Laboratory, John Ines Centre, Norwich NR4 7UH, United Kingdom.
Pontes Olga
Searle Iain
Yelina Nataliya
Yousafzai Faridoon K
Herr Alan J
Pikaard Craig S
Baulcombe David C
References (54)
54 references, click to expand
  1. An RNA-dependent RNA polymerase prevents meristem invasion by potato virus X and is required for the activity but not the production of a systemic silencing signal.
    Plant Physiol. 2005 Aug;138(4):1842-52 PMID: 16040651
  2. Evidence that siRNAs function as guides, not primers, in the Drosophila and human RNAi pathways.
    Mol Cell. 2002 Sep;10(3):537-48 PMID: 12408822
  3. Atypical RNA polymerase subunits required for RNA-directed DNA methylation.
    Nat Genet. 2005 Jul;37(7):761-5 PMID: 15924141
  4. Size-dependent cell-to-cell movement of defective interfering RNAs of Cymbidium ringspot virus.
    J Gen Virol. 2002 Jun;83(Pt 6):1505-10 PMID: 12029166
  5. Sequence and analysis of chromosome 3 of the plant Arabidopsis thaliana.
    Nature. 2000 Dec 14;408(6814):820-2 PMID: 11130713
  6. Evolution of the SNF2 family of proteins: subfamilies with distinct sequences and functions.
    Nucleic Acids Res. 1995 Jul 25;23(14):2715-23 PMID: 7651832
  7. The Arabidopsis chromatin-modifying nuclear siRNA pathway involves a nucleolar RNA processing center.
    Cell. 2006 Jul 14;126(1):79-92 PMID: 16839878
  8. Transitivity-dependent and -independent cell-to-cell movement of RNA silencing.
    EMBO J. 2003 Sep 1;22(17):4523-33 PMID: 12941703
  9. Analysis of the involvement of an inducible Arabidopsis RNA-dependent RNA polymerase in antiviral defense.
    Mol Plant Microbe Interact. 2003 Mar;16(3):206-16 PMID: 12650452
  10. Endogenous siRNAs derived from a pair of natural cis-antisense transcripts regulate salt tolerance in Arabidopsis.
    Cell. 2005 Dec 29;123(7):1279-91 PMID: 16377568
  11. Transgenes are dispensable for the RNA degradation step of cosuppression.
    Proc Natl Acad Sci U S A. 1998 Aug 4;95(16):9675-80 PMID: 9689140
  12. Proteomics.
    Annu Rev Biochem. 2003;72:783-812 PMID: 14527327
  13. The capacity of transgenic tobacco to send a systemic RNA silencing signal depends on the nature of the inducing transgene locus.
    Plant J. 2003 Jul;35(1):82-92 PMID: 12834404
  14. A SNF2-like protein facilitates dynamic control of DNA methylation.
    EMBO Rep. 2005 Jul;6(7):649-55 PMID: 15947783
  15. Cell-to-Cell, but not long-distance, spread of RNA silencing that is induced in individual epidermal cells.
    J Virol. 2004 Mar;78(6):3149-54 PMID: 14990735
  16. Involvement of putative SNF2 chromatin remodeling protein DRD1 in RNA-directed DNA methylation.
    Curr Biol. 2004 May 4;14(9):801-5 PMID: 15120073
  17. Secondary siRNAs result from unprimed RNA synthesis and form a distinct class.
    Science. 2007 Jan 12;315(5809):244-7 PMID: 17158288
  18. Finding nuclear localization signals.
    EMBO Rep. 2000 Nov;1(5):411-5 PMID: 11258480
  19. Phloem long-distance trafficking of GIBBERELLIC ACID-INSENSITIVE RNA regulates leaf development.
    Plant J. 2005 Apr;42(1):49-68 PMID: 15773853
  20. Role of RNA polymerase IV in plant small RNA metabolism.
    Proc Natl Acad Sci U S A. 2007 Mar 13;104(11):4536-41 PMID: 17360559
  21. Arabidopsis map-based cloning in the post-genome era.
    Plant Physiol. 2002 Jun;129(2):440-50 PMID: 12068090
  22. DICER-LIKE 4 is required for RNA interference and produces the 21-nucleotide small interfering RNA component of the plant cell-to-cell silencing signal.
    Nat Genet. 2005 Dec;37(12):1356-60 PMID: 16273107
  23. Arabidopsis micro-RNA biogenesis through Dicer-like 1 protein functions.
    Proc Natl Acad Sci U S A. 2004 Aug 24;101(34):12753-8 PMID: 15314213
  24. Enhancement of protein modeling by human intervention in applying the automatic programs 3D-JIGSAW and 3D-PSSM.
    Proteins. 2001;Suppl 5:39-46 PMID: 11835480
  25. Distinct populations of primary and secondary effectors during RNAi in C. elegans.
    Science. 2007 Jan 12;315(5809):241-4 PMID: 17124291
  26. An ARGONAUTE4-containing nuclear processing center colocalized with Cajal bodies in Arabidopsis thaliana.
    Cell. 2006 Jul 14;126(1):93-106 PMID: 16839879
  27. Genetic and functional diversification of small RNA pathways in plants.
    PLoS Biol. 2004 May;2(5):E104 PMID: 15024409
  28. Presence of ATG triplets in 5' untranslated regions of eukaryotic cDNAs correlates with a 'weak' context of the start codon.
