REVIEW

Mobile silencing in plants: what is the signal and what defines the target

  • Dacheng LIANG 1 ,
  • E. Jean FINNEGAN 1 ,
  • Elizebeth S. DENNIS 1 ,
  • Peter M. WATERHOUSE 2 ,
  • Ming-Bo WANG , 1
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  • 1. CSIRO Plant Industry, Clunies Ross Street, Canberra, ACT 2601, Australia
  • 2. School of Molecular Bioscience, University of Sydney, Sydney NSW 2006, Australia

Received date: 15 Feb 2011

Accepted date: 01 Mar 2011

Published date: 01 Apr 2011

Copyright

2014 Higher Education Press and Springer-Verlag Berlin Heidelberg

Abstract

RNA-mediated silencing in plants can spread from cell to cell and over a long distance, and such mobile silencing has been extensively studied in the past decade. However, major questions remain as to what is the exact nature of the mobile silencing signals, how the components of the RNA-directed DNA methylation pathway are involved, and why systemic spread of silencing has only been observed for transgenes but not endogenous genes. In this review, we provide an overview of the current knowledge on mobile gene silencing in plants and present a model where systemic silencing involves long nuclear RNA transcripts that serve as a template to amplify primary siRNA signals.

Cite this article

Dacheng LIANG , E. Jean FINNEGAN , Elizebeth S. DENNIS , Peter M. WATERHOUSE , Ming-Bo WANG . Mobile silencing in plants: what is the signal and what defines the target[J]. Frontiers in Biology, 2011 , 6(2) : 140 -146 . DOI: 10.1007/s11515-011-1145-3

1
Allen E, Xie Z, Gustafson A M, Carrington J C (2005). microRNA-directed phasing during trans-acting siRNA biogenesis in plants. Cell, 121(2): 207–221

DOI PMID

2
Bagasra O, Prilliman K R (2004). RNA interference: the molecular immune system. J Mol Histol, 35(6): 545–553

DOI PMID

3
Baulcombe D (2004). RNA silencing in plants. Nature, 431(7006): 356–363

DOI PMID

4
Brosnan C A, Mitter N, Christie M, Smith N A, Waterhouse P M, Carroll B J (2007). Nuclear gene silencing directs reception of long-distance mRNA silencing in Arabidopsis. Proc Natl Acad Sci USA, 104(37): 14741–14746

DOI PMID

5
Chinnusamy V, Zhu J K (2009). Epigenetic regulation of stress responses in plants. Curr Opin Plant Biol, 12(2): 133–139

DOI PMID

6
Crete P, Leuenberger S, Iglesias V A, Suarez V, Schöb H, Holtorf H, van Eeden S, Meins F Jr (2001). Graft transmission of induced and spontaneous post-transcriptional silencing of chitinase genes. Plant J, 28(5): 493–501

DOI PMID

7
Daxinger L, Kanno T, Bucher E, van der Winden J, Naumann U, Matzke A J, Matzke M (2009). A stepwise pathway for biogenesis of 24-nt secondary siRNAs and spreading of DNA methylation. EMBO J, 28(1): 48–57

DOI PMID

8
Dunoyer P, Brosnan C A, Schott G, Wang Y, Jay F, Alioua A, Himber C, Voinnet O (2010b). An endogenous, systemic RNAi pathway in plants. EMBO J, 29(10): 1699–1712

DOI PMID

41
Dunoyer P, Himber C, Ruiz-Ferrer V, Alioua A, Voinnet O (2007). Intra- and intercellular RNA interference in Arabidopsis thaliana requires component of the microRNA and heterochromatic silencing pathways. Nat Genet, 39(7): 848–856

DOI PMID

9
Dunoyer P, Himber C, Voinnet O (2005). 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, 37(12): 1356–1360

DOI PMID

10
Dunoyer P, Schott G, Himber C, Meyer D, Takeda A, Carrington J C, Voinnet O (2010a). Small RNA duplexes function as mobile silencing signals between plant cells. Science, 328(5980): 912–916

DOI PMID

11
Fusaro A F, Matthew L, Smith N A, Curtin S J, Dedic-Hagan J, Ellacott G A, Watson J M, Wang M B, Brosnan C, Carroll B J, Waterhouse P M (2006). RNA interference-inducing hairpin RNAs in plants act through the viral defence pathway. EMBO Rep, 7(11): 1168–1175

DOI PMID

12
Hamilton A J, Baulcombe D C (1999). A species of small antisense RNA in posttranscriptional gene silencing in plants. Science, 286(5441): 950–952

DOI PMID

13
Herr A J, Baulcombe D C (2004). RNA silencing pathways in plants. Cold Spring Harb Symp Quant Biol, 69(1): 363–370

DOI PMID

14
Himber C, Dunoyer P, Moissiard G, Ritzenthaler C, Voinnet O (2003). Transitivity-dependent and -independent cell-to-cell movement of RNA silencing. EMBO J, 22(17): 4523–4533

DOI PMID

15
Kalantidis K, Schumacher H T, Alexiadis T, Helm J M (2008). RNA silencing movement in plants. Biol cell, 100(1): 13–26

16
Klahre U, Crété P, Leuenberger S A, Iglesias V A, Meins F Jr (2002). High molecular weight RNAs and small interfering RNAs induce systemic posttranscriptional gene silencing in plants. Proc Natl Acad Sci USA, 99(18): 11981–11986

