Symplastic intercellular transport from a developmental perspective

Journal of Experimental Botany, Apr 2014

Plant cells have channel-like structures named plasmodesmata that allow for the symplastic molecular transport between neighbouring cells. The importance of plasmodesmata in whole plant development is well acknowledged. They mediate the cell-to-cell and vascular loading and unloading of metabolites, proteins, and other signalling molecules. However, it is still not clear how, mechanistically, these channels are regulated in response to developmental and environmental cues. This review aims to bring together knowledge acquired in recent years on plasmodesmata composition, regulation, and function. Progress in the discovery of factors that regulate symplastic transport and plant development in particular are discussed. This will hopefully highlight the challenges faced by the scientific community to unveil the mechanisms controlling symplastic communication during the formation and maintenance of plant meristems.

A PDF file should load here. If you do not see its contents the file may be temporarily unavailable at the journal website or you do not have a PDF plug-in installed and enabled in your browser.

Alternatively, you can download the file locally and open with any standalone PDF reader:

https://jxb.oxfordjournals.org/content/65/7/1857.full.pdf

Symplastic intercellular transport from a developmental perspective

Journal of Experimental Botany Symplastic intercellular transport from a developmental perspective Yoselin Benitez-Alfonso 0 0 Centre for Plant Sciences, School of Biology, University of Leeds , Leeds LS2 9JT , UK Plant cells have channel-like structures named plasmodesmata that allow for the symplastic molecular transport between neighbouring cells. The importance of plasmodesmata in whole plant development is well acknowledged. They mediate the cell-to-cell and vascular loading and unloading of metabolites, proteins, and other signalling molecules. However, it is still not clear how, mechanistically, these channels are regulated in response to developmental and environmental cues. This review aims to bring together knowledge acquired in recent years on plasmodesmata composition, regulation, and function. Progress in the discovery of factors that regulate symplastic transport and plant development in particular are discussed. This will hopefully highlight the challenges faced by the scientific community to unveil the mechanisms controlling symplastic communication during the formation and maintenance of plant meristems. Intercellular communication; meristem development; plasmodesmata; plasmodesmata proteins; plasmadesmata regulation; symplastic transport - © The Author 2014. Published by Oxford University Press on behalf of the Society for Experimental Biology. All rights reserved. For permissions, please email: of complex genetic and proteomic screens in different laboratoriess (Faulkner and Maule, 2011). New information has also been gained on the function of PD proteins, intracellular and extracellular regulators, and of mobile factors in the regulation of plant growth, organ patterning, and stress response in model and non-model organisms. This review compiles part of this information, focusing on recent evidence supporting or clarifying the role of symplastic transport in the initiation and maintenance of primary and secondary meristems. Identification of plasmodesmata proteins The proteomic analysis of digested cell walls represented a significant step towards the elucidation of PD molecular composition (Faulkner and Maule, 2011; Fernandez-Calvino et al., 2011; Salmon and Bayer, 2012). A number of proteins identified using this approach have been confirmed to target PDs in stable transgenic lines. These include PlasmoDesmataLocated Proteins (PDLPs), PlasmoDesmata Callose Binding proteins (PDCBs), Glycosyl Hydrolases family 17 (GHL17; BG), Receptor Like Kinases (RLK), etc. Some of these proteins (or families of proteins) have been characterized and their role in PD regulation and plant development has been studied (Thomas et al., 2008; Simpson et al., 2009; BenitezAlfonso et al., 2013; Faulkner et al., 2013). So far, no common molecular signature has been identified among PD proteins and, therefore, it is difficult to distinguish them (based on their sequence) from other secreted or plasma membranetargeted proteins, and/or from other family members playing redundant and non-redundant functions in the cell. Genetic and functional redundancy between PD proteins may have hindered their identification through genetic screens. Almost simultaneously, two forward genetic approaches were pursued to isolate PD mutants (Kobayashi et al., 2007; Benitez-Alfonso et al., 