Available online at www.sciencedirect.
com
Sucrose transporters of higher plants
Christina Kühn1 and Christopher PL Grof2
Recent advances have provided new insights into how sucrose is
moved from sites of synthesis to sites of utilisation or storage in
sink organs. Sucrose transporters play a central role, as they
orchestrate sucrose allocation both intracellularly and at the
whole plant level. Sucrose produced in mesophyll cells of leaves
may be effluxed into the apoplasm of mesophyll or phloem
parenchyma cells by a mechanism that remains elusive, but
experimentally consistent with facilitated transport or energy-
dependent sucrose/H+ antiport. From the apoplasm, sucrose/H+
symporters transport sucrose across the plasma membrane of
cells making up the sieve element/companion cell (SE/CC)
complex, the long distance conduits of the phloem. Phloem
unloading of sucrose in key sinks such as developing seeds
involves two sequential transport steps, sucrose efflux followed
by sucrose influx. Besides plasma membrane specific sucrose
transporters, sucrose transporters on the tonoplast contribute to
the capacity for elevated sucrose accumulation in storage
organs such as sugar beet roots or sugarcane culms. Except for
several sucrose facilitators from seed coats of some leguminous
plants all sucrose transporters cloned to date, including recently
identified vacuolar sucrose transporters, have been
characterised as sucrose/H+ symporters. Transporters
functioning to efflux sucrose into source or sink apoplasms as
well as those supporting sucrose/H+ antiport on tonoplasts,
remain to be identified. Sucrose transporter expression and
activity is tightly regulated at the transcriptional, post-
transcriptional as well as post-translational levels. Light quality
and phytohormones play essential regulatory roles and the
sucrose molecule itself functions as a signal.
Addresses
1
Humboldt University of Berlin, Institute of Biology, Department of Plant
Physiology, Philippstraße 13, Building 12, 10115 Berlin, Germany
2
School of Environmental and Life Sciences, University of Newcastle,
University Drive, Callaghan, NSW 2308, Australia
Corresponding author: Kühn, Christina (christina.kuehn@biologie.hu-
berlin.de) and Grof, Christopher PL (Chris.Grof@newcastle.edu.au)
Current Opinion in Plant Biology 2010, 13:288–298
This review comes from a themed issue on
Physiology and metabolism
Edited by Uwe Sonnewald and Wolf B. Frommer
Available online 18th March 2010
1369-5266/$ – see front matter
# 2010 Elsevier Ltd. All rights reserved.
DOI 10.1016/j.pbi.2010.02.001
Introduction
Photosynthetically produced sugar, principally sucrose, is
moved from source leaves to support growth of, and
Current Opinion in Plant Biology 2010, 13:288–298
carbon storage by, heterotrophic sink organs. Membrane
proteins play pivotal roles in mediating sucrose transport
within plants and their activities have a major impact
upon plant growth rates and crop yields. In the face of a
burgeoning global population, ongoing reduction in ara-
ble land and increased diversion of crops into biofuel
production, it is imperative to secure fundamental un-
derstanding of these key membrane transport processes
to improve crop yield.
Sucrose transporters play a key role not only in phloem
loading and unloading processes but also in the exchange
of sucrose between beneficial symbionts (mycorrhiza and
Rhizobium) as well as pathogens such as nematodes and
parasitic fungi. They are not only key regulators of
transport processes but also integral components of signal
transduction between sink and source metabolism.
Plant sucrose transporters belong to the major facilitator
superfamily (MFS) and are distantly related to hexose
transporters in bacteria, fungi, plants and animals [1–3].
Whereas the sucrose transporter from Schizosaccharomyces
pombe was demonstrated to transport sucrose [1], the
function of the animal sucrose transporter-like protein
AIM1 is still unknown at the molecular level [2]. The
evolutionary origin of sucrose transporters seems to be
very distant and sucrose transporters have been found
in multicellular primitive plants such as lycophytes
(Selaginella lepidophylla) and mosses (Physcomitrella patens).
However, the unicellular green alga Chlamydomonas
rheinhardtii, does not possess sucrose transporters.
The increasing complexity of plant structure and archi-
tecture and the accompanying shift from autotrophy
to heterotrophy highlights the importance of sucrose
transporters as sucrose generated in source leaves crosses
a number of membranes before arrival in sink organs such
as tubers, flowers and seeds where it is either utilised or
stored.
A growing sucrose transporter family
Increasing availability of molecular information provides
new opportunities to detect physiological roles for, and
regulation of, sucrose transporters. The first plant sucrose
transporter SoSUT1, from spinach (Spinacea oleracea), was
functionally identified using an elegant yeast comple-
mentation strategy [4] and has been instrumental for
the development of current understanding of fundamen-
tal transport processes. There are nine sucrose transporter
genes (SUTs or SUCs) described in Arabidopsis [5],
whereas the rice genome contains five SUT genes [6].
An analysis of the draft genomes of the monocots sor-
ghum, maize and Brachypodium [7], has led to a proposed
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 Sucrose transporters Kühn and Grof 289

