Research Article

Small Silencing RNAs in Plants Are Mobile and Direct Epigenetic Modification in Recipient Cells

Science  14 May 2010:
Vol. 328, Issue 5980, pp. 872-875
DOI: 10.1126/science.1187959

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siRNA Movement in Plant Tissues

Long-distance movement of RNA interference (RNAi)–derived signals in plants plays an important role in development and in defense against viral attack. The nature of the signals that spread from cell to cell is not known, although evidence suggests that they are nucleic acids of some sort (see the Perspective by Martienssen). Molnar et al. (p. 872, published online 22 April) and Dunoyer et al. (p. 912, published online 22 April) now show that in Arabidopsis, both exogenous and endogenous small interfering RNAs (siRNAs), rather than their long double-stranded precursor RNAs, are the molecules that transfer information between plant cells. A viral protein that counters RNAi though sequestering siRNAs blocked spreading of a transgene RNAi silencing signal. Furthermore, siRNA-processing enzymes were required in the source, and not the recipient, cells for spreading, and bombardment of plants with double-stranded siRNAs directly showed siRNA spread between cells. Endogenous siRNAs also spread between tissues and were capable of directing DNA methylation of target sequences in distant tissues.

Abstract

A silencing signal in plants with an RNA specificity determinant moves through plasmodesmata and the phloem. To identify the mobile RNA, we grafted Arabidopsis thaliana shoots to roots that would be a recipient for the silencing signal. Using mutants that block small RNA (sRNA) biogenesis in either source or recipient tissue, we found that transgene-derived sRNA as well as a substantial proportion of the endogenous sRNA had moved across the graft union, and we provide evidence that 24-nucleotide mobile sRNAs direct epigenetic modifications in the genome of the recipient cells. Mobile sRNA thus represents a mechanism for transmitting the specification of epigenetic modification and could affect genome defense and responses to external stimuli that have persistent effects in plants.

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