2009; Stonebloom et al., 2009; Xu et al., 2011, 2012). In both instances, intracellular regulators rather than PD-linked components were identified (see below). Similarly, an enhancer genetic screen using as the starter line the erl1erl2 mutant (defective in stomata differentiation) identified KOBITO1 as a regulator of PD permeability in epidermal pavement cells (Kong et al., 2012). Highlighting the importance of PD in vascular transport, screening for mutants in phloem transport successfully identified gain-of-function mutations in the PD protein Callose Synthase 3 (CALS3). CALS3 acts in the phloem where it controls symplastic connectivity and vascular development (Vaten et al., 2011). Alternative proteomic strategies have enriched the list of confirmed PD proteins in model and non-model species. For example, affinity purification of interactors, using as bait the non-cell autonomous protein CmPP16, identified PD-located Germin like proteins (Ham et al., 2012). Similar methodology, in this case using as bait PD-associated calreticulin, revealed PD-localization for a member of the glycosyltransferase-like family (Zalepa-King and Citovsky, 2013). Comparative genomic approaches have been useful for the identification of PD proteins in other species. Orthologues of Arabidopsis PD-located β-1,3 glucanases were identified in poplar. Localization and expression studies of these proteins revealed a novel role for members of this family in bud dormancy release (Rinne et al., 2011). In summary, despite major challenges in the isolation of PDs from cell walls, the combined use of genetic, proteomic, and cell biology approaches has led to the identification of PD-localized proteins and some important intracellular regulators. The increased availability of plant genomes, the development of biotechnological tools, and recent advances in cell biology and proteomic approaches are expected to accelerate knowledge acquisition on PD composition and function in model and non-model species. The functional characterization of PD proteins is far from complete but has already provided important clues about conditions and signalling pathways involved in PD function and regulation. Regulation of plasmodesmata transport Structural modifications of plasmodesmata PDs can originate during cell division (primary) or postcytokinesis (secondary) with a generally simple structure (a cell membrane single channel like structure transversed by an appressed ER-derived desmotubule) (Faulkner et  al., 2008; Burch-Smith et al., 2011). Simple PD, alone or in pairs (twinned), are frequently found in all symplatically connected cell types but PDs can also appear with different branched shapes/structures. The signals or conditions that induce the formation of branched PDs are mainly unknown. Little is also known about the consequences that these transitions have for intercellular transport. Branched PDs occur in mature cells where they presumably regulate more tightly PD aperture during cell growth and expansion. This theory was challenged following the discovery of embryogenesis mutants with increased branched PDs and increased symplastic connectivity (Burch-Smith and Zambryski, 2010). This finding highlights the lack of information on how transport capability is influenced by structural modifications of PDs. Several key questions remain unanswered, or only partially answered. Is the PD branching effect on symplastic transport different in different tissue types? Can branched PDs provide directionality in symplastic transport? or selectivity with regard to the type of molecular transport (passive or active) used by mobile molecules? These and other questions are at the core of current discussions on the generation of branched PDs and on their significance for development and during the plant response to environmental cues. Interested readers are encouraged to consult recent revisions on this topic (Faulkner et al., 2008; Ehlers and van Bel, 2010; Burch-Smith et  al., 2011; BurchSmith and Zambryski, 2012). The role of cell-wall polysaccharides Plasmodesmata are embedded in the cell wall, therefore modifications in cell-wall composition are likely to have an impact on symplastic transport. The role of the β-1,3 glucan callose, which is deposited in the neck region of the channel, is particularly well described (Chen and Kim, 2009; Ueki and Citovsky, 2011; Zavaliev et al., 2011; Burch-Smith and Zambryski, 2012; Li et  al., 2012). Changes in callose deposition, in response to intracellular or extracellular signals, control PD aperture and, thereby, regulates mass flow and size of the transported molecules. Turnover of callose in the cell wall surrounding the PD is mediated by the balanced activity of callose synthases and β-1,3 