Intercellular and systemic trafficking of RNAs in plants

Abstract

Plants have evolved dynamic and complex networks of cell-to-cell communication to coordinate and adapt their growth and development to a variety of environmental changes. In addition to small molecules, such as metabolites and phytohormones, macromolecules such as proteins and RNAs also act as signalling agents in plants. As information molecules, RNAs can move locally between cells through plasmodesmata, and over long distances through phloem. Non-cell-autonomous RNAs may act as mobile signals to regulate plant development, nutrient allocation, gene silencing, antiviral defence, stress responses and many other physiological processes in plants. Recent work has shed light on mobile RNAs and, in some cases, uncovered their roles in intercellular and systemic signalling networks. This review summarizes the current knowledge of local and systemic RNA movement, and discusses the potential regulatory mechanisms and biological significance of RNA trafficking in plants.

Fig. 1 |. Routes for RNA trafficking between plant cells.

a, PD as micro-channels for cell-to-cell movement of mobile molecules. PD are membrane-lined channels that traverse the cell wall and connect neighbouring cells. Cell wall, plasma membrane, endoplasmic reticulum (ER), desmotubule and callose are indicated. Red circles represent soluble molecules capable of moving through the desmotubule or cytoplasmic sleeve of PD. b, Phloem as a conduit for long-distance movement of molecules. Phloem is composed of stacked enucleated sieve elements assisted by companion cells. Mature sieve elements are connected to adjacent companion cells by highly modified and funnel-like plasmodesmata pore units (PPUs). Mobile molecules (red circles) are primarily transported from source to sink tissues over long distances through phloem. Arrows indicate the direction of movement. Gaps in the line indicate multiple, stacked sieve elements (one cell in the diagram) mediating long-distance transport. c, Putative vesicle-mediated RNA trafficking in plants. Vesicles containing RNAs are taken into MVBs, which subsequently fuse with the plasma membrane and release their intraluminal vesicles into the extracellular space as exosomes. These exosomes fuse with the plasma membrane of the recipient cell through endocytosis and unload the cargo RNAs. Alternatively, vesicles may transport RNAs to adjacent cells, either through exocytosis/endocytosis or through the PD channels between cells. Note that these are purely hypothetical events, as indicated by dashed lines in the diagram.

Fig. 2 |. Schematic drawing of non-cell-autonomous RNA silencing in plants.

SiRNAs (red) and miRNAs (blue) can act as mobile signals and move from cell to cell or over long distances to mediate non-cell-autonomous RNA silencing in plants. In the destination cells, siRNAs mediate RNA-directed DNA methylation or guide the cleavage of target RNAs, whereas miRNAs guide the cleavage or translational repression of target mRNAs. Filled orange circles indicate methyl groups on DNA or histones.

Fig. 3 |. Dynamic network of intercellular communication.

A hypothetical model of how RNA trafficking influences plant development and physiological processes. Internal or external stimuli may trigger the movement of plant RNAs, including mRNAs, siRNAs, miRNAs, rRNAs and tRNAs, from their synthesis sites (incipient cells) to distant tissues (recipient cells). These mobile RNAs may act non-cell-autonoumously. In the recipient cells, mRNAs, rRNAs and tRNAs may participate in translation, while miRNAs and siRNAs may mediate the silencing and regulation of genes. These mobile RNAs may therefore act as signalling molecules for intercellular information exchange to regulate plant development, nutrient allocation, stress responses and many other physiological processes in plants.