trends in plant science
Reviews
Sugar transporters in higher
plants – a diversity of roles
and complex regulation
Lorraine E. Williams, Remi Lemoine and Norbert Sauer
Sugar-transport proteins play a crucial role in the cell-to-cell and long-distance distribution of
sugars throughout the plant. In the past decade, genes encoding sugar transporters (or carriers) have been identified, functionally expressed in heterologous systems, and studied with
respect to their spatial and temporal expression. Higher plants possess two distinct families of
sugar carriers: the disaccharide transporters that primarily catalyse sucrose transport and the
monosaccharide transporters that mediate the transport of a variable range of monosaccharides. The tissue and cellular expression pattern of the respective genes indicates their
specific and sometimes unique physiological tasks. Some play a purely nutritional role and
supply sugars to cells for growth and development, whereas others are involved in generating
osmotic gradients required to drive mass flow or movement. Intriguingly, some carriers might
be involved in signalling. Various levels of control regulate these sugar transporters during
plant development and when the normal environment is perturbed. This article focuses on
members of the monosaccharide transporter and disaccharide transporter families, providing
details about their structure, function and regulation. The tissue and cellular distribution of
these sugar transporters suggests that they have interesting physiological roles.
I
n higher plants, CO2 fixation occurs predominantly in mesophyll cells of mature leaves. These are net exporters of sugars
and are known as ‘carbon sources’. Heterotrophic cells in
roots, reproductive structures, storage and developing organs rely
on a supply of sugars for their nutrition; these are known as ‘carbon sinks’ (net importers). Mechanisms must exist to ensure that
all sink tissues receive an adequate supply of sugars for growth
and development, and sugar transporters play a pivotal role in the
membrane transport of sugars and their distribution throughout
the plant (Fig. 1).
Long-distance transport of carbohydrates between sources and
sinks occurs in specific cells of the vascular system, the phloem
sieve elements (Fig. 1). During their development, sieve elements
extend longitudinally, degrade most of their organelles, including
vacuoles, ribosomes and nuclei, and form large, plasma membrane-lined pores in their terminal cell walls, the sieve plates. The
loss of organellar structures in sieve elements is paralleled by an
extreme increase in organelle density in the phloem companion
cells. Sieve elements and companion cells are intimately connected by numerous branched plasmodesmata and form the socalled sieve element–companion cell complex (SE–CCC). An
important function of companion cells is the supply of energy and
proteins to the sieve elements.
Phloem sap in sieve elements moves by bulk flow with rates of
up to 1 m per h. At the source, accumulation of sugar inside the
SE–CCC (at a concentration of several hundred mM to .1 M)
results in the osmotic uptake of water, forcing sap to flow along
the sieve tube. Unloading of sugar at the sink results in loss of
water from the sieve tube and thus the gradient of pressure is
maintained. Sucrose represents the main form of reduced carbon
transported in sieve elements, although some plants can also
transport raffinose, stachyose and polyols. These solutes are less
subject to metabolism than glucose. After its synthesis, sucrose
can pass the entire route from the mesophyll cells to the sieve
element–companion cell in the symplast, moving from cell to cell
via plasmodesmata (symplastic loading; Fig. 1). However, frequently, sucrose is released from the mesophyll cells and actively
loaded from the apoplast into the SE–CCC (apoplastic loading).
Plasma membrane sucrose–H1 symporters are fundamental to this
process. Unloading of sucrose at the sinks might also occur either
symplastically or apoplastically. The route depends on species
(both pathways might operate in the same organism), organ or
tissue, and developmental stage. Sink cells either import sucrose
from the apoplast directly via sucrose transporters or, alternatively,
sucrose can be hydrolysed to glucose and fructose by cell-wallbound invertases and taken up via monosaccharide transporters.
Plants appear to have several monosaccharide and disaccharide
transporters to coordinate sugar transport in diverse tissues, at different developmental stages and under varying environmental
conditions. The nomenclature in the literature for plant sugar
transporters has become rather confusing with SUT and SUC
being used for disaccharide transporters, and STP, MST, HEX
and ST being used for monosaccharide transporters. Here we will
refer to disaccharide transporters as DSTs and refer to monosaccharide transporters as MSTs. Some of the physiological functions of these sugar transporters, as suggested from work at the
molecular level, will be discussed. Other proteins that have been
implicated in the transport of sugars [e.g. sugar-binding protein,
SBP (Ref. 1)] will not be considered here.