glucanases, enzymes responsible for the synthesis and breakdown of callose respectively (Chen and Kim, 2009; Vaten et  al., 2011; Zavaliev et al., 2011; Benitez-Alfonso et al., 2013). Other PD proteins, such as PDCBs (Simpson et al., 2009), and class 1 Reversibly Glycosylated polypeptides (Zavaliev et  al., 2010; Burch-Smith et  al., 2012), influence callose accumulation at the PD. The cell redox status and calcium homeostasis are also known regulators of callose turnover at the PD, although the mechanism behind this regulation is not very clear (see below). Interestingly, recent research identified PD-located receptors involved in the control of callose deposition at the PD (Ueki et al., 2010; Lee et al., 2011). The identification of receptors at the PD might shed some new light into the mechanism underlying the control of symplastic connectivity by callose in response to extracellular signals (Fig. 1). The expression at the PD of callose metabolic enzymes is known to be important in the spreading of viruses and other pathogens (Lee and Lu, 2011; Ueki and Citovsky, 2011; Li et  al., 2012; Zavaliev et  al., 2013), but recent publications confirmed their role in the formation of symplastic domains during development (Rinne et  al., 2011; Benitez-Alfonso et al., 2013). Regulated callose biosynthesis has been shown to play a role in stomatal and vascular patterning and in the formation and maintenance of the apical and lateral meristems (Guseman et al., 2010; Bishopp et al., 2011; Vaten et al., 2011; Slewinski et al., 2012). Other cell-wall components are likely to be involved in the regulation of PD aperture although their function is not as well defined. Digestion of Chara corallina cell walls with enzymes that break down cellulose or pectins decrease the average number of spokes (anchor points to the cell wall) per plasmodesma suggesting that these polysaccharides contribute to stabilize PD structure (Brecknock et al., 2011). A role for pectin modification in the control of PD permeability was supported by the identification of pectin methylesterases (PME) linked to PD (Chen et al., 2000; Chen and Citovsky 2003). In tobacco, these enzymes have been found to bind viral movement proteins and be required for the local and systemic spreading of tobamoviruses. As before, the molecular mechanism and the signals involved in regulating PME activity have not yet been identified. Redox conditions and calcium fluxes modify plasmodesmata permeability Evidences from different sources indicate that PD aperture (and vascular transport) is regulated by calcium and cell redox homeostasis (Baluska et  al., 2001; Benitez-Alfonso et  al., 2010; van Bel et  al., 2011). Reactive Oxygen Species (ROS, Fig. 1. Regulation of plasmodesmata transport by callose. Cartoon representing a simple open plasmodesmata traversing the cell wall to facilitate molecular transport (molecular flux) between neighbouring cells (1). Callose deposited in the PD neck region controls channel aperture. Signals released in the apoplast (or generated intracellularly) activate receptors located in the vicinity of PDs which trigger signalling cascades that modulate the expression of genes involved in callose metabolism (2, 4). Increased callose deposition constricts PD aperture and restricts molecular transport (3) whereas induced expression of genes involved in callose degradation promotes intercellular transport (1). 2013). A  few of the recent original articles will be revisited here to illustrate the progress in this area of research. PD transport and the formation and maintenance of the apical meristems e.g. peroxides, superoxides etc.) and nitric oxide are generated in response to a wide range of environmental stresses and as a by-product of normal aerobic metabolism (Suzuki et  al., 2011). Changes in calcium fluxes (or patterns) also occur in response to biotic and abiotic stimuli and modulate calciumdependent processes occurring in different cellular organelles (Baluska et al., 2001). These molecules are known to play a role in defence and, together with phytohormones, act as signalling molecules in plant growth and morphogenesis. Ample cross-talk exists between redox signalling and calcium signalling pathways such that the contribution of these messengers in plant metabolism, cellular response, and cellular transport is often difficult to discern (Rodriguez-Serrano et  al., 2009; Mazars et al., 2010; Suzuki et al., 2011). The relationship between changes in calcium fluxes and PD aperture was investigated using a calcium-sensitive dye, carboxyfluorescein as symplasmic reporter and chemicals or conditions that affect calcium intracellular levels (Tucker and Boss, 1996; Holdaway-Clarke et al., 2000). The localization at the PD of proteins