    Bioinformatics. 2001 Oct;17(10):890-900 PMID: 11673233
  29. ARGONAUTE4 control of locus-specific siRNA accumulation and DNA and histone methylation.
    Science. 2003 Jan 31;299(5607):716-9 PMID: 12522258
  30. Large-scale sequencing reveals 21U-RNAs and additional microRNAs and endogenous siRNAs in C. elegans.
    Cell. 2006 Dec 15;127(6):1193-207 PMID: 17174894
  31. RNA commutes to work: regulation of plant gene expression by systemically transported RNA molecules.
    Bioessays. 2001 Dec;23(12):1087-90 PMID: 11746226
  32. HC-Pro suppression of transgene silencing eliminates the small RNAs but not transgene methylation or the mobile signal.
    Plant Cell. 2001 Mar;13(3):571-83 PMID: 11251097
  33. Endogenous targets of RNA-directed DNA methylation and Pol IV in Arabidopsis.
    EMBO J. 2006 Jun 21;25(12):2828-36 PMID: 16724114
  34. Two classes of short interfering RNA in RNA silencing.
    EMBO J. 2002 Sep 2;21(17):4671-9 PMID: 12198169
  35. A species of small antisense RNA in posttranscriptional gene silencing in plants.
    Science. 1999 Oct 29;286(5441):950-2 PMID: 10542148
  36. RNA polymerase IV directs silencing of endogenous DNA.
    Science. 2005 Apr 1;308(5718):118-20 PMID: 15692015
  37. Reinforcement of silencing at transposons and highly repeated sequences requires the concerted action of two distinct RNA polymerases IV in Arabidopsis.
    Genes Dev. 2005 Sep 1;19(17):2030-40 PMID: 16140984
  38. Systemic spread of sequence-specific transgene RNA degradation in plants is initiated by localized introduction of ectopic promoterless DNA.
    Cell. 1998 Oct 16;95(2):177-87 PMID: 9790525
  39. Systemic acquired silencing: transgene-specific post-transcriptional silencing is transmitted by grafting from silenced stocks to non-silenced scions.
    EMBO J. 1997 Aug 1;16(15):4738-45 PMID: 9303318
  40. RNA silencing in plants.
    Nature. 2004 Sep 16;431(7006):356-63 PMID: 15372043
  41. Partially redundant functions of Arabidopsis DICER-like enzymes and a role for DCL4 in producing trans-acting siRNAs.
    Curr Biol. 2005 Aug 23;15(16):1494-500 PMID: 16040244
  42. Phloem long-distance transport of CmNACP mRNA: implications for supracellular regulation in plants.
    Development. 1999 Oct;126(20):4405-19 PMID: 10498677
  43. Systemic signalling in gene silencing.
    Nature. 1997 Oct 9;389(6651):553 PMID: 9335491
  44. microRNA-directed phasing during trans-acting siRNA biogenesis in plants.
    Cell. 2005 Apr 22;121(2):207-21 PMID: 15851028
  45. Plant nuclear RNA polymerase IV mediates siRNA and DNA methylation-dependent heterochromatin formation.
    Cell. 2005 Mar 11;120(5):613-22 PMID: 15766525
  46. Initiation and maintenance of virus-induced gene silencing
    Plant Cell. 1998 Jun;10(6):937-46 PMID: 9634582
  47. A systemic small RNA signaling system in plants.
    Plant Cell. 2004 Aug;16(8):1979-2000 PMID: 15258266
  48. A diverse and evolutionarily fluid set of microRNAs in Arabidopsis thaliana.
    Genes Dev. 2006 Dec 15;20(24):3407-25 PMID: 17182867
  49. The Arabidopsis double-stranded RNA-binding protein HYL1 plays a role in microRNA-mediated gene regulation.
    Proc Natl Acad Sci U S A. 2004 Jan 27;101(4):1093-8 PMID: 14722360
  50. Structure of the SWI2/SNF2 chromatin-remodeling domain of eukaryotic Rad54.
    Nat Struct Mol Biol. 2005 Apr;12(4):350-6 PMID: 15806108
  51. A two-hit trigger for siRNA biogenesis in plants.
    Cell. 2006 Nov 3;127(3):565-77 PMID: 17081978
  52. Biochemical specialization within Arabidopsis RNA silencing pathways.
    Mol Cell. 2005 Aug 5;19(3):421-8 PMID: 16061187
  53. A simple and rapid method for the preparation of plant genomic DNA for PCR analysis.
    Nucleic Acids Res. 1991 Mar 25;19(6):1349 PMID: 2030957
  54. mRNA sequence features that contribute to translational regulation in Arabidopsis.
    Nucleic Acids Res. 2005 Feb 16;33(3):955-65 PMID: 15716313
Article Info
Journal
The Plant cell
Abbr.
Plant Cell
ISSN
1040-4651
Published
2007-05-00
Epub
2007-00-25
Pages
1507-21
Language
English
Region
England
NLM ID
9208688
PMCID
PMC1913737
Subset
IM
Grants
NIGMS NIH HHS · R01 GM077590 · United States
NIGMS NIH HHS · R01GM-077590 · United States
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