Plasmodesmata (PD) are plasma membrane-lined cytoplasmic channels that cross the cell wall and establish symplasmic continuity between neighboring cells in plants. Recently, a wide range of cellular RNAs (including mRNAs and small RNAs (sRNAs)) have been reported to move from cell to cell through PD trafficking pathways. sRNAs are key molecules that function in transcriptional and post-transcriptional RNA silencing, which is a gene expression regulatory mechanism that is conserved among eukaryotes and is important for protection against invading nucleic acids (such as viruses and transposons) and for developmental and physiological regulation. One of the most intriguing aspects of RNA silencing is that it can function either cell autonomously or non-cell autonomously in post-transcriptional RNA silencing pathways. Although the mechanisms underlying cell-to-cell trafficking of RNA and RNA silencing signals are not fully understood, the movement of specific RNAs seems to play a critical role in cell-to-cell and long-distance regulation of gene expression, thereby coordinating growth and developmental processes, gene silencing, and stress responses. In this review, we summarize the current knowledge regarding cell-to-cell trafficking of RNA molecules (including small RNAs), and we discuss potential molecular mechanisms of cell-to-cell trafficking that are mediated by complex networks.
In plants, transgenes with inverted repeats are used to induce efficient RNA silencing, which is also frequently induced by highly transcribed sense transgenes. RNA silencing induced by sense transgenes is dependent on RNA-dependent RNA polymerase 6 (RDR6), which converts single-stranded (ss) RNA into double-stranded (ds) RNA. By contrast, it has been proposed that RNA silencing induced by self-complementary hairpin RNA (hpRNA) does not require RDR6, because the hpRNA can directly fold back on itself to form dsRNA. However, it is unclear whether RDR6 plays a role in hpRNA-induced RNA silencing by amplifying dsRNA to spread RNA silencing within the plant. To address the efficiency of hpRNA-induced RNA silencing in the presence or absence of RDR6, Wild type (WT, Col-0) and rdr6-11 Arabidopsis thaliana lines expressing green fluorescent protein (GFP) were generated and transformed with a GFP-RNA interference (RNAi) construct. Whereas most GFP-RNAi-transformed WT lines exhibited almost complete silencing of GFP expression in the T1 generation, various levels of GFP expression remained among the GFP-RNAi-transformed rdr6-11 lines. Homozygous expression of GFP-RNAi in the T3 generation was not sufficient to induce complete GFP silencing in several rdr6-11 lines. Our results indicate that RDR6 is required for efficient hpRNA-induced RNA silencing in plants. INTRODUCTIONGene silencing is a mechanism that employs small RNAs and protein effectors to interfere with the expression of homologous genes at the transcriptional and post-transcriptional levels (Voinnet, 2008). Transcriptional gene silencing (TGS), which takes place through repression of transcription, is often associated with methylation of the corresponding homologous promoter (Neuhuber et al., 1994;Park et al., 1996). Post-transcriptional gene silencing (PTGS), occurring through sequencespecific degradation of target mRNAs, is characterized by accumulation of small interfering RNA (siRNA) and methylation of target gene sequences (Depicker and Montagu, 1997;Vaucheret et al., 2001). Gene silencing was first discovered in plants and is highly conserved among multicellular eukaryotes. It initiates with the formation of dsRNA, which is subsequently processed into siRNA. siRNAs are produced from dsRNAs by an RNase III-like enzyme called DICER, which has dsRNA-binding, RNA helicase and P-element-induced wimpy testes (PIWI)-Argonaute (AGO)-Zwille (PAZ) domains (Bernstein et al., 2001). Plants possess four DICER homologs: DCL1, DCL2, DCL3, and DCL4. DCL1 is responsible for producing various sizes of microRNAs (small RNAs encoded in the genome), whereas DCL2, DCL3, and DCL4 produce 22, 24, and 21 nucleotide (nt) siRNAs, respectively (Bartel, 2004;Dunoyer et al., 2005;Xie et al., 2004). The 24 nt siRNAs are reported to guide RNAdirected DNA methylation (RdDM) in plants (Wassenegger et al., 1994), whereas the 21 and 22 nt siRNAs are known to trigger cognate mRNA degradation and secondary siRNA biogenesis, respectively (Chen et al., 2010;Hamilton et al., 2002).The guide str...
SummaryPhosphoinositides (PIs) are essential metabolites which are generated by various lipid kinases and rapidly respond to a variety of environmental stimuli in eukaryotes. One of the precursors of important regulatory PIs, phosphatidylinositol (PtdIn) 4-phosphate, is synthesized by PtdIns 4-kinases (PI4K). Despite its wide distribution in eukaryotes, its role in plants remains largely unknown. Here, we show that the activity of AtPI4Kc3 gene, an Arabidopsis (Arabidopsis thaliana) type II PtdIn 4-kinase, is regulated by DNA demethylation and some abiotic stresses. AtPI4Kc3 is targeted to the nucleus and selectively bounds to a few PtdIns. It possessed autophosphorylation activity but unexpectedly had no detectable lipid kinase activity. Overexpression of AtPI4Kc3 revealed enhanced tolerance to high salinity or ABA along with inducible expression of a host of stress-responsive genes and an optimal accumulation of reactive oxygen species. Furthermore, overexpressed AtPI4Kc3 augmented the salt tolerance of bzip60 mutants. The ubiquitin-like domain of AtPI4Kc3 is demonstrated to be essential for salt stress tolerance. Besides, AtPI4Kc3-overexpressed plants showed a late-flowering phenotype, which was caused by the regulation of some flowering pathway integrators. In all, our results indicate that AtPI4Kc3 is necessary for reinforcement of plant response to abiotic stresses and delay of the floral transition.
Plants possess dynamic networks of intercellular communication that are crucial for plant development and physiology. In plants, intercellular communication involves a combination of ligand-receptor-based apoplasmic signaling, and plasmodesmata and phloem-mediated symplasmic signaling. The intercellular trafficking of macromolecules, including RNAs and proteins, has emerged as a novel mechanism of intercellular communication in plants. Various forms of regulatory RNAs move over distinct cellular boundaries through plasmodesmata and phloem. This plant-specific, non-cell-autonomous RNA trafficking network is also involved in development, nutrient homeostasis, gene silencing, pathogen defense, and many other physiological processes. However, the mechanism underlying macromolecular trafficking in plants remains poorly understood. Current progress made in RNA trafficking research and its biological relevance to plant development will be summarized. Diverse plant regulatory mechanisms of cell-to-cell and systemic long-distance transport of RNAs, including mRNAs, viral RNAs, and small RNAs, will also be discussed.
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