involved in calcium response (such as centrin-like and calreticulins) further supported this relationship (Baluska et al., 2001). Moreover, it was recently reported that synaptotagmins (proteins involved in sensing calcium) are required for the intercellular movement of viruses through PDs via an endocytic pathway (Lewis and Lazarowitz, 2010). The role of ROS in symplastic transport was discovered through the characterization of Arabidopsis mutants impaired in plasmodesmal connectivity and cell redox homeostasis (Benitez-Alfonso and Jackson, 2009; Benitez-Alfonso et  al., 2009; Stonebloom et al., 2009, 2011). Follow up experiments using plants treated with different oxidants revealed that the concentration, origin, and/or molecular nature of the redox signal are major determinants in this regulation: a plastidial redox imbalance causes a decrease in symplastic transport by increasing callose deposition whereas defective mitochondria can lead to enhanced transport capacity by increasing PD branching (Rutschow et  al., 2011). This finding is particularly exciting as it suggests a high level of specificity in the redox signal that trigger PD modifications. More research in this area is required to uncover the molecular pathway underlying the differential regulation of PD transport by ROS. Since ROS and calcium levels are powerful indicators of environmental changes, the regulation of PD transport by these signalling molecules represents a mechanism to translate external inputs into appropriate developmental responses through regulating the transport of developmental and/or nutritional factors. using disarmed viruses to increase PD permeability has been recently described as a viable method to induce flowering in crops (McGarry and Kragler, 2013). Symplastic connectivity regulates the development of secondary root organs Although, it has been shown that the development of the embryonic root meristem is highly dependent on the symplastic transport of factors that specify cell fate, the importance of this process in post-embryonic root organ formation has only recently emerged (Benitez-Alfonso et  al., 2013; Maule et al., 2013). The development of root hair cells and of secondary meristems (lateral roots) increases the root capacity to acquire water and other nutrients from the soil. These processes are regulated by the transport of phytohormones and the activation of signalling pathways that promote cell division and tissue morphogenesis (Benkova and Bielach, 2010; Lee and Cho, 2013). The crucial role of PD-mediated transport of developmental factors (such as CAPRICE: Kurata et al., 2005) in the differentiation of epidermal cells into root hairs has also been described (Lee and Cho, 2013). The formation of lateral roots (LR) from xylem pole pericycle cells (XPP) in Arabidopsis is fundamentally a different process but, as for root hairs, symplastic connectivity seems to be important. Phloem unloading of the dye carboxyfluorescein into the surrounding tissue is observed in the root tip but, as the root matures, connectivity between the phloem and the adjacent pericycle disappears (Wright and Oparka, 1997). This change in symplastic connectivity occurs despite the presence of numerous plasmodesmata (high PD frequency) connecting the phloem–pericycle interface (Wright and Oparka, 1997; Ma and Peterson, 2001). After reprogramming of XPP, and during the initial stages of LR formation, dye unloading is restored but the primordia again appear symplastically isolated from the phloem in the late stages (Oparka et  al., 1995). These experiments suggest an active regulation of PD aperture during lateral root development. Phloem unloading is re-established when a new vascular system is formed in older (emerging) primordia. These results were confirmed using the symplastic reporter pSUC2-GFP in a more recent paper (Benitez-Alfonso et al., 2013). Together with phloem unloading, changes in symplastic connectivity in the interface formed by the primordia, neighbouring XPP, and overlying tissues were also described. A  role for callose in the control of symplastic connectivity during the initiation of lateral root primordia was proposed which was supported by the identification of two novel PD-located β-1,3 glucanases expressed in early stages of LR development. Results obtained from the analysis of mutants and inducible and over-expression lines affected in callose deposition at the PD suggest that the pathways for symplastic transport around newly formed primordia must be open for correct LR spatial patterning to occur. Later in development, increased callose deposition symplastically isolates the primordia from the neighbouring tissue which seems to influence the successful emergence of the young lateral