Home LiteratureArticle Details
PMID: 16924537 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

A single transgene locus triggers both transcriptional and post-transcriptional silencing through double-stranded RNA production.

Planta ·Vol. 225 ·No. 2 ·2007-01-00 ·Pages 365-79

Mourrain P, van Blokland R, Kooter JM, Vaucheret H

Abstract

Silencing of a target locus by an unlinked silencing locus can result from transcription inhibition (transcriptional gene silencing; TGS) or mRNA degradation (post-transcriptional gene silencing; PTGS), owing to the production of double-stranded RNA (dsRNA) corresponding to promoter or transcribed sequences, respectively. The involvement of distinct cellular components in each process suggests that dsRNA-induced TGS and PTGS likely result from the diversification of an ancient common mechanism. However, a strict comparison of TGS and PTGS has been difficult to achieve because it generally relies on the analysis of distinct silencing loci. We describe a single transgene locus that triggers both TGS and PTGS, owing to the production of dsRNA corresponding to promoter and transcribed sequences of different target genes. We describe mutants and epigenetic variants derived from this locus and propose a model for the production of dsRNA. Also, we show that PTGS, but not TGS, is graft-transmissible, which together with the sensitivity of PTGS, but not TGS, to RNA viruses that replicate in the cytoplasm, suggest that the nuclear compartmentalization of TGS is responsible for cell-autonomy. In contrast, we contribute local and systemic trafficking of silencing signals and sensitivity to viruses to the cytoplasmic steps of PTGS and to amplification steps that require high levels of target mRNAs.

