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Intercellular and systemic spread of RNA and RNAi in plants

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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. WIREs RNA 2013, 4:279–293. doi: 10.1002/wrna.1160

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Figure 1.

Symplasmic communication channels in plant. A model for plasmodesmata is shown in median longitudinal (top) and transverse (bottom) views. The abbreviations are the following: CW, cell wall; DP, docking protein; ER, endoplasmic reticulum; IPM, inner plasma membrane leaflet; OPM, outer plasma membrane leaflet; PDP, plasmodesmal proteins; PM, plasma membrane. (Reprinted with permission from Ref 17. Copyright 2001 Nature publishing group; Reprinted with permission from Ref 18. Copyright 2006 Elsevier Ltd)

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Figure 2.

A model describing the two mechanisms involved in the movement proteins mediated cell‐to‐cell movement of PVX and TMV. In PVX (lower part), TGBp2 and TGBp3 form a vesicle protein complex that binds to the TGBp1–viral RNA complex and moves along the endoplasmic reticulum network using actin filaments. TGBp3 directs the targeting to plasmodesmata, and the TGBp1–viral RNA complex interacts with the plasmodesmal trafficking machinery for its intercellular delivery. Finally, the TGBp2–TGBp3 complex is recycled by the endocytic pathway. In TMV (upper part), viral RNA complex assembly might require a network of microtubules. Actin‐driven endoplasmic reticulum motility is essential for intracellular and intercellular delivery of movement proteins–viral RNA complexes with TMV‐replicase. (Reprinted with permission from Ref 18. Copyright 2006 Elsevier Ltd; Reprinted with permission from Ref 41. Copyright 2010 Springer Ltd)

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Figure 3.

A simplified model for endogenous, mRNA trafficking mechanism acting via the phloem to regulate plant development. (a) The gibberellic acid insensitive (GAI) RNA regulates leaf morphology in Arabidopsis, tomato and pumpkin, (b, d) NAC (a member of NAC domain gene family) RNA controls shoot and root apical meristem development in pumpkin, (c) Movement of BEL1 transcription factor (BEL5) mRNA from leaf to stolon tip facilitates tuber formation in potato, and (e) mobile arabidopsis thaliana centroradialis homolog (ATC), and flowering locus T (FT), FVE, agamous‐like24 (AGL24) RNA negative and positively regulate floral induction respectively in Arabidopsis.

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Figure 4.

A simple model for cell‐to‐cell, local and extensive RNAi movement in plants. (a) PolII‐mediated, IR transgene‐derived dsRNAs are diced into 21‐nt siRNA by DCL4, which acts through AGO1 to direct target cleavage. The 21‐nt siRNA, dsRNA or aberrant mRNA might traffic into neighboring 10–15 cells to trigger silencing machinery through plasmodesmata by an unknown mechanism. PolIVa/NRPD1a, RDR2, CLSY1, and JMJ14 were reported to be involved in the modification of the signal in donor or recipient cells via this local silencing pathway. (b) An unknown signal(s) could be amplified by RDR6 to generate new dsRNA, which is processed by the silencing machinery. This process could be reiterated to induce extensive silencing spreads (more than 10–15 cells) in Arabidopsis through the plasmodesmata. DCL3 and AGO4 might be required for the reception of graft‐transmissible signal(s) from the root stock to the scion. (Reprinted with permission from Ref 72. Copyright 2011 Institute of Plant and Microbial Biology)

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Figure 5.

A proposed model for signal communication between roots and shoots to regulate miR399 and phosphate2 (PHO2) upon phosphate starvation. Details in text. SRS, systemic root‐born signal; SSS, systemic shoot‐born signal; LRS, local root‐born signal. (Reprinted with permission from Ref 66. Copyright 2009 American Society of Plant Biologists)

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