Multi-gene families for sugar transporters
In Arabidopsis, 14 putative MST genes have been identified to
date2 and at least seven DST genes can be found in Arabidopsis
data libraries. Heterologous expression in yeast or Xenopus
oocytes has been carried out for some of the family members, and
evidence suggests that they function as proton symporters3–8. Generally the DSTs are highly specific for sucrose, although some
have been shown to transport maltose9. Their Km values are in the
1360 - 1385/00/$ – see front matter © 2000 Elsevier Science Ltd. All rights reserved. PII: S1360-1385(00)01681-2
July 2000, Vol. 5, No. 7
283
trends in plant science
Reviews
P
P
Autotrophic
source cell
Companion
cell
S
H+
S
?
Sieve elements
Water
ATP
H
Source
+
ADP+Pi
H+
S
S
(Fig. 4). Only a few DSTs and MSTs have
been localized precisely at the membrane
level12,13. Many authors have simply
assumed that these proteins are localized at
the plasma membrane, because they are
targeted to this membrane in transgenic
yeast. Detailed studies are required to confirm this for each family member. Some of
the more interesting physiological functions of a range of sugar transporters, as
suggested from work at the molecular
level, are discussed below.
Phloem-associated sucrose transporters
S
In apoplastic phloem loading, a DST protein
at the plasma membrane of phloem cells accuS
mulates sucrose in the SE–CCC to drive longdistance transport (Figs 1 and 4). In some
Path
plants these sucrose transporters have been
S
S
detected in sieve elements (Ref. 12), whereas
+
H
others have been observed in companion
G+F
cells14,15. This might be explained by species
+
+
H G
S H
differences, but recent work in Plantago has
shown that there are sucrose transporters speInvertase
cific to either companion cells or sieve elS
S
ements (R. Stadler et al., unpublished). All of
these transporters result from gene transcripP
tion in the companion cell, and it will be
Sink
Heterotrophic
important to determine the signals and mechsink cell
anisms that regulate their final destination. In
Solanaceae, SUT1 (DST) mRNA is localized
in the sieve elements, suggesting that tranWater
scription occurs in the companion cell and
Trends in Plant Science
might be followed by the transportation of
mRNA through the plasmodesmata and transFig. 1. The contribution of sugar transporters to long-distance sugar transport between sources
lation within the sieve elements12.
and sinks. Long-distance transport of sucrose (S) between sources and sinks occurs in sieve
In Solanaceous species, antisense studies
elements of the phloem, which constitute part of the vascular system (path). Sucrose is transported in the phloem sap by bulk flow. In the source leaf, sucrose can pass the entire route from
have shown that SUT1 (DST) is indeed
the mesophyll cells (source cell) to the sieve element–companion cell in the symplast, moving
essential for phloem loading and long-disfrom cell to cell via plasmodesmata (P). However, in many species, sucrose leaves the symplast
tance transport16,17. Potato plants with drastiat some point, possibly via sucrose efflux carriers (red circle), and is actively accumulated from
cally lowered expression of SUT1 (DST)
the apoplast into sieve elements and/or companion cells by plasma membrane proton–sucrose
had a reduced tuber yield (size and number),
symporters (purple and dark-blue circles, respectively). Energization is via the proton-motive
and mature leaves accumulated sugars
force generated by the plasma membrane H1-ATPase (black square). Passive influx of water
because of impaired export16,17. This was
into the sieve tubes presumably occurs via water channels. Expression of sucrose carriers
confirmed in tobacco, where strong anti(light-green circle) along the path has been related to a function for retrieving sucrose leaked
sense plants had a dwarf phenotype, and
from the phloem. Unloading of sucrose into sink cells might occur symplastically via plassugar export from leaves was also drastimodesmata or sucrose might be delivered to the apoplast via a sucrose efflux carrier (pink circle). Here, it is either taken up directly by plasma membrane sucrose transporters (yellow
cally impaired18. In wild-type plants,
circle), or first hydrolysed to glucose (G) and fructose (F) by the cell-wall invertase (dark-green
lengthy dark exposure leads to starch degraelipse) then taken up via plasma membrane monosaccharide transporters (light-blue circle).
dation in leaves and subsequent exportation
of sucrose to sink organs. However, in antisense plants, starch remains in the leaves
0.3–1.0 mM range9. The MSTs have broader substrate specificity, and this is related to impaired sucrose export. Phloem-localized
transporting a range of hexoses and pentoses with Km values for the SUT1 (DST) homologues might play an additional role in both the
preferred substrate being typically 10–100 mM (Ref. 2). MSTs and retrieval of sucrose leaking from sieve elements along the transloDSTs share little homology at the amino acid level, although there cation pathway and possibly in catalysing the export of sucrose
are structural similarities (Fig. 2). They are thought to be members of from the phloem in sinks19 (Fig. 1). Moreover, the same transporters
the major facilitator superfamily10,11. Whereas DST genes appear to are not always confined to the phloem but are also present at lower
be specific for plants, numerous genes that are homologous to the levels in other leaf cells where they might function in retrieval17,20.
