Intercellular and systemic movement of RNA silencing signals

Abstract

In most eukaryotes, double-stranded RNA is processed into small RNAs that are potent regulators of gene expression. This gene silencing process is known as RNA silencing or RNA interference (RNAi) and, in plants and nematodes, it is associated with the production of a mobile signal that can travel from cell-to-cell and over long distances. The sequence-specific nature of systemic RNA silencing indicates that a nucleic acid is a component of the signalling complex. Recent work has shed light on the mobile RNA species, the genes involved in the production and transport of the signal. This review discusses the advances in systemic RNAi and presents the current challenges and questions in this rapidly evolving field.

Figure 1

sRNA movement in Arabidopsis. sRNAs produced in photosynthetic source tissues such as the leaves move to growing points and photosynthetic sinks through the phloem, the tissue that carries proteins, hormones and nucleic acids (Lough and Lucas, 2006). The phloem contains two cell types, the enucleated sieve elements, which are porous and allow movement of solutes, and the phloem companion cells, which support the sieve elements. The xylem transports water and ions. sRNAs unload from the phloem and move from cell-to-cell through plasmodesmata. Some 21 nt miRNAs are likely mobile and cleave complementary mRNAs (Pant et al, 2008; Carlsbecker et al, 2010) whereas mobile 24 nt siRNAs direct DNA methylation (Molnar et al, 2010) and 21 nt siRNAs target RNAs for degradation (Chitwood et al, 2009). The parenchyma represents the bulk of the plant tissue. The mesophyll parenchyma is present in leaves and is the site of photosynthesis.

Figure 2

The genetic requirements of siRNA movement in Arabidopsis. siRNAs generated by DCL3 or DCL4 likely move from cell-to-cell through plasmodesmata and long distances through the phloem. Mobile 21 nt siRNAs associate with AGO1 to direct posttranscriptional gene silencing (Dunoyer et al, 2005, 2007, 2010b), whereas mobile 24 nt siRNAs may associate with AGO4, 6 or 9 to direct DNA methylation (Me) or other chromatin marks associated with transcriptional gene silencing (Zilberman et al, 2003; Havecker et al, 2010). Either sRNA can likely initiate signal amplification in recipient tissues via the action of RNA Polymerase IV and/or RDRs (Schwach et al, 2005; Brosnan et al, 2007). The contribution of long RNAs to systemic RNA silencing in plants is unknown.