root (Maule et al., 2013). Not surprisingly, PD proteins expressed during lateral root initiation and emergence, are regulated after treatment with synthetic auxins and this regulation disappeared in the mutant solitary-root (slr), which displays reduced sensitivity to auxin (Benitez-Alfonso et al., 2013; Maule et al., 2013). The mobility in the phloem of IAA (indoleacetic acid)induced transcripts has recently been reported (Notaguchi et  al., 2012). Regulated symplastic connectivity might be required to control the unloading of these transcripts, and the transport of other non-cell autonomous proteins, into specific root domains, which might be crucial in the establishment of a correct LR pattern. Disparate data suggest that symplastic connectivity might also influence the formation of symbiotic nodules. Nodules are secondary root organs initiated upon the association of rhizobia to root hairs (Oldroyd and Downie, 2008). Analysis of symplastic domains formed in Medicago truncatula roots infected with rhizobia indicated that intercellular symplastic transport between the phloem and the adjacent tissues is positively regulated in the initial dividing cells of the nodule (Complainville et  al., 2003). Improving symplastic permeability, using transgenic plants expressing a viral movement protein, increases nodule formation suggesting that PD regulation is important for nodule development and/or function. Evidence from ultrastructural studies indicate an increase in the number of secondary PDs in nodules from infected Datisca glomerata root compared with uninfected root tissues (Schubert et al., 2011). By contrast, plasmodesmal connectivity in Casuarina glauca nodules, infected with the actinorhizal Frankia, was reduced by about 30–50% compared with neighbouring uninfected cortical cells (Schubert et al., 2013). Further research is required to discover the specific role of PD in nodule initiation and function and to identify factors regulating this process. This will hopefully shed some light on the differences observed between symbiotic systems. The crucial roles of PD in the communication of signals and nutrients between cells, tissues, and organs and the consequences of altering PD regulation for plant development and response to the environment are very well established. Recently, new data on the proteomic composition of these intercellular channels have been collected. Now, the challenge is to understand the specific function of these proteins in PD biogenesis, modification, and/or transport capability. Changes in PD structure, and/or in the composition of the surrounding cell wall, occur in response to developmental and environmental signals (including ROS and calcium fluxes) but information on the mechanism behind this regulation is often missing. More research is required to dissect the molecular components involved and to understand the importance of these regulatory mechanisms in plant growth, morphogenesis, and stress response. New knowledge reinforces the importance of symplastic connectivity and transport in the formation and maintenance of the apical and secondary meristems. Novel mobile transcription factors, siRNAs, microRNAs, and transcripts, that act non-cell autonomously in the meristems, have been identified. Putting this information together with the data acquired on PD composition and regulation should reveal new strategies to investigate how these factors interact to control plant growth, adaptation, and survival to adverse environments. Progress on this research could also yield new potential targets for biotechnological modifications of PD with the aim of improving these traits in agriculturally important crops. Acknowledgements The author gratefully acknowledges Jim Barnes for critical reading and editing of the manuscript. Baluska F, Cvrckova F, Kendrick-Jones J, Volkmann D. 2001. Sink plasmodesmata as gateways for phloem unloading. Myosin VIII and calreticulin as molecular determinants of sink strength? Plant Physiology 126, 39–46. Benitez-Alfonso Y, Cilia M, San RA, Thomas C, Maule A, Hearn S, Jackson D. 2009. Control of Arabidopsis meristem development by thioredoxin-dependent regulation of intercellular transport. Proceedings of the National Academy of Sciences, USA 106, 3615–3620. Benitez-Alfonso Y, Faulkner C, Pendle A, Miyashima S, Helariutta Y, Maule A. 2013. Symplastic intercellular connectivity regulates lateral root patterning. Developmental Cell 26, 136–147. Benitez-Alfonso Y, Jackson D. 2009. Redox homeostasis regulates plasmodesmal communication in Arabidopsis meristems. Plant Signaling and Behavior 4, 655–659. Benitez-Alfonso Y, Jackson D, Maule A. 2010. Redox regulation of intercellular transport. Protoplasma 248, 131–140. Benkova E, Bielach A. 