MSTs are found in bacteria, fungi and mammals (Fig. 3).
Sugar transporters in roots
Diverse locations for sugar transporters
Plant cells appear to possess sugar transporters tailored to meet
their specific requirements at particular stages of development
284
July 2000, Vol. 5, No. 7
Roots represent heterotrophic carbon sinks and can be divided
into zones of cell division, elongation and maturation. AtSTP4
(MST), a monosaccharide transporter from Arabidopsis, is found
trends in plant science
Reviews
only at the root tip, probably in the root
meristem21 (Fig. 4). This indicates that part
of the post-phloem transport in Arabidopsis
roots occurs apoplastically and that the role
of AtSTP4 (MST) is to import hexoses generated from sucrose hydrolysis by cell-wall
invertase following phloem unloading. In
Medicago truncatula, the gene for the
monosaccharide transporter, Mtst1 (MST),
is only expressed in cells immediately
behind the root apical meristem, in cells
within the elongation zone and possibly in
the zone of cell division22. Elongating cells
have a high requirement for hexoses as precursors for macromolecular synthesis and
to allow them to maintain osmotic pressure
during elongation22. Mtst1 (MST) is also
expressed in primary phloem fibres where it
might provide hexoses for cell wall biosynthesis and deposition22.
Sucrose transporters have also been
detected in particular cells of the root:
DcSUT2 (DST) is expressed in storage
parenchyma tissues of carrot tap-roots
where it seems to import sucrose for storage23. This and other DST homologues
have also been detected in phloem cells of
the root, where they might retrieve sucrose
into the phloem or possibly catalyse the
efflux of sucrose from the phloem19.
A role for sugar transporters in developing
and germinating seeds
(a)
Disaccharide-H+-symporter (PmSUC2)
400
120
50
220
350
170
90
470
300
440
270
1
510
Cytoplasmic side
Monosaccharide-H+-symporter (NtMST1)
(b)
50
380
80
140
310
450
200
20
The developing embryo is symplastically iso410
lated from maternal tissues and is reliant on
480
230
the import of sugars from the surrounding
apoplastic space. Sugars are required for
embryo development and for the deposition
1
of storage compounds necessary for germi270
nation. DSTs and MSTs have been identified
Cytoplasmic side
in Vicia faba, Pisum sativum and Hordeum
vulgare (Refs 24–26). In Vicia, VfSTP1
523
(MST) is expressed in the embryo cotyledon
epidermal cells. Expression is confined to epiTrends in Plant Science
dermal regions covering the mitotically active
Fig. 2. Topological models of the disaccharide–H1symporter, (a) PmSUC2 [disaccharide
parenchyma, indicating that this transporter
24
transporter
(DST)] and (b) the monosaccharide–H1 symporter, NtMST1 [monosaccharide
serves to supply substrate for metabolism .
transporter (MST)]. MSTs and DSTs have predicted molecular masses of ~55 kDa and
During later stages of embryo development,
hydrophobicity analysis indicates that they are highly hydrophobic integral membrane proVfSTP1 (MST) is replaced by the sucrose
teins. They share little homology at the amino acid level, although there are structural simi24
transporter VfSUT1 (DST) . VfSUT1 (DST)
larities and they are thought to be members of the major facilitator superfamily. In this family,
expression is highest in epidermal cells with
it is proposed that the twelve transmembrane a-helical structure has evolved from an ancestransfer-cell morphology and with storage
tral six-transmembrane-segment transporter gene following gene duplication and fusion10.
activity in the underlying parenchyma, indiFamily members generally possess a large central loop between transmembrane domains six
and seven (the length of this loop varies in members of the DST and MST families).
cating that the encoded transporter is responsible for providing substrate for the synthesis
of storage compounds24.
Certain seeds accumulate storage reserves in the endosperm dur- is transferred symplastically to the phloem region. The high expresing development. Upon germination, these are hydrolysed and the sion of RcSUT1 (DST) in the phloem indicates that sugars are
products, including sugars, are released into the apoplastic space released into the apoplast before active loading by this transporter.