DOI PMID

17
Lakatos L, Csorba T, Pantaleo V, Chapman E J, Carrington J C, Liu Y P, Dolja V V, Calvino L F, López-Moya J J, Burgyán J (2006). Small RNA binding is a common strategy to suppress RNA silencing by several viral suppressors. EMBO J, 25(12): 2768–2780

DOI PMID

18
Law J A, Jacobsen S E (2010). Establishing, maintaining and modifying DNA methylation patterns in plants and animals. Nat Rev Genet, 11(3): 204–220

DOI PMID

19
Mallory A C, Ely L, Smith T H, Marathe R, Anandalakshmi R, Fagard M, Vaucheret H, Pruss G, Bowman L, Vance V B (2001). HC-Pro suppression of transgene silencing eliminates the small RNAs but not transgene methylation or the mobile signal. Plant Cell, 13(3): 571–583

PMID

20
Metzlaff M, O’Dell M, Cluster P D, Flavell R B (1997). RNA-mediated RNA degradation and chalcone synthase A silencing in petunia. Cell, 88(6): 845–854

DOI PMID

21
Mlotshwa S, Voinnet O, Mette M F, Matzke M, Vaucheret H, Ding S W, Pruss G, Vance V B (2002). RNA silencing and the mobile silencing signal. Plant Cell, 14(Suppl): S289–S301

PMID

22
Molnar A, Melnyk C W, Bassett A, Hardcastle T J, Dunn R, Baulcombe D C (2010). Small silencing RNAs in plants are mobile and direct epigenetic modification in recipient cells. Science, 328(5980): 872–875

DOI PMID

23
Palauqui J C, Elmayan T, Pollien J M, Vaucheret H (1997). Systemic acquired silencing: transgene-specific post-transcriptional silencing is transmitted by grafting from silenced stocks to non-silenced scions. EMBO J, 16(15): 4738–4745

DOI PMID

24
Roberts A G, Cruz S S, Roberts I M, Prior D, Turgeon R, Oparka K J (1997). Phloem unloading in sink leaves of Nicotiana benthamiana: Comparison of a fluorescent solute with a fluorescent virus. Plant Cell, 9(8): 1381–1396

DOI PMID

25
Shaharuddin N A, Han Y, Li H, Grierson D (2006). The mechanism of graft transmission of sense and antisense gene silencing in tomato plants. FEBS Lett, 580(28-29): 6579–6586

DOI PMID

26
Smith L M, Pontes O, Searle I, Yelina N, Yousafzai F K, Herr A J, Pikaard C S, Baulcombe D C (2007). An SNF2 protein associated with nuclear RNA silencing and the spread of a silencing signal between cells in Arabidopsis. Plant Cell, 19(5): 1507–1521

DOI PMID

27
Tijsterman M, Plasterk R H (2004). Dicers at RISC; the mechanism of RNAi. Cell, 117(1): 1–3

DOI PMID

28
Vaistij F E, Jones L, Baulcombe D C (2002). Spreading of RNA targeting and DNA methylation in RNA silencing requires transcription of the target gene and a putative RNA-dependent RNA polymerase. Plant Cell, 14(4): 857–867

DOI PMID

29
Voinnet O (2005). Non-cell autonomous RNA silencing. FEBS Lett, 579(26): 5858–5871

DOI PMID

30
Voinnet O (2008). Use, tolerance and avoidance of amplified RNA silencing by plants. Trends Plant Sci, 13(7): 317–328

DOI PMID

31
Voinnet O, Baulcombe D C (1997). Systemic signalling in gene silencing. Nature, 389(6651): 553

DOI PMID

32
Voinnet O, Vain P, Angell S, Baulcombe D C (1998). Systemic spread of sequence-specific transgene RNA degradation in plants is initiated by localized introduction of ectopic promoterless DNA. Cell, 95(2): 177–187

DOI PMID

33
Wang M B, Dennis E S (2009). SPT5-like, a new component in plant RdDM. EMBO Rep, 10(6): 573–575

DOI PMID

34
Wang M B, Metzlaff M (2005). RNA silencing and antiviral defense in plants. Curr Opin Plant Biol, 8(2): 216–222

DOI PMID

35
Wang M B, Waterhouse P M (2000). High-efficiency silencing of a β-glucuronidase gene in rice is correlated with repetitive transgene structure but is independent of DNA methylation. Plant Mol Biol, 43(1): 67–82

DOI PMID

36
Wassenegger M, Krczal G (2006). Nomenclature and functions of RNA-directed RNA polymerases. Trends Plant Sci, 11(3): 142–151

DOI PMID

37
Waterhouse P M, Wang M B, Finnegan E J (2001). Role of short RNAs in gene silencing. Trends Plant Sci, 6(7): 297–301

DOI PMID

38
Xie Z, Johansen L K, Gustafson A M, Kasschau K D, Lellis A D, Zilberman D, Jacobsen S E, Carrington J C (2004). Genetic and functional diversification of small RNA pathways in plants. PLoS Biol, 2(5): E104

DOI PMID

39
Yoshikawa M, Peragine A, Park M Y, Poethig R S (2005). A pathway for the biogenesis of trans-acting siRNAs in Arabidopsis. Genes Dev, 19(18): 2164–2175

DOI PMID

40
Zhang B, Pan X, Cobb G P, Anderson T A (2006). Plant microRNA: a small regulatory molecule with big impact. Dev Biol, 289(1): 3–16

DOI PMID

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