2010. Lateral root organogenesis: from cell to organ. Current Opinion in Plant Biology 13, 677–683. Bishopp A, Lehesranta S, Vaten A, Help H, El-Showk S, Scheres B, Helariutta K, Mahonen AP, Sakakibara H, Helariutta Y. 2011. Phloemtransported cytokinin regulates polar auxin transport and maintains vascular pattern in the root meristem. Current Biology 21, 927–932. Brecknock S, Dibbayawan TP, Vesk M, Vesk PA, Faulkner C, Barton DA, Overall RL. 2011. High resolution scanning electron microscopy of plasmodesmata. Planta 234, 749–758. Burch-Smith TM, Cui Y, Zambryski PC. 2012. Reduced levels of class 1 reversibly glycosylated polypeptide increase intercellular transport via plasmodesmata. Plant Signaling and Behavior 7, 62–67. Burch-Smith TM, Stonebloom S, Xu M, Zambryski PC. 2011. Plasmodesmata during development: re-examination of the importance of primary, secondary, and branched plasmodesmata structure versus function. Protoplasma 248, 61–74. Burch-Smith TM, Zambryski PC. 2010. Loss of INCREASED SIZE EXCLUSION LIMIT (ISE)1 or ISE2 increases the formation of secondary plasmodesmata. Current Biology 20, 989–993. Burch-Smith TM, Zambryski PC. 2012. Plasmodesmata paradigm shift: regulation from without versus within. Annual Review of Plant Biology 63, 239–260. Chen MH, Citovsky V. 2003. Systemic movement of a tobamovirus requires host cell pectin methylesterase. The Plant Journal 35, 386–392. Chen MH, Sheng J, Hind G, Handa AK, Citovsky V. 2000. Interaction between the tobacco mosaic virus movement protein and host cell pectin methylesterases is required for viral cell-to-cell movement. EMBO Journal 19, 913–920. Chen XY, Kim JY. 2009. Callose synthesis in higher plants. Plant Signaling and Behavior 4, 489–492. Complainville A, Brocard L, Roberts I, Dax E, Sever N, Sauer N, Kondorosi A, Wolf S, Oparka K, Crespi M. 2003. Nodule initiation involves the creation of a new symplasmic field in specific root cells of medicago species. The Plant Cell 15, 2778–2791. Ehlers K, van Bel AJ. 2010. Dynamics of plasmodesmal connectivity in successive interfaces of the cambial zone. Planta 231, 371–385. Faulkner C, Akman OE, Bell K, Jeffree C, Oparka K. 2008. Peeking into pit fields: a multiple twinning model of secondary plasmodesmata formation in tobacco. The Plant Cell 20, 1504–1518. Faulkner C, Maule A. 2011. Opportunities and successes in the search for plasmodesmal proteins. Protoplasma 248, 27–38. Faulkner C, Petutschnig E, Benitez-Alfonso Y, Beck M, Robatzek S, Lipka V, Maule AJ. 2013. LYM2-dependent chitin perception limits molecular flux via plasmodesmata. Proceedings of the National Academy of Sciences, USA 110, 9166–9170. Fernandez-Calvino L, Faulkner C, Walshaw J, Saalbach G, Bayer E, Benitez-Alfonso Y, Maule A. 2011. Arabidopsis plasmodesmal proteome. PLoS One 6, e18880. Furuta K, Lichtenberger R, Helariutta Y. 2012. The role of mobile small RNA species during root growth and development. Current Opinion in Cell Biology 24, 211–216. Guseman JM, Lee JS, Bogenschutz NL, Peterson KM, Virata RE, Xie B, Kanaoka MM, Hong Z, Torii KU. 2010. Dysregulation of cellto-cell connectivity and stomatal patterning by loss-of-function mutation in Arabidopsis chorus (glucan synthase-like 8). Development 137, 1731–1741. Ham BK, Li G, Kang BH, Zeng F, Lucas WJ. 2012. Overexpression of Arabidopsis plasmodesmata germin-like proteins disrupts root growth and development. The Plant Cell 24, 3630–3648. Holdaway-Clarke TL, Walker NA, Hepler PK, Overall RL. 2000. Physiological elevations in cytoplasmic free calcium by cold or ion injection result in transient closure of higher plant plasmodesmata. Planta 210, 329–335. Hyun TK, Uddin MN, Rim Y, Kim JY. 2011. Cell-to-cell trafficking of RNA and RNA silencing through plasmodesmata. Protoplasma 248, 101–116. Kim I, Zambryski PC. 2008. Intercellular trafficking of macromolecules during embryogenesis. Methods in Molecular Biology 427, 145–155. Kobayashi K, Otegui MS, Krishnakumar S, Mindrinos M, Zambryski P. 2007. INCREASED SIZE EXCLUSION LIMIT 2 encodes a putative DEVH box RNA helicase involved in plasmodesmata function during Arabidopsis embryogenesis. The Plant Cell 19, 1885–1897. Koizumi K, Wu S, Macrae-Crerar A, Gallagher KL. 2011. An essential protein that interacts with endosomes and promotes movement of the SHORT-ROOT transcription factor. Current Biology 21, 1559–1564. Kong D, Karve R, Willet A, Chen MK, Oden J, Shpak ED. 2012. Regulation of plasmodesmatal permeability and stomatal patterning by the glycosyltransferase-like protein KOBITO1. Plant Physiology 159, 156–168. Kurata T, Ishida T, Kawabata-Awai C, et al. 2005. Cell-to-cell movement of the CAPRICE protein in Arabidopsis root epidermal cell differentiation. Development 132, 5387–5398. Le HR, Bellini C. 2013. The plant-specific dof transcription factors family: new players involved in vascular system development and functioning in Arabidopsis. Frontiers in Plant Science 4, 164. Maule AJ, Benitez-Alfonso Y, Faulkner C. 2011. Plasmodesmata: membrane tunnels with attitude. Current Opinion in Plant Biology 14, 683–690. Lee RD , Cho HT . 