(Fig. 5). In germinating seeds of Ricinus communis, a sucrose carrier, RcSUT1 (DST), is expressed at high levels in both the coty- A variety of roles for sugar transporters in floral organs
ledon epidermal cells that are situated adjacent to the endosperm Developing pollen grains are strong sinks that require carbohyand also in the phloem13. This suggests that the epidermal cells ini- drate import from the apoplast during maturation, germination
tially accumulate sucrose from the apoplast and from here sucrose and growth. The Arabidopsis monosaccharide transporter gene,
July 2000, Vol. 5, No. 7
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(a)
(b)
EcXyIE
SspGTR
EcAraE Prokaryotes
EcGaIP
AtERD6
HsGLUT1 Mammal
ScHXT2
100
46
ScGAL2
98
ScHXT1
100
99
Fungi
ScHXT3
AmMST1
96
ScSNF3
100
ScRGT2
CkHUP2
97
CkHUP1 Lower plants
100
CkHUP3
NtMST1
VvMST1
42
48
RcSTC
30
AtSTP1
100 18
AtSTP12
VfMST1
99
95
MtMST1
AtSTP4
76
PhPMT1
100
64
AtSTP11
78
99
AtSTP10
100
AtSTP9
RcHEX6
100
77
AtSTP3
SspSGT2
100
RcHEX1
90
AtSTP7
89
97
PaMST1
100
AtSTP14
81
AtSTP13
100
LeMST1
AtSTP2
75
AtSTP6
100
AtSTP8
100
100
20
71
40
EcMeIB
AtSUC3
100
Arabidopsis
HvSUT1
100
Monocots
OsSUT1
54
HvSUT2
99
DcSUT1
97
Arabidopsis
AtSUC4
PmSUC1
100
100
21
BvSUT1
SoSUT1
AmSUT1
89
AbSUT1
84
95
PmSUC2
29
56
Plants
with symplastic
phloem loading
StSUT1
100
NtSUT1
VfSUT1
Higher
plants
AtSUC2
35
AtSUC13
100
71
100
AtSUC8
84
66
100
Arabidopsis
AtSUC1
AtSUC5
DcSUT2
AgSUT1
Trends in Plant Science
Fig. 3. Phylogenetic analysis for (a) monosaccharide transporters (MSTs) and (b) disaccharide transporters (DST). (a) Sugar-transport proteins homologous to lower and higher plant monosaccharide transporters are found in prokaryotes, fungi and mammals, indicating that the
corresponding genes form an ancient gene family. Monosaccharide transporters from one species, such as the Arabidopsis AtSTPs, do not
form a single subcluster within the higher plant subfamily, suggesting that several independent genes already existed at the beginning of or
early in higher plant evolution. The less closely related Arabidopsis AtERD6 protein (Accession no. D89051), described as a putative sugar
transporter, clusters with the human glucose facilitator. (b) Proteins closely related to higher plant sucrose transporters are not found in bacteria, fungi or mammals, indicating that plant sucrose-transporter genes evolved comparatively late. Sucrose transporters from Arabidopsis
cluster together with sucrose transporters from monocots and from plants with symplastic phloem loading. A functionally uncharacterized
transporter from Schizosaccharomyces pombe (Accession no. Z99165) shows some similarity, but only in the N-terminal half of the protein.
EcMelB (the outgroup) is extremely distantly related to plant sucrose transporters45. Bootstrap values given at internal nodes indicate the percentage of the occurence of these nodes in 100 replicates (maximum parsimony) of the data set. The sequence of the E. coli xylose permease (EcXylE; black) and of the E. coli melibiose transporter (EcMelB; black) were used as outgroups in (a) and (b), respectively. Accession
numbers for nonplant monosaccharide transporter sequences are AmMST1 (Amanita muscaria monosaccharide transporter), Z83828;
EcAraE (E. coli arabinose transporter), J03732; EcGalP (E. coli galactose permease), AE000377; EcMelB (E. coli melibiose transporter),
K01991; EcXylE (E. coli xylose transporter), P09098; HsGlut1 (Homo sapiens glucose transporter), 87529; ScHXT1 (Saccharomyces cerevisiae hexose transporter), M82963; ScHXT2 (S. cerevisiae hexose transporter), M33270; ScHXT3 (S. cerevisiae hexose transporter),
L07080; ScRGT2 (S. cerevisiae hexose transporter-like glucose sensor), Z74186; ScSNF3 (S. cerevisiae hexose transporter-like glucose sensor), J03246; SspGTR (Synechocystis sp. glucose transporter), X16472. Maximum parsimony (MP) bootstrap analyses of aligned sequences
