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
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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
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
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.
The author gratefully acknowledges Jim Barnes for critical reading and
editing of the manuscript.
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