2013 . Auxin, the organizer of the hormonal/ environmental signals for root hair growth . Frontiers in Plant Science 4, 448 . Lee JY , Lu H. 2011 . Plasmodesmata: the battleground against intruders . Trends in Plant Science 16, 201 - 210 . Lee JY , Wang X , Cui W , et al. 2011 . A plasmodesmata-localized protein mediates crosstalk between cell-to-cell communication and innate immunity in Arabidopsis . The Plant Cell 23 , 3353 - 3373 . Lewis JD , Lazarowitz SG . 2010 . Arabidopsis synaptotagmin SYTA regulates endocytosis and virus movement protein cell-to-cell transport . Proceedings of the National Academy of Sciences , USA 107 , 2491 - 2496 . Li W , Zhao Y , Liu C , Yao G , Wu S , Hou C , Zhang M , Wang D. 2012 . Callose deposition at plasmodesmata is a critical factor in restricting the cell-to-cell movement of soybean mosaic virus . Plant Cell Reports 31 , 905 - 916 . Liang D , White RG , Waterhouse PM . 2012 . Gene silencing in Arabidopsis spreads from the root to the shoot, through a gating barrier, by template-dependent, nonvascular, cell-to-cell movement . Plant Physiology 159 , 984 - 1000 . Ma F , Peterson CA . 2001 . Frequencies of plasmodesmata in Allium cepa L. roots: implications for solute transport pathways . Journal of Experimental Botany 52 , 1051 - 1061 . Maule AJ , Gaudioso-Pedraza R , Benitez-Alfonso Y. 2013 . Callose deposition and symplastic connectivity are regulated prior to lateral root emergence . Communicative and Integrative Biology 6 , e26531 . Mazars C , Thuleau P , Lamotte O , Bourque S. 2010 . Cross-talk between ROS and calcium in regulation of nuclear activities . Molecular Plant 3 , 706 - 718 . McGarry RC , Kragler F. 2013 . Phloem-mobile signals affecting flowers: applications for crop breeding . Trends in Plant Science 18 , 198 - 206 . Molnar A , Melnyk CW , Bassett A , Hardcastle TJ , Dunn R , Baulcombe DC . 2010 . Small silencing RNAs in plants are mobile and direct epigenetic modification in recipient cells . Science 328 , 872 - 875 . Notaguchi M , Wolf S , Lucas WJ . 2012 . Phloem-mobile Aux/IAA transcripts target to the root tip and modify root architecture . Journal of Integrative Plant Biology 54 , 760 - 772 . Oldroyd GE , Downie JA . 2008 . Coordinating nodule morphogenesis with rhizobial infection in legumes . Annual Review of Plant Biology 59 , 519 - 546 . Oparka KJ , Prior D , Wright KM . 1995 . Symplastic communication between primary and developing lateral roots of Arabidopsis thaliana . Journal of Experimental Botany 46 , 187 - 197 . Rinne PL , Welling A , Vahala J , Ripel L , Ruonala R , Kangasjarvi J , van der Schoot C. 2011 . Chilling of dormant buds hyperinduces FLOWERING LOCUS T and recruits GA-inducible 1,3-beta-glucanases to reopen signal conduits and release dormancy in Populus . The Plant Cell 23 , 130 - 146 . Rodriguez-Serrano M , Romero-Puertas MC , Pazmino DM , Testillano PS , Risueno MC , del Rio LA , Sandalio LM . 2009 . Cellular response of pea plants to cadmium toxicity: cross talk between reactive oxygen species, nitric oxide, and calcium . Plant Physiology 150 , 229 - 243 . Rutschow HL , Baskin TI , Kramer EM . 2011 . Regulation of solute flux through plasmodesmata in the root meristem . Plant Physiology 155 , 1817 - 1826 . Salmon MS , Bayer EM . 2012 . Dissecting plasmodesmata molecular composition by mass spectrometry-based proteomics . Frontiers in Plant Science 3, 307 . Schlereth A , Moller B , Liu W , Kientz M , Flipse J , Rademacher EH , Schmid M , Jurgens G , Weijers D. 2010 . MONOPTEROS controls embryonic root initiation by regulating a mobile transcription factor . Nature 464 , 913 - 916 . Schubert M , Koteyeva NK , Wabnitz PW , Santos P , Buttner M , Sauer N , Demchenko K , Pawlowski K. 2011 . Plasmodesmata distribution and sugar partitioning in nitrogen-fixing root nodules of Datisca glomerata . Planta 233 , 139 - 152 . Schubert M , Koteyeva NK , Zdyb A , Santos P , Voitsekhovskaja OV , Demchenko KN , Pawlowski K. 2013 . Lignification of cell walls of infected cells in Casuarina glauca nodules that depend on symplastic sugar supply is accompanied by reduction of plasmodesmata number and narrowing of plasmodesmata . Physiologia Plantarum 147 , 524 - 540 . Sevilem I , Miyashima S , Helariutta Y. 2013 . Cell-to-cell communication via plasmodesmata in vascular plants . Cell Adhesion and Migration 7 , 27 - 32 . Simpson C , Thomas C , Findlay K , Bayer E , Maule AJ . 