were conducted with the PHYLIP package 3.572c. Addition of taxa was jumbled and repeated three times for each individual bootstrap replication in the MP analysis. Output treefiles were combined with the CONSENSE program and converted into a graphical representation by the
TREEVIEW program. Accession numbers of plant sucrose transporters used in this tree are AbSUT1 (Asarina barclaiana, AF191024);
AgSUT1 (Apium graveolens, AF063400); AmSUT1 (Alonsoa meridionalis, AF191025); AtSUC1 (Arabidopsis thaliana, X75365);
AtSUC2 (A. thaliana, X75382); AtSUC3 (A. thaliana, AC004138); AtSUC4 (A. thaliana, AC000132); AtSUC5 (A. thaliana, AJ252133);
AtSUC8 (A. thaliana, AAC69375); AtSUC13 (A. thaliana, AB016875); BvSUT1 (Beta vulgaris, X83850); DcSUT1 (Daucus carota,
Y16766); DcSUT2 (D. carota, AB036758); HvSUT1 (Hordeum vulgare, Accession no. not yet available); HvSUT2 (H. vulgare, Accession
no. not yet available); NtSUT1 (Nicotiana tabacum, X82276); OsSUT1 (Oryza sativa, D87819); PmSUC1 (Plantago major,
X75764); PmSUC2 (P. major, X75764); SoSUT1 (Spinacea oleracea, X67125); StSUT1 (Solanum tuberosum, X69165); VfSUT1
(Vicia faba, Z93774). Accession nos of plant monosaccharide transporters used in this tree are AtSTP1 (A. thaliana, X55350); AtSTP2
(A. thaliana, AJ001362); AtSTP3 (A. thaliana, AJ002399); AtSTP4 (A. thaliana, X66857); AtSTP6 (A. thaliana, AC013454); AtSTP7
(A. thaliana, AF001308); AtSTP8 (A. thaliana, AF077407); AtSTP9 (A. thaliana, AC007980); AtSTP10 (A. thaliana, AB025631); AtSTP11
(A. thaliana, AB007648); AtSTP12 (A. thaliana, AL022603); AtSTP13 (A. thaliana, AF077407); AtSTP14 (A. thaliana, AC004260);
CkHUP1 (Chlorella kessleri, Y07520); CkHUP2 (C. kessleri, X66855); CkHUP3 (C. kessleri, X75440); LeMST1 (Lycopersicum
esculentum, AJ010942); MtMST1 (Medicago truncatula, U38651); PaMST1 (Picea abies, Z83829); PhPMT1 (Petunia hybrid, AF061106);
RcHEX1 (Ricinus communis, L08197); RcHEX6 (R. communis, L08188); RcSTC (R. communis, L08196); SspSGT2 (Saccharum hybrid,
L21753); VfMST1 (V. faba, Z93775); VvMST1 (Vitis vinifera, AJ001061).
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trends in plant science
Reviews
AtSTP2 (MST), is expressed after meiosis
of the pollen mother cell at the time when
the uninucleate microspores are develop(e)
ing27. This correlates with the time when
callose surrounding the microspores is
Papilla
(d)
degraded. After this, AtSTP2 (MST)
Pollen tube
27
mRNA and protein are rapidly degraded .
Thus, AtSTP2 (MST) could serve in the
Transmitting
uptake of glucose (resulting from callose
tissue
degradation) and also other monosaccharides such as xylose, mannose or galactose
(from degradation of other cell-wall components) into the symplastically isolated,
Pollen
Pollen
developing male gametophyte27.
sac
Carbohydrates are also required to supConnective
ply energy for pollen germination and
(a)
(b)
tissue
pollen-tube growth. PhPMT1 (MST), a
putative hexose transporter gene in Petunia, is expressed specifically in mature
Xylem
anthers and pollen, and not in any other flovessel
ral or vegetative tissues28. Thus, in this
Companion
species, sucrose might be hydrolysed to
cells
glucose and fructose by a cell-wall invertase before uptake by PhPMT1 (MST) in
the growing pollen tube28. A similar local(c)
ization has been shown for the Arabidopsis
AtSTP4 (MST) monosaccharide transporter21 (Fig. 4); however, its function is
unclear because in this species (and in
many others) sucrose is the preferred carbon source during pollen germination and
growth in vitro. Recent studies describing
the expression of the sucrose transporter
genes, AtSUC1 (DST) in germinating Arabidopsis pollen (Fig. 4) and NtSUT3 (DST)
in tobacco pollen, are consistent with
this29,30. Interestingly, AtSUC1 (DST)
mRNA was detected in developing pollen
whereas the protein was only found after
pollen germination, indicating that expresFig. 4. Tissue and cellular distribution of various sugar transporters. The tissue or cell-specific
sion might be translationally regulated and
expression of several sugar transporters indicates their specific physiological tasks. For example,
induced during germination29.
