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

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.

References

[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

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

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

[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

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

[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

[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

[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

[9] 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

[10] 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

[11] 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

[12] 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

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

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

[15] 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

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

[17] 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

[18] 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

[19] 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

[20] 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

[21] 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

[22] 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

[23] 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

[24] 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

[25] 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

[26] 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

[27] 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

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

[29] 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

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

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

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

[33] 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

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

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

[36] 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

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

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

[39] 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

[40] 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

[41] 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

RIGHTS & PERMISSIONS

Higher Education Press and Springer-Verlag Berlin Heidelberg