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FEBS Letters 581 (2007) 2318–2324
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The monosaccharide transporter(-like) gene family in Arabidopsis
Michael Büttner*
Molekulare Pflanzenphysiologie, Universität Erlangen-Nürnberg, Staudtstraße 5, D-91058 Erlangen, Germany
Received 14 February 2007; revised 6 March 2007; accepted 7 March 2007
Available online 15 March 2007
Edited by Ulf-Ingo Flügge and Julian Schroeder
Abstract The availability of complete plant genomes has
greatly influenced the identification and analysis of phylogenetically related gene clusters. In Arabidopsis, this has revealed the
existence of a monosaccharide transporter(-like) gene family
with 53 members, which play a role in long-distance sugar partitioning or sub-cellular sugar distribution and catalyze the transport of hexoses, but also polyols and in one case also pentoses
and tetroses. An update on the currently available information
on these Arabidopsis monosaccharide transporters, on their
sub-cellular localization and physiological function will be given.
Ó 2007 Federation of European Biochemical Societies. Published by Elsevier B.V. All rights reserved.
Keywords: Monosaccharide transport; Hexoses; Polyols;
Sugar compartmentation; Sink development
1. Introduction
In higher plants, sugars play important roles as nutrients as
well as signal molecules during the entire life cycle. While the
green phototrophic parts of the plant (source) synthesize sugars as products of their photosynthetic activity during the
day, non-green parts (sink) depend on a constant import of
carbohydrates delivered via the phloem. In addition, source
and sink cells allocate sugars between different cellular compartments.
This distribution of sugars on the sub-cellular level but also
for long-distance transport requires several essential transport
steps across membranes [1]. In most higher plants, sucrose is
the main transport form for carbon partitioning between
source and sink via the phloem [2]. Upon release from the
phloem, sucrose is either directly transported into sink cells
or, after cleavage of sucrose by an extracellular invertase, the
monosaccharides glucose and fructose taken up [3]. There is
evidence, that the decision whether sucrose or monosaccharides are delivered greatly influences developmental aspects,
as could be demonstrated for the seed development in fava
bean [4,5].
In addition to long-distance carbon partitioning, sugars are
also distributed on the single cell level into different organelles,
depending on the actual requirements. During the day, many
plant species use up to half of their assimilated carbon for
*
Fax: +49 (0) 9131/852 8751.
E-mail address: [email protected]
starch synthesis and transient storage in chloroplasts of source
leaves [6]. At night, transitory starch is degraded phosphorolytically or hydrolytically (primary pathway for export) to
release glucose or maltose, respectively [6,7], which can then
be exported from the chloroplast. There is a number of biochemical studies providing direct evidence for glucose transport across the chloroplast envelope [8,9]. Furthermore,
hexoses can be imported into the vacuole for transient or
long-term storage. Experiments on isolated vacuoles provided
biochemical evidence for the uptake of hexoses into these
organelles , and both mechanisms, passive diffusion as well
as active transport have been suggested [10]. Besides plastids
and vacuoles there might be other sub-cellular compartments
that require the uptake of hexoses and recently it was shown
that also mitochondria import glucose [11].
The application of a non-aqueous fractionation technique
allowed estimates of the relative amounts of sugars in sub-cellular compartments. Measurements of sugar concentrations in
a variety of plants revealed that in leaves the vast majority of
glucose is found in the vacuole [12–17] (Lohaus G., personal
communication).
Besides glucose and fructose, sugar alcohols like sorbitol,
mannitol and myo-inositol are found in many plants [18] and
may also be transported into vacuoles [19,20].
The transport of sugars across membrane barriers is greatly
mediated by transport proteins, which catalyze either passive
(but selective) diffusion or energy-dependent active transport
thereby allowing accumulation of sugar substrates. Despite
the long-standing knowledge of long-distance sugar partitioning and sub-cellular sugar compartmentation, the molecular
cloning and characterization of the corresponding transport
proteins from higher plants did not succeed for decades. For
a long time it was assumed, that each plant has only one transporter for monosaccharides and one transporter for sucrose.