sugar transporters have been implicated in processes as diverse as phloem loading and unloading,
AtSUC1 (DST) is also expressed in a
pollen development and germination, and pathogen interaction. (a) Expression of the sucrose
ring of parenchymatic cells surrounding
transporter gene AtSUC2 (disaccharide transporter, DST) in the veins of Arabidopsis source leaves
the transmitting tissue of the style and in
indicates a role in phloem loading. The expression is demonstrated by the activity of the reporter
29
the epidermal cell layers of the funiculi .
gene for b-glucuronidase (GUS) driven by the AtSUC2 promoter19. In (b), the AtSUC2 (DST)
This expression pattern is unlikely to
protein was immunolocalized with fluorescent secondary antibodies in companion cells of leaf
reflect a higher requirement for carbohyminor veins15. Xylem vessels are identified by the yellow autofluorescence of lignin. (c) Expression of the monosaccharide transporter gene, AtSTP4, from Arabidopsis in root tips is shown
drates by these cells; instead it might indiby GUS expression under the control of the AtSTP4 promoter21. The expression of this carrier is
cate that AtSUC1 (DST) modulates the
also induced by wounding and pathogen attack. (d) In situ hybridization of AtSUC1 (DST) mRNA
availability of water in this region, which
on an anther cross-section29. At this stage, the AtSUC1 (DST) protein is detected in the connective
could establish a cue for pollen-tube guidtissue but not in the pollen, suggesting translational regulation. The sucrose carrier AtSUC1 (DST)
ance towards the ovule29.
mRNA from Arabidopis has been identified in the connective tissue of mature anthers and also
In anthers, AtSUC1 (DST) mRNA and
in pollen. In the connective tissue, AtSUC1 (DST) could be involved in the control of anther
protein were detected in parenchymatic
dehiscence. (e) The monosaccharide transporter AtSTP4 (MST) is detected in pollen tubes
cells surrounding the central vascular bungrowing inside the transmitting tissue of the style (longitudinal section through a style). Specific
dle of anther connective tissue just before
antibodies were used and the fluorescence of the secondary antibodies appears in green.
29
anther opening by dehiscence (Fig. 4).
Interestingly, the sucrose transporter AtSUC1 (DST) is also present in germinating pollen29.
Accumulation of sucrose by AtSUC1
(DST) could decrease the water potential
and hence result in water uptake from the adjacent cells of the Sugar transporters in plant–microorganism interactions
anther walls29. This would result in dehydration of the endothecium Some sugar transporters seem to play a role in certain
and an increased tension of its wall thickenings, finally causing plant–microorganism interactions. The sink-specific, woundanther opening29.
induced monosaccharide transporter, AtSTP4 (MST) is induced
July 2000, Vol. 5, No. 7
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(a)
(b)
Lipids
Sucrose
Co
Endosperm
(c) (i)
(ii)
LE
LE
(iii)
t yle
tyl
co
po
y
H
ns
do
Proteins
Amino
acids
cope with the increased demand related to
defence activities, or serve to recover sugars from the apoplast (particularly if hostcell permeability is increased) and thus
reduce the loss of carbohydrate to the
pathogen.
Sugar transporters are also important in
carbon transfer to mycorrhizal fungi22. Colonization of Medicago truncatula roots with
the mycorrhizal fungus Glomus versiforme,
induces expression of the monosaccharide
transporter gene, MtST1 (MST), in cortical
cells of the root that correlates with regions
that are heavily colonized by the fungus22.
The effect is localized to cells within the
immediate vicinity of the fungus, either in
cells containing an arbuscule, or cells that
are frequently in contact with intercellular
hyphae. The nature of the signal for the
induction of plant sugar-carriers during
microorganism interactions is not yet clear.
LE
Role in sugar sensing
Sugars can act as regulatory signals that
affect gene expression and hence plant
development. In relation to resource allocation, the ability to sense altered sugar
concentrations could have important
advantages by allowing the plant to tailor
its metabolism in source tissues to meet the
demands in sinks. There is great interest in
Fig. 5. Localization of the sucrose carrier in a germinating Ricinus seedling. Seeds accudissecting the signalling processes that are
mulate storage reserves in the endosperm during development. Upon germination, these are
involved in sugar sensing and response
hydrolysed and the products, including sugars, are released into the apoplastic space. Sevenpathways. There are three possible sugarday-old dark-grown germinating Ricinus seedlings are shown in (a) with (left) and without
sensing systems in plants32:
(right) an endosperm. (b) Breakdown of lipids and protein in the endosperm and the release of
• A hexokinase-sensing system.
sucrose and amino acids into the apoplast for uptake by the cotyledon. (c) Expression pattern
• A sucrose-transport-associated sensor.
of the sucrose transporter, RcSUT1 (DST)13,46, in the germinating Ricinus seedling (three-day• A glucose-transport-associated sensor.
