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Proceedings of the National Academy of... Mar 2020The coordinated redistribution of sugars from mature "source" leaves to developing "sink" leaves requires tight regulation of sugar transport between cells via...
The coordinated redistribution of sugars from mature "source" leaves to developing "sink" leaves requires tight regulation of sugar transport between cells via plasmodesmata (PD). Although fundamental to plant physiology, the mechanisms that control PD transport and thereby support development of new leaves have remained elusive. From a forward genetic screen for altered PD transport, we discovered that the conserved eukaryotic glucose-TOR (TARGET OF RAPAMYCIN) metabolic signaling network restricts PD transport in leaves. Genetic approaches and chemical or physiological treatments to either promote or disrupt TOR activity demonstrate that glucose-activated TOR decreases PD transport in leaves. We further found that TOR is significantly more active in mature leaves photosynthesizing excess sugars than in young, growing leaves, and that this increase in TOR activity correlates with decreased rates of PD transport. We conclude that leaf cells regulate PD trafficking in response to changing carbohydrate availability monitored by the TOR pathway.
Topics: Arabidopsis; Arabidopsis Proteins; Biological Transport; Carbohydrate Metabolism; Gene Expression Profiling; Gene Expression Regulation, Developmental; Gene Expression Regulation, Plant; Gene Knockdown Techniques; Gene Silencing; Phosphatidylinositol 3-Kinases; Plant Cells; Plant Leaves; Plasmodesmata; Protein Transport; Signal Transduction; Nicotiana
PubMed: 32051250
DOI: 10.1073/pnas.1919196117 -
Journal of Plant Physiology Feb 2021Plant tissues exhibit a symplasmic organization; the individual protoplasts are connected to their neighbors via cytoplasmic bridges that extend through pores in the... (Review)
Review
Plant tissues exhibit a symplasmic organization; the individual protoplasts are connected to their neighbors via cytoplasmic bridges that extend through pores in the cell walls. These bridges may have diameters of a micrometer or more, as in the sieve pores of the phloem, but in most cell types they are smaller. Historically, botanists referred to cytoplasmic bridges of all sizes as plasmodesmata. The meaning of the term began to shift when the transmission electron microscope (TEM) became the preferred tool for studying these structures. Today, a plasmodesma is widely understood to be a 'nano-scale' pore. Unfortunately, our understanding of these nanoscopic channels suffers from methodological limitations. This is exemplified by the fact that state-of-the-art EM techniques appear to reveal plasmodesmal pore structures that are much smaller than the tracer molecules known to diffuse through these pores. In general, transport processes in pores that have dimensions in the size range of the transported molecules are governed by different physical parameters than transport process in the macroscopic realm. This can lead to unexpected effects, as experience in nanofluidic technologies demonstrates. Our discussion of problems of size in plasmodesma research leads us to conclude that the field will benefit from technomimetic reasoning - the utilization of concepts developed in applied nanofluidics for the interpretation of biological systems.
Topics: Biological Transport; Phloem; Plasmodesmata; Terminology as Topic
PubMed: 33388666
DOI: 10.1016/j.jplph.2020.153341 -
Plants (Basel, Switzerland) Feb 2024During plant development, mobile proteins, including transcription factors, abundantly serve as messengers between cells to activate transcriptional signaling cascades... (Review)
Review
During plant development, mobile proteins, including transcription factors, abundantly serve as messengers between cells to activate transcriptional signaling cascades in distal tissues. These proteins travel from cell to cell via nanoscopic tunnels in the cell wall known as plasmodesmata. Cellular control over this intercellular movement can occur at two likely interdependent levels. It involves regulation at the level of plasmodesmata density and structure as well as at the level of the cargo proteins that traverse these tunnels. In this review, we cover the dynamics of plasmodesmata formation and structure in a developmental context together with recent insights into the mechanisms that may control these aspects. Furthermore, we explore the processes involved in cargo-specific mechanisms that control the transport of proteins via plasmodesmata. Instead of a one-fits-all mechanism, a pluriform repertoire of mechanisms is encountered that controls the intercellular transport of proteins via plasmodesmata to control plant development.