However, after the isolation of the first sugar transport protein
(AtSTP1) from a higher plant by using the HUP1 gene from
the unicellular alga Chlorella kessleri as probe [21,22], things
turned out to be more complicated. Further screening
approaches using PCR or heterologous hybridization lead to
the identification of a family of 14 AtSTP genes in Arabidopsis
[23]. While for the uptake of hexoses across the plasma membrane the transport proteins have been identified for a variety
of plants [1,24], we are only beginning to identify the proteins
responsible for hexose transport on the sub-cellular level
(Fig. 2). Only after the completion of the Arabidopsis genome,
phylogenetic analysis revealed the existence of a monosaccharide transporter(-like) Gene Family with 53 members, which
include good candidates for intra-cellular transporters of
0014-5793/$32.00 Ó 2007 Federation of European Biochemical Societies. Published by Elsevier B.V. All rights reserved.
doi:10.1016/j.febslet.2007.03.016
M. Büttner / FEBS Letters 581 (2007) 2318–2324
and sugar alcohols (see also SUBA: the Arabidopsis Subcellular Database; http://www.suba.bcs.uwa.edu.au). The present
review tries to summarize the currently available information
on these Arabidopsis monosaccharide transporters, on their
sub-cellular localization and physiological function.
2. Arabidopsis monosaccharide transporter(-like) gene family
The MST(-like) family includes 53 genes with significant
homology to known monosaccharide transporters (http://
www.arabidopsis.org/browse/genefamily/Monos.jsp). As depicted in the phylogenetic tree of Fig. 1, these genes can be
grouped into seven distinct sub-families, which clearly have
one common origin. All of these transporters share strong
similarities in their membrane topology with 12 predicted
membrane spanning domains (http://aramemnon.botanik.
uni-koeln.de). Within the sub-families, the homologies are quite
high, ranging from 42% to 96% similarity. When the subfamilies are compared to each other, the degree of homology
significantly drops supporting the grouping of these genes into
distinct families. Although in some cases the overall homology
to the already characterized sugar transporters is relatively low,
all of these proteins show conserved amino acid clusters including two known sugar transport signatures (http://ca.expasy.org/
cgi-bin/nicedoc.pl?PDOC00190), which strongly support a
function of these proteins as sugar transporters.
3. AtSTP (Sugar Transport Protein) genes
To date, the AtSTPs represent the best characterized family
of hexose transporters in Arabidopsis. All known AtSTPs are
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plasma membrane proteins and catalyze the uptake of hexoses
from the apoplastic space into the cell. AtSTP1 was the first
monosaccharide transporter identified in a higher plant [21].
Expression in Schizosaccharomyces pombe and Xenopus oocytes revealed that AtSTP1 is a high-affinity monosaccharide/
proton symporter capable of transporting a range of hexoses
but not fructose [25]. AtSTP1 is most abundant in germinating
seeds and seedling roots [26], where it accounts for up to 60%
of the monosaccharide transport capacity as was shown by uptake studies with an Atstp1 mutant line. Furthermore, AtSTP1
is expressed in guard cells of cotyledons, rosette leaves, sepals,
ovaries and stems [27]. In this cell type, AtSTP1 expression is
strongly increased in the dark and also diurnally regulated
with a peak around midday, which is paralleled by an accumulation of sucrose in guard cells. Thus, a function of AtSTP1 in
monosaccharide import into guard cells during the night and a
possible role in osmoregulation during the day was suggested
[27]. The AtSTP4 gene encodes another high-affinity hexose
transporter and is expressed in root tips, pollen tubes, and
leaves. Interestingly, AtSTP4 expression strongly increases in
response to wounding and pathogen attack [28]. Moreover,
the coordinated expression of AtSTP4 and the invertase gene
Atbfruct1 (AtcwINV1; At3g13790) in the host response to
powdery mildew infection could be demonstrated [29], further
supporting the functional interaction of STPs and cell wall
invertases in the supply of sink tissues with hexoses. The
high-affinity hexose transporter AtSTP2 is found specifically
in pollen, where it most likely is responsible for the uptake
of glucose derived from callose degradation during early
phases of pollen maturation [30]. Surprisingly, three more hexose transporter genes, AtSTP6, AtSTP9 and AtSTP11, were
found to be expressed in pollen during different stages of pollen development [31–33]. AtSTP6 expression is confined to the
Fig. 1. Phylogenetic tree of the monosaccharide transporter(-like) gene family in Arabidopsis. The complete protein sequences of the MSTs were
aligned using the Clustal X algorithm and a phylogenetic tree was constructed using the TreeView 1.6 software. Sub-family names, Munich
Information Center for Protein Sequences (MIPS) codes and gene names (where available) are indicated.