old). RcSUT1 transcripts were localized by in situ hybridization using an antisense RcSUT1
cRNA probe. Dark staining, indicating RcSUT1 expression, is seen in both the cotyledon
Based on sugar signal transduction processes
lower epidermal cells (LE) that are situated adjacent to the endosperm (parts i–iii) and also in
in Saccharomyces, it has been proposed that
the phloem (red arrows in iii). No equivalent staining was observed in sections probed with
members of the sugar transporter family in
the sense probe (results not shown). The expression pattern indicates that the epidermal cells
plants might play a role in sugar sensing33. In
initially accumulate sucrose from the apoplast and from here sucrose is transferred symplastiyeast, it has been shown that membranecally to the phloem region. The high level of expression of RcSUT1 in the phloem indicates
bound receptors closely related to sugar
that sugars are released into the apoplast before active loading by this transporter. Scale bars
transporters are used to sense external sugar
5 100 mm in (i) and (ii); 50 mm in (iii). (c) reproduced, with permission, from Ref. 13.
concentrations and activate a signal transduction pathway leading to the regulation of
approximately fourfold in Arabidopsis seedlings infected with transporter gene expression and insertion or degradation of proteins
Alternaria brassicicola or Fusarium oxysporum, and also in sus- at the plasma membrane. This allows yeast to respond to a rapidly
pension-cultured cells of Arabidopsis treated with bacterial or changing external environment. The yeast glucose sensors, ScSNF3
fungal elicitors21. It has been concluded that AtSTP4 (MST) plays (senses low glucose levels) and ScRGT2 (senses high glucose leva role in the transportation of monosaccharides into the sink els) are homologous to yeast and plant glucose transporters (Fig. 3)
tissues and that it responds to an increased demand for carbohy- but do not mediate significant glucose transport34. The large Cdrate by cells under stress conditions21. Induction of AtSTP4 terminal extensions of these proteins are required for the trans(MST) expression is also observed during plant and fungal mission of the glucose signal. To date, there is no direct evidence for
biotrophic interaction, for example, Arabidopsis infected with a role of plant monosaccharide and disaccharide transporters as
the powdery mildew Erysiphe cichoracearum31. Expression of sensors. Nevertheless, the finding that several members of the plant
AtSTP4 (MST) is induced dramatically in source leaves infected MST and DST families have unusual cytoplasmic extensions, which
with mildew and, although the fungus is confined to epidermal are predicted to be cytosolic, has initiated studies in relation to the
cells, AtSTP4 (MST) expression is induced in many cell types possible role of these proteins in sugar sensing33.
within the leaf following infection (M. Gilbert et al., unpublished).
The signalling pathway by which this occurs is unknown, and the Regulation of sugar transporters
role of this transporter in this interaction is unclear. It might help As sugar transporters play such a key role in source–sink interacto increase carbohydrate import into infected tissues, in order to tions, it is likely that they are tightly controlled. There are several
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levels at which regulation might occur35,36. As for all H1-symporters, regulation of activity by the proton-motive force is clearly
important. Thus, modulations in the activity of the H1-ATPase
would immediately affect their sugar transport kinetics.
There are numerous examples for transcriptional regulation of
DST or MST gene expression, such as changes in DST expression
pattern in leaves undergoing sink-to-source transition19,37 during seed
development (MST and DST)24, or during pollen maturation and germination (MST and DST)27,28. There is also evidence that biotic and
abiotic factors (e.g. mechanical treatments, light, water and salt
stress, phytohormones, and pathogen attack) have effects on the
expression of certain sugar transporters21,36,38. Post-transcriptional
control mechanisms such as mRNA stability (turnover), mRNA
translation and post-translational control have also been described
for sugar transporters. Examples include the diurnal regulation of
DSTs (Refs 12,39), phosphorylation–dephosphorylation40, and possible modification of activity by the lipid environment36.
There is evidence that changing sugar levels might have an effect
on sugar transporter expression and activity. Evidence has been
provided that a putative sucrose-sensing pathway could modulate
the expression levels and activity of a proton–sucrose transporter
as a function of changing sucrose concentrations in the leaf
(hexoses do not elicit the response)41. This would have a direct
impact on assimilate partitioning at the level of phloem translocation. Changes in transcriptional activity or mRNA turnover
mediate this repression by sucrose but additional regulation by
alterations in protein turnover or direct modification cannot be
ruled out. The response is reversible, highlighting the dynamic
nature of this signalling pathway.
Evidence for sugar regulation of transporters is variable.