PubMed: 38475529
DOI: 10.3390/plants13050684 -
Plant Physiology Dec 2021Sucrose, hexoses, and raffinose play key roles in the plant metabolism. Sucrose and raffinose, produced by photosynthesis, are translocated from leaves to flowers,... (Review)
Review
Sucrose, hexoses, and raffinose play key roles in the plant metabolism. Sucrose and raffinose, produced by photosynthesis, are translocated from leaves to flowers, developing seeds and roots. Translocation occurs in the sieve elements or sieve tubes of angiosperms. But how is sucrose loaded into and unloaded from the sieve elements? There seem to be two principal routes: one through plasmodesmata and one via the apoplasm. The best-studied transporters are the H+/SUCROSE TRANSPORTERs (SUTs) in the sieve element-companion cell complex. Sucrose is delivered to SUTs by SWEET sugar uniporters that release these key metabolites into the apoplasmic space. The H+/amino acid permeases and the UmamiT amino acid transporters are hypothesized to play analogous roles as the SUT-SWEET pair to transport amino acids. SWEETs and UmamiTs also act in many other important processes-for example, seed filling, nectar secretion, and pollen nutrition. We present information on cell type-specific enrichment of SWEET and UmamiT family members and propose several members to play redundant roles in the efflux of sucrose and amino acids across different cell types in the leaf. Pathogens hijack SWEETs and thus represent a major susceptibility of the plant. Here, we provide an update on the status of research on intercellular and long-distance translocation of key metabolites such as sucrose and amino acids, communication of the plants with the root microbiota via root exudates, discuss the existence of transporters for other important metabolites and provide potential perspectives that may direct future research activities.
Topics: Amino Acids; Biological Transport; Membrane Transport Proteins; Phloem; Plasmodesmata; Sugars
PubMed: 34015139
DOI: 10.1093/plphys/kiab228 -
Journal of Virology Aug 2019Positive-stranded RNA virus movement proteins (MPs) generally lack sequence-specific nucleic acid-binding activities and display cross-family movement complementarity...
Positive-stranded RNA virus movement proteins (MPs) generally lack sequence-specific nucleic acid-binding activities and display cross-family movement complementarity with related and unrelated viruses. Negative-stranded RNA plant rhabdoviruses encode MPs with limited structural and functional relatedness with other plant virus counterparts, but the precise mechanisms of intercellular transport are obscure. In this study, we first analyzed the abilities of MPs encoded by five distinct rhabdoviruses to support cell-to-cell movement of two positive-stranded RNA viruses by using -complementation assays. Each of the five rhabdovirus MPs complemented the movement of MP-defective mutants of tomato mosaic virus and potato X virus. In contrast, movement of recombinant MP deletion mutants of sonchus yellow net nucleorhabdovirus (SYNV) and tomato yellow mottle-associated cytorhabdovirus (TYMaV) was rescued only by their corresponding MPs, i.e., SYNV sc4 and TYMaV P3. Subcellular fractionation analyses revealed that SYNV sc4 and TYMaV P3 were peripherally associated with cell membranes. A split-ubiquitin membrane yeast two-hybrid assay demonstrated specific interactions of the membrane-associated rhabdovirus MPs only with their cognate nucleoproteins (N) and phosphoproteins (P). More importantly, SYNV sc4-N and sc4-P interactions directed a proportion of the N-P complexes from nuclear sites of replication to punctate loci at the cell periphery that partially colocalized with the plasmodesmata. Our data show that cell-to-cell movement of plant rhabdoviruses is highly specific and suggest that cognate MP-nucleocapsid core protein interactions are required for intra- and intercellular trafficking. Local transport of plant rhabdoviruses likely involves the passage of viral nucleocapsids through MP-gated plasmodesmata, but the molecular mechanisms are not fully understood. We have conducted complementation assays with MPs encoded by five distinct rhabdoviruses to assess their movement specificity. Each of the rhabdovirus MPs complemented the movement of MP-defective mutants of two positive-stranded RNA viruses that have different movement strategies. In marked contrast, cell-to-cell movement of two recombinant plant rhabdoviruses was highly specific in requiring their cognate MPs. We have shown that these rhabdovirus MPs are localized to the cell periphery and associate with cellular membranes, and that they interact only with their cognate nucleocapsid core proteins. These interactions are able to redirect viral nucleocapsid core proteins from their sites of replication to the cell periphery. Our study provides a model for the specific inter- and intracellular trafficking of plant rhabdoviruses that may be applicable to other negative-stranded RNA viruses.
Topics: Cell Membrane; Genetic Complementation Test; Plant Viral Movement Proteins; Plant Viruses; Protein Binding; Rhabdoviridae; Nicotiana; Virus Internalization
PubMed: 31118256
DOI: 10.1128/JVI.00296-19 -
ELife Nov 2019Regulation of molecular transport via intercellular channels called plasmodesmata (PDs) is important for both coordinating developmental and environmental responses...
Regulation of molecular transport via intercellular channels called plasmodesmata (PDs) is important for both coordinating developmental and environmental responses among neighbouring cells, and isolating (groups of) cells to execute distinct programs. Cell-to-cell mobility of fluorescent molecules and PD dimensions (measured from electron micrographs) are both used as methods to predict PD transport capacity (i.e., effective symplasmic permeability), but often yield very different values. Here, we build a theoretical bridge between both experimental approaches by calculating the effective symplasmic permeability from a geometrical description of individual PDs and considering the flow towards them. We find that a dilated central region has the strongest impact in thick cell walls and that clustering of PDs into pit fields strongly reduces predicted permeabilities. Moreover, our open source multi-level model allows to predict PD dimensions matching measured permeabilities and add a functional interpretation to structural differences observed between PDs in different cell walls.