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latest stage in pollen development, when the exine is formed
and the grain is fully developed [32]. AtSTP9, the only AtSTP
known to be specific for glucose, shows an interesting regulation. While the AtSTP9 mRNA was already detectable during
early pollen development, the AtSTP9 protein is found only
after pollen germination in the pollen tube [31]. A similar
regulation was also found for the AtSTP4 gene (R. Stadler,
personal communication). This preloading of pollen with transcripts has already been described for other genes that play a
role in pollen germination and/or pollen tube growth [34]. Finally, AtSTP11 was characterized as a pollen tube-specific
monosaccharide transporter [33]. In view of the high number
of AtSTPs found in pollen it is surprising that no hexose transporter was identified in the female gametophyte to date.
Recently, another high-affinity hexose transporter gene,
AtSTP13, was shown to be expressed in vascular tissue of petals and to be induced during programmed cell death (PCD),
suggesting that hexose transport plays a role in PCD in plants
[35]. All so far characterized AtSTPs are high-affinity hexose
transporters ðK Glc
M 10-100 lMÞ found in sink tissues with one
exception: AtSTP3 has an unusually low affinity for glucose
ðK Glc
M 2 mMÞ and the AtSTP3 gene is expressed in green tissues, where it is proposed to have a function in sugar retrieval
[23]. Interestingly, AtSTP3 is also inducible by wounding and
pathogen attack.
In summary, the AtSTPs are high-affinity (except AtSTP3)
monosaccharide/H+ symporters of the plasma membrane,
which have Km-values for glucose in the micro-molar range
and accept a broad spectrum of monosaccharide substrates
(except AtSTP9). The observed AtSTP expression profiles suggest important roles during sink development (except for
AtSTP3).
4. AtVGT (Vacuolar Glucose Transporter)-like genes
As shown in Fig. 1, the sub-family which stands closest to
the AtSTPs is comprised of three genes, At3g03090,
At5g17010 and At5g59250, which in several databases are
annotated as putative sugar transporters similar to the bacterial xylose permease LbXylT (gi:2895856; Acc AF045552).
However, LbXylT shows significant homology to most MSTlike Transporters ranging from 26% to 42%. In fact, the polyol
transporter PLT6 shows the highest homology to LbXylT, and
several other transporters from different MST-like sub-families
share the same degree of similarity to this bacterial xylose
transporter as the VGT-like proteins, indicating that the
homology does not necessarily reflect substrate specificity. Recently, two genes from this family, AtVGT1 (At3g03090) and
AtVGT2 (At5g17010), have been shown to localize to the vacuolar membrane [36]. For AtVGT1, active transport of glucose
but not xylose was demonstrated by functional expression in
yeast and uptake studies in isolated yeast vacuoles. AtVGT1
is strongly expressed in pollen, at basal levels in leaves and
stems and not detectable in roots. The analysis of Atvgt1 mutant lines indicate an important function of this vacuolar glucose transporter during developmental processes like seed
germination and flowering [36]. In contrast, the gene product
of At5g5925, the third member of this sub-group, seems to
be localized in the chloroplast membrane. The encoded protein
has an N-terminal extension carrying a potential plastid target
signal and was identified in chloroplast membrane prepara-
M. Büttner / FEBS Letters 581 (2007) 2318–2324
tions during independent proteomic approaches (see SUBA
database: http://www.suba.bcs.uwa.edu.au).