MeSH Terms
Epistasis, Genetic Gene Expression Regulation, Plant Gene Silencing Nitrite Reductases/genetics Plant Leaves/genetics Plants, Genetically Modified RNA, Double-Stranded/biosynthesis,genetics,metabolism Tobacco/genetics Transgenes/genetics
Chemicals
RNA, Double-Stranded Nitrite Reductases
Authors & Affiliations
4 authors, click to expand affiliations / ORCID
Mourrain Philippe
Laboratoire de Biologie Cellulaire, Institut Jean-Pierre Bourgin, INRA, 78026, Versailles Cedex, France.
van Blokland Rik
Kooter Jan M
Vaucheret Hervé
References (45)
45 references, click to expand
  1. Resistance of RNA-mediated TGS to HC-Pro, a viral suppressor of PTGS, suggests alternative pathways for dsRNA processing.
    Curr Biol. 2001 Jul 24;11(14):1119-23 PMID: 11509235
  2. Potent and specific genetic interference by double-stranded RNA in Caenorhabditis elegans.
    Nature. 1998 Feb 19;391(6669):806-11 PMID: 9486653
  3. Transcriptional silencing and promoter methylation triggered by double-stranded RNA.
    EMBO J. 2000 Oct 2;19(19):5194-201 PMID: 11013221
  4. RNA target sequences promote spreading of RNA silencing.
    Plant Physiol. 2003 Jan;131(1):245-53 PMID: 12529532
  5. SGS3 and SGS2/SDE1/RDR6 are required for juvenile development and the production of trans-acting siRNAs in Arabidopsis.
    Genes Dev. 2004 Oct 1;18(19):2368-79 PMID: 15466488
  6. Expression of a truncated tomato polygalacturonase gene inhibits expression of the endogenous gene in transgenic plants.
    Mol Gen Genet. 1990 Dec;224(3):477-81 PMID: 2266949
  7. DNA methylation and chromatin structure affect transcriptional and post-transcriptional transgene silencing in Arabidopsis.
    Curr Biol. 2000 Dec 14-28;10(24):1591-4 PMID: 11137011
  8. Sequence homology requirements for transcriptional silencing of 35S transgenes and post-transcriptional silencing of nitrite reductase (trans)genes by the tobacco 271 locus.
    Plant Mol Biol. 1996 Dec;32(6):1075-83 PMID: 9002606
  9. 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
  10. Introduction of a Chimeric Chalcone Synthase Gene into Petunia Results in Reversible Co-Suppression of Homologous Genes in trans.
    Plant Cell. 1990 Apr;2(4):279-289 PMID: 12354959
  11. Flavonoid genes in petunia: addition of a limited number of gene copies may lead to a suppression of gene expression.
    Plant Cell. 1990 Apr;2(4):291-9 PMID: 2152117
  12. Perspective: machines for RNAi.
    Genes Dev. 2005 Mar 1;19(5):517-29 PMID: 15741316
  13. Fertile hypomorphic ARGONAUTE (ago1) mutants impaired in post-transcriptional gene silencing and virus resistance.
    Plant Cell. 2002 Mar;14(3):629-39 PMID: 11910010
  14. Plant viral suppressors of RNA silencing.
    Virus Res. 2004 Jun 1;102(1):97-108 PMID: 15068885
  15. The complex interplay between plant viruses and host RNA-silencing pathways.
    Curr Opin Plant Biol. 2005 Aug;8(4):415-23 PMID: 15939663
  16. Post-transcriptional small RNA pathways in plants: mechanisms and regulations.
    Genes Dev. 2006 Apr 1;20(7):759-71 PMID: 16600909
  17. Nitrite reductase silencing as a tool for selecting spontaneous haploid plants.
    Plant Cell Rep. 1995 Jan;15(1-2):12-6 PMID: 24185645
  18. Graft transmission of induced and spontaneous post-transcriptional silencing of chitinase genes.
    Plant J. 2001 Dec;28(5):493-501 PMID: 11849590
  19. RNA silencing in plants--defense and counterdefense.
    Science. 2001 Jun 22;292(5525):2277-80 PMID: 11423650
  20. Genetic and functional diversification of small RNA pathways in plants.
    PLoS Biol. 2004 May;2(5):E104 PMID: 15024409
  21. Reversible methylation and inactivation of marker genes in sequentially transformed tobacco plants.
    EMBO J. 1989 Mar;8(3):643-9 PMID: 16453872
  22. A pathway for the biogenesis of trans-acting siRNAs in Arabidopsis.
    Genes Dev. 2005 Sep 15;19(18):2164-75 PMID: 16131612
  23. Epigenetic changes in the expression of the maize A1 gene in Petunia hybrida: role of numbers of integrated gene copies and state of methylation.
    Mol Gen Genet. 1990 Jul;222(2-3):329-36 PMID: 1703268
  24. ARGONAUTE4 control of locus-specific siRNA accumulation and DNA and histone methylation.
    Science. 2003 Jan 31;299(5607):716-9 PMID: 12522258
  25. Virus resistance and gene silencing in plants can be induced by simultaneous expression of sense and antisense RNA.
    Proc Natl Acad Sci U S A. 1998 Nov 10;95(23):13959-64 PMID: 9811908
  26. Transcriptional and posttranscriptional gene silencing are mechanistically related.
    Curr Biol. 2001 Mar 20;11(6):436-40 PMID: 11301254
  27. Plant viral suppressors of post-transcriptional silencing do not suppress transcriptional silencing.
    Plant J. 2000 Apr;22(1):51-9 PMID: 10792820
  28. Inhibition of tobacco nitrite reductase activity by expression of antisense RNA.
    Plant J. 1992 Jul;2(4):559-69 PMID: 1285356
  29. Microgranular cellulose improves dsRNA recovery from plant nucleic acid extracts.
    Biotechniques. 1997 Oct;23(4):610-1 PMID: 9343672
  30. Molecular and genetic analysis of nitrite reductase co-suppression in transgenic tobacco plants.
    Mol Gen Genet. 1995 Aug 21;248(3):311-7 PMID: 7565593
  31. Endogenous trans-acting siRNAs regulate the accumulation of Arabidopsis mRNAs.
    Mol Cell. 2004 Oct 8;16(1):69-79 PMID: 15469823
  32. RNA polymerase IV directs silencing of endogenous DNA.
    Science. 2005 Apr 1;308(5718):118-20 PMID: 15692015
  33. 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
  34. 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
  35. Gene silencing mediated by promoter homology occurs at the level of transcription and results in meiotically heritable alterations in methylation and gene activity.
    Plant J. 1996 Feb;9(2):183-94 PMID: 8820605
  36. Production of aberrant promoter transcripts contributes to methylation and silencing of unlinked homologous promoters in trans.
    EMBO J. 1999 Jan 4;18(1):241-8 PMID: 9878066
  37. 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
  38. RNA silencing genes control de novo DNA methylation.
    Science. 2004 Feb 27;303(5662):1336 PMID: 14988555
  39. Arabidopsis mutants impaired in cosuppression.
    Plant Cell. 1998 Oct;10(10):1747-58 PMID: 9761800
  40. Distinct mechanisms determine transposon inheritance and methylation via small interfering RNA and histone modification.
    PLoS Biol. 2003 Dec;1(3):E67 PMID: 14691539
  41. RNA-directed transcriptional gene silencing in plants can be inherited independently of the RNA trigger and requires Met1 for maintenance.
    Curr Biol. 2001 May 15;11(10):747-57 PMID: 11378384
  42. The action of ARGONAUTE1 in the miRNA pathway and its regulation by the miRNA pathway are crucial for plant development.
    Genes Dev. 2004 May 15;18(10):1187-97 PMID: 15131082
  43. DICER-LIKE 4 functions in trans-acting small interfering RNA biogenesis and vegetative phase change in Arabidopsis thaliana.
    Proc Natl Acad Sci U S A. 2005 Sep 6;102(36):12984-9 PMID: 16129836
  44. Specific and heritable genetic interference by double-stranded RNA in Arabidopsis thaliana.
    Proc Natl Acad Sci U S A. 2000 Apr 25;97(9):4985-90 PMID: 10781109
  45. Transposon silencing in the Caenorhabditis elegans germ line by natural RNAi.
    Nature. 2003 Nov 20;426(6964):310-4 PMID: 14628056
Article Info
Journal
Planta
Abbr.
Planta
ISSN
0032-0935
Published
2007-01-00
Epub
2006-00-19
Pages
365-79
Language
English
Region
Germany
NLM ID
1250576
Subset
IM
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