Topics: Biological Transport; Biophysics; Cell Movement; Cell Wall; Computer Simulation; Models, Biological; Particle Size; Permeability; Plasmodesmata
PubMed: 31755863
DOI: 10.7554/eLife.49000 -
Essays in Biochemistry Sep 2022Systemic acquired resistance (SAR), a type of long-distance immunity in plants, provides long-lasting resistance to a broad spectrum of pathogens. SAR is thought to... (Review)
Review
Systemic acquired resistance (SAR), a type of long-distance immunity in plants, provides long-lasting resistance to a broad spectrum of pathogens. SAR is thought to involve the rapid generation and systemic transport of a mobile signal that prepares systemic parts of the plant to better resist future infections. Exploration of the molecular mechanisms underlying SAR have identified multiple mobile regulators of SAR in the last few decades. Examination of the relationship among several of these seemingly unrelated molecules depicts a forked pathway comprising at least two branches of equal importance to SAR. One branch is regulated by the plant hormone salicylic acid (SA), and the other culminates (based on current knowledge) with the phosphorylated sugar derivative, glycerol-3-phosphate (G3P). This review summarizes the activities that contribute to pathogen-responsive generation of SA and G3P and the components that regulate their systemic transport during SAR.
Topics: Disease Resistance; Gene Expression Regulation, Plant; Glycerol; Glycerophosphates; Phosphates; Plant Diseases; Plant Growth Regulators; Plants; Salicylic Acid; Sugars
PubMed: 35920211
DOI: 10.1042/EBC20210098 -
Methods in Molecular Biology (Clifton,... 2022Array tomography (AT) is a new high-throughput imaging method for high-resolution imaging of ultrastructure and for 3-D reconstruction of cells and organelles. Here, we...
Array tomography (AT) is a new high-throughput imaging method for high-resolution imaging of ultrastructure and for 3-D reconstruction of cells and organelles. Here, we describe the entire procedure for obtaining a spatial image of the distribution of plasmodesmata (PD). As example, the protocol is applied here to reconstruct the number and arrangement of PD between cells undergoing differentiation during Arabidopsis somatic embryogenesis.
Topics: Image Processing, Computer-Assisted; Imaging, Three-Dimensional; Plasmodesmata; Tomography; Tomography, X-Ray Computed
PubMed: 35349133
DOI: 10.1007/978-1-0716-2132-5_4 -
Plants (Basel, Switzerland) Sep 2022Plant viruses exploit the endomembrane system of infected cells for their replication and cell-to-cell transport. The replication of viral RNA genomes occurs in the... (Review)
Review
Plant viruses exploit the endomembrane system of infected cells for their replication and cell-to-cell transport. The replication of viral RNA genomes occurs in the cytoplasm in association with reorganized endomembrane compartments induced by virus-encoded proteins and is coupled with the virus intercellular transport via plasmodesmata that connect neighboring cells in plant tissues. The transport of virus genomes to and through plasmodesmata requires virus-encoded movement proteins (MPs). Distantly related plant viruses encode different MP sets, or virus transport systems, which vary in the number of MPs and their properties, suggesting their functional differences. Here, we discuss two distinct virus transport pathways based on either the modification of the endoplasmic reticulum tubules or the formation of motile vesicles detached from the endoplasmic reticulum and targeted to endosomes. The viruses with the movement proteins encoded by the triple gene block exemplify the first, and the potyviral system is the example of the second type. These transport systems use unrelated mechanisms of endomembrane reorganization. We emphasize that the mode of virus interaction with cell endomembranes determines the mechanism of plant virus cell-to-cell transport.
PubMed: 36145804
DOI: 10.3390/plants11182403 -
Microorganisms Mar 2021Of the various proteins encoded by plant viruses, one of the most interesting is the movement protein (MP). MPs are unique to plant viruses and show surprising... (Review)
Review
Of the various proteins encoded by plant viruses, one of the most interesting is the movement protein (MP). MPs are unique to plant viruses and show surprising structural and functional variability while maintaining their core function, which is to facilitate the intercellular transport of viruses or viral nucleoprotein complexes. MPs interact with components of the intercellular channels, the plasmodesmata (PD), modifying their size exclusion limits and thus allowing larger particles, including virions, to pass through. The interaction of MPs with the components of PD, the formation of transport complexes and the recruitment of host cellular components have all revealed different facets of their functions. Multitasking is an inherent property of most viral proteins, and MPs are no exception. Some MPs carry out multitasking, which includes gene silencing suppression, viral replication and modulation of host protein turnover machinery. This review brings together the current knowledge on MPs, focusing on their structural variability, various functions and interactions with host proteins.
PubMed: 33801711
DOI: 10.3390/microorganisms9040695