5. AtTMT (Tonoplast Monosaccharide Transporter) genes
The AtTMT sub-family is composed of three MST homologs with an extended middle loop between the putative transmembrane helices six and seven. Such an extended cytoplasmic
domain is also present in the sucrose transporter AtSUT2/AtSUC3, which was therefore discussed as possible sugar sensor
[37] due to the structural resemblance to the yeast glucose sensors SNF3 and RGT2. However, neither for AtSUT2/AtSUC3
nor for the AtTMTs a function in sugar sensing could be demonstrated so far. Proteomic studies of the Arabidopsis and barley tonoplast indicated the presence of AtTMT transporters in
the vacuolar membrane [38,39]. This could be further supported in a recent study by Wormit and coworkers, showing
that AtTMT-GFP fusions localize to the tonoplast and that
Attmt mutant lines upon cold stress accumulate less glucose
in the vacuole than wildtype plants [40]. AtTMT1 and
AtTMT2 expression is induced by stresses like drought, salt
and cold and by sugars indicating that AtTMTs play a role
in vacuolar hexose transport, mainly under stress conditions.
(For additional information on vacuolar transporters see also
E. Neuhaus, ‘‘Vacuolar transport’’; in this issue).
6. AtpGlcT (Plastidic Glucose Transporter) genes/AtSGB1
(Suppressor of G Protein Beta1)
Using a differential labeling strategy, a putative glucose
transporter pGlcT of the chloroplast inner envelope membrane
was identified in spinach [41]. The corresponding gene in Arabidopsis has three close homologs (43–71% amino acid similarity), which together form the sub-family of putative plastidic
glucose transporters, named after the spinach pGlcT.
A function of pGlcTs in the export of glucose derived from the
amylolytic breakdown of transitory starch was suggested [41],
however, a direct proof of transport activity as well as a mutant
analysis to support this function is missing to date. Interestingly,
it was recently suggested that plastidic glucose efflux is an active
process coupled with the transport of a proton [9]. (For detailed
information on chloroplast glucose transporters see also Weber
and Fischer, ‘‘Plastid Transport’’; in this issue).
Despite the high homology (42–69% similarity) within this
sub-family, not all members are found in plastids. Recently,
SGB1 (suppressor of G protein beta1) was identified as a
Golgi-localized hexose transporter homolog [42]. Arabidopsis
agb1 mutant seedlings, which lack the b-subunit (AGB1) of
the heterotrimeric G protein complex, have reduced number
of cells due to altered cell division in the hypocotyl and are
D -glucose hypersensitive. In a screen for gain-of-function suppressors of the agb1 mutation, SGB1 was found to restore cell
number and hypocotyl length. Some components of the newly
synthesized cell wall like pectins and xyloglucans are assembled in the Golgi. One explanation, how SGB1 overexpression
could rescue hypocotyl length in the agb1 mutant, could be elevated glucose transport into the Golgi thereby increasing cell
wall synthesis [42]. It will be interesting to see, whether this
sub-family is further divided into groups with different sub-cellular localization and function.
M. Büttner / FEBS Letters 581 (2007) 2318–2324
7. AtPLT (Polyol Transporter) genes
Polyols are osmotically active solutes that accumulate in a
number of plants in response to cold, water or salt stress
[18]. The first plant mannitol transporter AgMaT1 was isolated from celery by complementation of a yeast mutant [43].
Also in Arabidopsis, sugar alcohols seem to play a role and
the corresponding transport proteins have been identified
and partially characterized [44–46], but so far the physiological
functions of these transporters are unclear. Within the MST(-like) family, six genes share significant homology with previously identified polyol transporters. Analysis of AtPLT5, the
first member of this sub-group, revealed that this transporter
resides in the plasma membrane and is a broad-spectrum
H+-symporter for linear polyols, such as sorbitol, xylitol,
erythritol, or glycerol, but also the cyclic polyol myo-inositol
and different hexoses and pentoses including ribose, tetroses
and a sugar acid [44,45]. AtPLT5 is primarily expressed in sink
tissues, most strongly in the root elongation zone, but also in
the vascular tissue of leaves and some floral organs like siliques
and the floral abscission zone [44,45]. Polyols are also found in
the vacuole. In celery, mannitol is transiently stored in the vacuoles of the parenchyma cells of petioles where it crosses the
tonoplast by passive diffusion [20]. In contrast, sorbitol is
actively transported into vacuoles in apple fruit [19]. However,
none of the AtPLT gene products was localized to the tonoplast so far.
8. AtINT (Inositol Transporter) genes
Inositol (in muscle cells called myo-inositol) is an ubiquitous
cellular component in a variety of organisms including plants.