2009 . An Arabidopsis GPI-anchor plasmodesmal neck protein with callose binding activity and potential to regulate cell-to-cell trafficking . The Plant Cell 21 , 581 - 594 . Slewinski TL , Baker RF , Stubert A , Braun DM . 2012 . Tie-dyed2 encodes a callose synthase that functions in vein development and affects symplastic trafficking within the phloem of maize leaves . Plant Physiology 160 , 1540 - 1550 . Stahl Y , Simon R . 2013 . Gated communities: apoplastic and symplastic signals converge at plasmodesmata to control cell fates . Journal of Experimental Botany 64 , 5237 - 5241 . Stahl Y , Grabowski S , Bleckmann A , et al. 2013 . Moderation of Arabidopsis root stemness by CLAVATA1 and ARABIDOPSIS CRINKLY4 receptor kinase complexes . Current Biology 23 , 362 - 371 . Stonebloom S , Brunkard JO , Cheung AC , Jiang K , Feldman LJ , Zambryski PC . 2011 . Redox states of plastids and mitochondria differentially regulate intercellular transport via plasmodesmata . Plant Physiology 158 , 190 - 199 . Stonebloom S , Burch-Smith T , Kim I , Meinke D , Mindrinos M , Zambryski P. 2009 . Loss of the plant DEAD-box protein ISE1 leads to defective mitochondria and increased cell-to-cell transport via plasmodesmata . Proceedings of the National Academy of Sciences , USA 106 , 17229 - 17234 . Suzuki N , Miller G , Morales J , Shulaev V , Torres MA , Mittler R . 2011 . Respiratory burst oxidases: the engines of ROS signaling . Current Opinion in Plant Biology 14 , 691 - 699 . Thomas CL , Bayer EM , Ritzenthaler C , Fernandez-Calvino L , Maule AJ . 2008 . Specific targeting of a plasmodesmal protein affecting cell-tocell communication . PLoS Biology 6 , e7 . Tucker EB , Boss WF . 1996 . Mastoparan-induced intracellular Ca2+ fluxes may regulate cell-to-cell communication in plants . Plant Physiology 111 , 459 - 467 . Turgeon R , Wolf S. 2009 . Phloem transport: cellular pathways and molecular trafficking . Annual Review of Plant Biology 60 , 207 - 221 . Ueki S , Citovsky V. 2011 . To gate, or not to gate: regulatory mechanisms for intercellular protein transport and virus movement in plants . Molecular Plant 4 , 782 - 793 . Ueki S , Spektor R , Natale DM , Citovsky V. 2010 . ANK, a host cytoplasmic receptor for the Tobacco mosaic virus cell-to-cell movement protein, facilitates intercellular transport through plasmodesmata . PLoS Pathogens 6 , e1001201 . van Bel AJ , Knoblauch M , Furch AC , Hafke JB . 2011 . ( Questions) (n) on phloem biology . 1. Electropotential waves, Ca2+ fluxes and cellular cascades along the propagation pathway . Plant Science 181 , 210 - 218 . Van Norman JM , Breakfield NW , Benfey PN . 2011 . Intercellular communication during plant development . The Plant Cell 23 , 855 - 864 . Vaten A , Dettmer J , Wu S , et al. 2011 . Callose biosynthesis regulates symplastic trafficking during root development . Developmental Cell 21 , 1144 - 1155 . Wright KM , Oparka KJ . 1997 . Metabolic inhibitors induce symplastic movement of solutes from the transport phloem of Arabidopsis roots . Journal of Experimental Botany 48 , 1807 - 1814 . Wu S , Gallagher KL . 2012 . Transcription factors on the move . Current Opinion in Plant Biology 15 , 645 - 651 . Xu M , Cho E , Burch-Smith TM , Zambryski PC . 2012 . Plasmodesmata formation and cell-to-cell transport are reduced in decreased size exclusion limit 1 during embryogenesis in Arabidopsis . Proceedings of the National Academy of Sciences , USA 109 , 5098 - 5103 . Xu XM , Jackson D. 2010 . Lights at the end of the tunnel: new views of plasmodesmal structure and function . Current Opinion in Plant Biology 13 , 684 - 692 . Xu XM , Wang J , Xuan Z , Goldshmidt A , Borrill PG , Hariharan N , Kim JY , Jackson D. 2011 . Chaperonins facilitate KNOTTED1 cell-to-cell trafficking and stem cell function . Science 333 , 1141 - 1144 . Zalepa-King L , Citovsky V. 2013 . A plasmodesmal glycosyltransferaselike protein . PLoS One 8 , e58025 . Zavaliev R , Levy A , Gera A , Epel BL . 2013 . Subcellular dynamics and role of Arabidopsis beta-1,3-glucanases in cell-to-cell movement of tobamoviruses . Molecular Plant-Microbe Interactiona 26 , 1016 - 1030 . Zavaliev R , Sagi G , Gera A , Epel BL . 2010 . The constitutive expression of Arabidopsis plasmodesmal-associated class 1 reversibly glycosylated polypeptide impairs plant development and virus spread . Journal of Experimental Botany 61 , 131 - 142 . Zavaliev R , Ueki S , Epel BL , Citovsky V. 2011 . Biology of callose (beta1,3-glucan) turnover at plasmodesmata . Protoplasma 248 , 117 - 130 .


This is a preview of a remote PDF: https://jxb.oxfordjournals.org/content/65/7/1857.full.pdf

Yoselin Benitez-Alfonso. Symplastic intercellular transport from a developmental perspective, Journal of Experimental Botany, 2014, 1857-1863, DOI: 10.1093/jxb/eru067