Key Points
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Plasmodesmata are plant-unique intercellular communication channels that acquired the capacity to dilate significantly to allow the trafficking of proteins and RNA within a symplasmic domain. This property is thought to contribute to the supracellular nature of plants.
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A subset of proteins that regulate the signalling processes beyond the cells in which they are synthesized can traffic through plasmodesmata to function as non-cell-autonomous proteins (NCAPs).
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One mode of trafficking through plasmodesmata might be controlled by a gate open/gate closed (GO/GC) pathway that leads to the formation of symplasmic domains in which certain unbound molecules (up to ∼40 kDa) can diffuse between neighbouring cells. A second, selective, mode of trafficking through plasmodesmata might involve a specific interaction between each NCAP and the plasmodesmal machinery.
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Intercellular trafficking of transcription factors that regulate developmental patterning and/or cell-fate determination underscores the important role carried out by the NCAP pathway.
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RNA can function both as a local and a long-distance information macromolecule by trafficking between cells through plasmodesmata and between organs through the vascular conduit that is provided by phloem. Specific mRNA molecules that can move through phloem might enter various meristematic tissues to redirect developmental events.
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Phloem translocation has important roles in transmitting RNA-interference signals and systemic signals in response to wounds and pathogen attacks, and in coordinating plant nitrogen metabolism and symbiosis. The formation of a new symplasmic domain between the phloem and a nodule initial illustrates the operation of the integrated signalling system that is provided by plasmodesmata and phloem.
Abstract
The evolution of intercellular communication had an important role in the increasing complexity of both multicellular and supracellular organisms. Plasmodesmata, the intercellular organelles of the plant kingdom, establish an effective pathway for local and long-distance signalling. In higher plants, this pathway involves the trafficking of proteins and various forms of RNA that function non-cell-autonomously to affect developmental programmes.
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Acknowledgements
Our thanks go to colleagues who provided unpublished work for inclusion in this review and especially to J. Bowman, B. Scheres and T.-S. Yu for providing unpublished photomicrographs. We apologize to all those whose work could not be discussed due to space limitations. Work in our laboratory on plasmodesmata and the supracellular nature of plants is supported by grants from the Department of Energy Office of Basic Energy Sciences and the National Science Foundation.
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Glossary
- CELL–CELL COMMUNICATION
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Signalling that occurs through the release of a ligand into the extracellular milieu. From there, it can diffuse and bind to its membrane-bound receptor to activate a specific signal cascade within the target cell.
- NUCLEAR PORE COMPLEX
-
A large multiprotein complex that forms a channel in the nuclear envelope of eukaryotic cells. It joins the inner and outer nuclear membranes and allows transport of proteins and nucleic acids to and from the nucleus.
- METABOLITES
-
Small molecules (100–500 Da), such as simple sugars, organic acids and amino acids, that participate in biochemical and/or physiological processes that occur within the cell.
- SYMPLASMIC DOMAIN
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The confinement of molecular exchange by a cytoplasmic continuum to a discrete field of cells.
- GAP JUNCTION
-
Communicating junction (normally permeant to molecules of up to 3 kDa) between adjacent cells. It is composed of 12 connexin protein subunits — each of the coupled cells contributes a connexon, or hemichannel, that is formed from 6 connexin subunits.
- CELL-TO-CELL COMMUNICATION
-
Signalling that involves the direct movement of an information molecule into the cytoplasm of neighbouring cells without entry into the extracellular milieu. This pathway involves gap junctions in animals and plasmodesmata in plants and algae.
- RIBONUCLEOPROTEIN (RNP) COMPLEX
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A complex of protein and RNA. In many cases, the proteins can recognize their cognate mRNA molecules (selective binding) and mediate their delivery to specific regions within the cell.
- SUPRACELLULAR ORGANISMS
-
Organs of these complex organisms consist of populations of cells, but almost every cell is interconnected by plasmodesmata to its nearest neighbours. As the phloem interconnects all symplasmic domains in the plant, such a system of organization works above the level of the cell, hence the term 'supracellular'.
- NON-CELL-AUTONOMOUS PROTEINS (NCAPS)
-
Plant proteins that move between cells using either the cell–cell or cell-to-cell pathway. Examples include small ligands that diffuse through the extracellular milieu and bind to receptors that are located in the plasma membrane, and transcription factors that enter the nuclei of neighbouring cells to participate in cell-fate determination.
- NON-CELL-AUTONOMOUS PROTEIN PATHWAY
-
(NCAP pathway). The route along which NCAPs move between cells. The components of this pathway can include structural elements within the cytoplasm (for example, the cytoskeleton), carriers/chaperones, plasmodesmal docking proteins, structural constituents of the plasmodesmata and regulatory proteins (such as protein kinases).
- MICROINJECTION
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A method that is used to introduce a range of test molecules into the cytoplasm of living cells. In plants, this technique has provided a powerful tool to explore, directly, the capacity of a protein (or fluorescent molecule) to be transported from cell to cell through plasmodesmata.
- GREEN FLUORESCENT PROTEIN
-
A heterologous protein from Aequorea victoria (jellyfish) that is used to study NCAP trafficking through plasmodesmata. It is also used to trace the movement of a tagged protein both within the cell and during intercellular trafficking.
- INFLORESCENCE STEM
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The stem that carries the flowers.
- SHOOT APICAL MERISTEM
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The vegetative apex of a plant consists of a group of stem cells (or initials) that form the shoot apical meristem, together with the lateral organs — leaf primordia, vascular initials, axillary buds and the stem — that are derived from these cells.
- MOVEMENT PROTEIN
-
A virally-encoded protein that binds to viral RNA/DNA to mediate the cell-to-cell trafficking of the infectious component of the viral genome. Endogenous NCAPs can also be referred to as movement proteins.
- PROTOPLAST
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An osmotically sensitive plant cell that lacks its cell wall but still has its plasma membrane.
- XYLEM
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Vascular tissue that delivers water and mineral nutrients, which are taken up by the root system, to vegetative organs. It also provides mechanical support.
- PHLOEM
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A component of the plant vascular system that delivers sugars, amino acids, mineral nutrients and information molecules (hormones, peptide hormones, proteins and RNA) to developing tissues and organs. Translocation occurs from source tissues to tissues that require nutrients to support growth. Transport occurs through a unique sieve-tube system, is unidirectional, and is driven by a gradient of positive pressure.
- COMPANION CELL
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A specialized cell that is associated with a sieve element in the phloem of flowering plants.
- SIEVE ELEMENT
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A cell of the phloem that functions in the long-distance transport of sugars and signalling molecules.
- SYMPLASM
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A cytoplasmic continuum that occurs between cells of a tissue or organ. It is mediated by plasmodesmata or gap junctions.
- SYSTEMIC ACQUIRED RESISTANCE (SAR)
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Resistance to pathogens that occurs when defence signalling molecules are transmitted through the phloem to upregulate specific defence genes.
- MONOCOTYLEDON
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A plant that has a single cotyledon (seed leaf) as an embryo.
- PRIMORDIA
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Plants form appendages, such as leaves, flowers and lateral roots, through the generation of groups of cells that collectively are called primordia. Cells that are incorporated into these developmental domains are ultimately derived from the shoot or root apical meristems.
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Lucas, W., Lee, JY. Plasmodesmata as a supracellular control network in plants. Nat Rev Mol Cell Biol 5, 712–726 (2004). https://doi.org/10.1038/nrm1470
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DOI: https://doi.org/10.1038/nrm1470
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