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It is mostly phosphorylated and functions in cellular signalling
(inositol triphosphate, IP3), as structural component of membranes (phosphatidylinositol) and as storage form of phosphorus in seeds (phytate). The four members of the Arabidopsis
MST(-like) family show strong homology to myoinositol
transporters from yeast and human and to the myo-inositol
transporters MITR1 and MITR2 from Mesembryanthemum
crystallinum (common ice plant) [47]. In contrast to MITR1
and MITR2, which are thought to catalyze Na+/myo-inositol
symport and were localized in the tonoplast, the Arabidopsis
AtINT4 is a highly specific myo-inositol/proton symporter
and was found in the plasma membrane [46]. AtINT4 is
strongly expressed in pollen and phloem companion cells,
where it could function in phloem loading with myo-inositol,
possibly to allow raffinose synthesis [46]. MITR1 and MITR2
from M. crystallinum were found in the tonoplast and are
thought to play a role in salt tolerance. Interestingly, in a
recent proteome analysis, AtINT1, another member of this
Arabidopsis sub-family, was also identified as a vacuolar membrane protein. However, since proteomic approaches often
produce a small number of false-positives, this result has to
be reconfirmed by an independent method.
9. AtERD6-like genes
The 19 AtERD6-like genes represent the least investigated
sub-group in the MST(-like) family, which share 48–95% similarity with each other. The AtERD6-homologs were named
after the ERD6 (early-responsive to dehydration) gene, which
is coding for a putative sugar transporter [48]. The ERD6 gene
is induced upon dehydration and cold treatment, but expression studies in yeast were not successful in proving sugar
Fig. 2. Schematic illustration of the sub-cellular distribution of monosaccharides and the localization determined for MST(-like) transporters. The
transport direction for glucose, fructose and polyols into the cell and within the cell is indicated by arrows and the corresponding transporter names
are given in boxes (STP: Sugar Transport Protein, VGT: Vacuolar Glucose Transporter, TMT: Tonoplast Monosaccharide Transporter, pGlcT:
Plastidic Glucose Transporter, SGB1: Suppressor of G protein Beta1, PLT: Polyol Transporter, INT: Inositol Transporter, ERD6-like: earlyresponsive to dehydration).
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transport activity [48]. Furthermore, this family includes two
closely related MST homologs, SFP1 and SFP2 (sugar-porter
family protein), that are found as tandem genes on chromosome 5 [49]. Both genes are differentially regulated and SFP1
was shown to be senescence-induced, which is paralleled by
an accumulation of monosaccharides in such tissues. However,
for both, SFP1 and SFP2, the functional characterization is
missing so far. Interestingly, some AtERD6 genes show high
homology to a putative sugar transporter from Beta vulgaris,
that was shown to be located in the vacuolar membrane by
co-localization studies, but also for this sugar beet homolog
transport activity could not be demonstrated [50]. A similar
localization for at least some members of the AtERD6 subgroup was suggested by expression studies of GFP fusion
proteins (Büttner and Hannich, unpublished results). This is
further supported by the identification of At1g75220 and
At1g19450, the two AtERD6 members most homologous to
the sugar beet transporter, in a recent proteomic search for
tonoplast proteins [39].
The AtERD6 genes also show considerable homology to the
mammalian GLUT family. These glucose transporters are
facilitators, which raises the possibility that the AtERD6 transporters differ from the known plant monosaccharide transporters mechanistically. So far, such sugar transporters that
facilitate an energy-independent monosaccharide transport
(influx and/or efflux) have not been identified in plants. Possibly, AtERD6 homologs play a role in the transport of sugars
out of the vacuole during conditions, where a re-allocation
of carbohydrates is important (Fig. 2). Such conditions include
senescence, wounding, pathogen attack, C/N-starvation as well
as diurnal changes in transient storage of sugars in the vacuole.
According to the Genevestigator database (https://www.genevestigator.ethz.ch), several of the AtERD6 genes are strongly
regulated in response to some of these developmental and environmental signals.
10. Conclusions
The availability of complete plant genomes has greatly influenced the identification and analysis of phylogenetically
related gene clusters. In Arabidopsis, this has lead to an
enormous progress in the elucidation of common functional
characteristics but also divergence within gene families like
the monosaccharide transporter(-like) gene family. In deed,
MST genes form distinct sub-families share certain features,
however, the currently available data also show that the degree
of homology does not necessarily reflect sub-cellular localization or substrate specificity. So far, substrate sugars known
to be transported by MSTs include mainly hexoses, but also
polyols and in one case (AtPLT5) also pentoses and tetroses.