AtSUC2 (DST) expression (analysed using a SUC2 promoter–
GUS construct) appears unaffected by sugars19. However, downregulation might not be seen in these experiments because of the
stability of the GUS protein. In addition, it is still possible that
activity might be affected by other mechanisms, even if the promoter is insensitive to sugars. The expression of the Vicia faba
sucrose carrier gene, VfSUT1 (DST), but not the glucose transporter, VfSTP1 (MST), decreased in cotyledons following exposure to high concentrations of sucrose or glucose (150 mM),
whereas lower levels (10 mM) had no effect on transcript levels24.
Sucrose-feeding experiments with detached maize leaves led to an
increase in transcript leaves of ZmSUT1 (Ref. 42) (DST). By contrast, no evidence was found for sugar regulation of three monosaccharide-transporter genes (CST1–3) (MSTs) in suspensioncultured cells of Chenopodium rubrum43.
Thus, for sugar transporters, it is now emerging that various
levels of control are implemented that allow plant cells to regulate
the fluxes of sugars across the plasma membrane during normal
growth and development, and also when their natural environment
is perturbed.
The future
To comprehend source–sink regulation fully and to be in a position to manipulate the complex interactions for agricultural benefit, it is vital that the underlying membrane transport processes
are thoroughly characterized. This includes determining precisely
the range of sugar transporters that are involved, their
structure–function relationships, and defining their cellular and
temporal expression pattern. A particular goal would be the ability to manipulate competition between sinks. For this we need to
find out how sugar carriers are regulated in metabolic and storage
sinks and to relate this to the information available on the activity
of the sucrose metabolizing enzymes, invertase and sucrose synthase. Extracellular invertase is up-regulated in several situations
affecting source–sink relations (e.g. following application of phytohormones and elicitors, pathogen attack and wounding)44 but further work is required to investigate the coordination of events. In
sink cells, it is important to understand why, in some cases, sucrose
is cleaved by a cell-wall invertase and therefore hexose carriers are
involved, whereas in other cases sucrose is taken up and cleaved
inside the cells. In germinating pollen, both monosaccharide and
disaccharide transporters are present28–30, although sucrose is the
preferred carbon source for in vitro germination and hexoses are
inhibiting. Clearly, work is needed for a full comprehension of the
respective role of each carrier type in such cells.
We need to clarify which mechanisms exist for the efflux of
sugars from cells, for example, for efflux from the mesophyll or
from apoplastically unloading phloem cells. Under nonenergized
conditions, influx carriers might be operating in efflux, allowing
sugars to be transported down their concentration gradient; alternatively, different transporters might be involved. In addition, the
identification of tonoplast sugar transporters is important for
understanding storage and remobilization from the vacuole. We
must also consider that entirely different mechanisms might exist
for sugar transport, such as those involving ABC transporters.
More evidence is required on the physiological function of
sugar transporters to support the information from expression
studies. In particular, no antisense studies have been reported for
any of the monosaccharide transporters. We eagerly await studies
on knockout mutants to dissect the transport processes in greater
detail. The phenotype of such plants will provide clues concerning
the physiological role and importance of particular transporters. In
addition, plants with transporter genes under the control of cellspecific promoters will enable us to learn more about source–sink
interactions and pathways of sugar movement.
Sensing functions are essential in allowing plants to adapt to
changing environments. One of the major challenges will be to
identify sugar-sensing mechanisms and the signal transduction
pathways. It will be important to ascertain whether members of
the sugar-transporter families are involved in this function.
Acknowlegements
Our work has been supported by a grant from the European Commission DG XII Biotechnology programme (ContractBIO4-CT960583). L.E.W. is grateful to the Royal Society for support. R.L.’s
work is supported by the CNRS, the French Ministry for Education
and Research and by the Région Poitou Charentes. N.S’s work was
supported by the Deutsche Forschungsgemeinschaft. The help of
Volker Huss with Figure 3 and the help of Cyril Maingourd with
Figure 4 is gratefully acknowledged.
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Lorraine Williams* is at the School of Biological Sciences,
University of Southampton, Bassett Crescent East, Southampton,
UK SO16 7PX; Remi Lemoine is at the Laboratoire de Biochimie
et Physiologie Végétales, ESA CNRS 6161, Bâtiment Botanique,
40 Avenue du Recteur Pineau, F-86022 Poitiers Cedex, France
(tel 133 5 49454183; fax 133 5 49454186; e-mail
[email protected]); Norbert Sauer is at the
Dept of Botany II, Molecular Plant Physiology, University of
Erlangen, Staudtstrasse, D-91058 Erlangen, Germany
(tel 149 9131 85 28212; fax 149 9131 85 28751;
e-mail [email protected]).
*Author for correspondence (tel 144 2380 594278;
fax 144 2380 594319; e-mail [email protected])
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