11. Monosaccharide transporters in other plants
The number of EST libraries and even complete genomes
from different plant species is constantly growing. The evolutionary aspects of plant monosaccharide transporters have
been addressed recently by Johnson et al. [51], and in this
excellent study the authors conclude that the seven MST
sub-families of Arabidopsis are ancient in land plants and all
have homologs present in land plants at least 400 million years
M. Büttner / FEBS Letters 581 (2007) 2318–2324
ago. In some cases, the analysis of the corresponding orthologs
in other plants might help to elucidate the biological function
of MST(-like) transporters.
12. Future goals
Despite the appreciable progress in the analysis of MST(like) transporters in Arabidopsis, important questions concerning individual members but also entire sub-families have to be
addressed in the future.
(i) There is an exceptionally high number of AtSTPs expressed in pollen. This is particularly surprising, since
in vitro pollen germination requires sucrose and the
addition of glucose leads to an instantaneous burst of
the pollen tubes [52]. AtSTPs are found during different
stages of pollen development, however, knockouts mutants of individual AtSTPs are fertile and not affected
in pollen maturation [31–33]. The importance of sugar
supply during this essential step in plant reproduction
has to be further demonstrated by the analysis of multiple AtSTP knockout mutants to determine the distinct
roles of individual AtSTPs during pollen development,
germination, and pollen tube growth.
(ii) Another open question is how fructose, which is generated by sucrose-cleavage in the apoplast, enters the cell.
Only two of the so far characterized AtSTPs transport
fructose at significant rates but they are not expressed
in all sink tissues [32,35]. Either the AtSTP transport
properties found in heterologous systems do not completely reflect the in planta situation, or another family
of plasma membrane transporters is responsible for the
fructose uptake (Fig. 2), as recently suggested for
AtPLT5 [44,45].
(iii) Candidates from different sub-families have been localized to the same compartment. This was found for
AtVGTs, AtTMTs and several AtERD6-homologs in
the vacuolar membrane and for pGlcT and one
AtVGT-homolog in the chloroplast membrane. It will
be important to sort out the individual functions and
requirements of these transporters in the corresponding
compartment. In addition, it was shown recently that
within the plasma membrane so-called lipid rafts form
microdomains leading to an intra-membrane compartmentation. Interestingly, the HUP1 hexose transporter
is restricted to such microdomains in yeast [53]. It remains to be seen if this compartmentation within membranes is important for the activity/stability of plant
MSTs and if it is also found in intracellular membranes.
(iv) Relatively little is known about the regulation of MSTs
on both, the transcriptional and post-transcriptional
level. Microarray data indicate an effect of a wide range
of developmental and external factors on the expression
of MST genes. In grape vine, the promoter of the hexose
transporter gene VvHT1 contains two sugar boxes, and
its activity is induced by sucrose and glucose. Furthermore, binding of the ABA-inducible transcription factor
VvMSA to these promoter boxes was demonstrated,
suggesting that VvMSA is involved in a common transduction pathway of sugar and ABA signaling [54]. In
addition, MST-mediated sugar transport might be regulated on the protein level. A large-scale screening for
M. Büttner / FEBS Letters 581 (2007) 2318–2324
in vivo phosphorylated membrane proteins identified a
phosphorylation-site in the AtSTP1 protein (Nühse
T.S. and Peck S.C., personal communication) [55] and
studies with kinase activators suggest that AtSTP13 is
negatively regulated by phosphorylation [35].
Sugar supply is essential for sink organ development, which
can be significantly improved by modulating the sink strength.
This was demonstrated by the expression of a cell wall invertase [56] and also changes in the corresponding transport steps
into cells and/or cellular compartments could have similar
effects. Some agriculturally important plants like sugar beet
[57] and sugar cane [58] store a considerable amount of sugars
in the vacuoles of storage organs. Therefore, future studies will
have to elucidate the role of MST(-like) transporters in
long-distance and sub-cellular sugar partitioning and its
impact on plant development and plant responses to external
factors.
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