Figure 1

Rooted phylogenetic dendrogram of representative sucrose transporters from monocotyledonous and dicotyledonous species, mosses and fungi.
Sequence from Aspergillus clavatus (ACLA009530), has been used as the outgroup. Arabidopsis thaliana: AtSUC1, At1g71880; AtSUC2, At1g22710;
AtSUT2, At2g02860; AtSUT4, At1g09960; AtSUC9, At5g06170. Daucus carota: DcSUT1A, CAA76367; Hevea brasiliensis: HbSUT2a, ABJ51934;
HbSUT5, ABK60189. Hordeum vulgare: HvSUT1, CAB75882. Lycopersicum esculentum renamed Solanum lycopersicum: LeSUT1, CAA57726;
LeSUT2, AAG12987; LeSUT4, AAG09270. Lotus japonicus: LjSUT4, CAD61275. Lolium perenne: LpSUT1, EU255258; LpSUT2, ACU87542. Nicotiana
tabacum: NtSUT1A, CAA57727. Oryza sativa: OsSUT1, AAF90181; OsSUT3, BAB68368; OsSUT5, BAC67165. Pisum sativum: PsSUT1, AAD41024;
PsSUF1, ABB30163; PsSUF4, A3DSX1. Saccharum hybrid: ShSUT1, AAV41028. Solanum tuberosum: StSUT1, CAA48915; StSUT4, AAG25923.
Sorghum bicolor (Sorghum Genome Project: www.phytozome.net): SbSUT1, Sb01g045720; SbSUT2, Sb04g038030; SbSUT3, Sb01g022430;
SbSUT4, Sb08g023310; SbSUT5, Sb04g023860; SbSUT6, Sb07g028120. Triticum aestivum: TaSUT1A, AAM13408; TaSUT1B, AAM13409; TaSUT1D,
AAM13410. Zea mays (Maize Genome Project: http://www.maizesequence.org/index.html. ClustalW was used for sequence alignment and
analysis. PhylML v3.0 was used to derive the phylogeny and the data were converted into Newick format before transfer to Dendroscope
(http://www-ab.informatik.uni-tuebingen.de/software/dendroscope) [88]): ZmSUT1, BAA83501; ZmSUT2, AAS91375; ZmSUT3, ACF86653;
ZmSUT4, AAT51689; ZmSUT5, ACF85284; ZmSUT6, ACF85673. Accession numbers are also used as additional descriptors in the tree in those
instances where confusion may arise because of variations in nomenclature.

separation into five groups where the fifth group is made
up exclusively of functionally uncharacterised monocot
transporters (Figure 1).
All sucrose transporters to date have been characterised as
sucrose/H+ symporters with the exception of sucrose
facilitators (SUFs) from Pisum sativum and Phaseolus vul-
garis, reported to catalyse bi-directional sucrose transport
in a pH-independent and energy-independent manner
[8].
Intracellular localisation of sucrose
transporters
Members of the high affinity dicot SUT1 Clade, which
exhibit apparent Km values between 0.07 and 2.0 mM
sucrose, are expressed in the plasma membranes of

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290 Physiology and metabolism
SEs [9–11] or CCs [12,13] or in some instances both cell
types [14].
Although phylogenetically separated from the dicot
SUT1s, the SUTs belonging to the monocot specific
Clade 3 (rice, maize, sugarcane, barley, Lolium and
wheat), have been immunolocalised to the plasma mem-
brane of SEs in wheat [15] and both SEs and companions
cells of rice [16]. Those few that have been functionally
characterised in heterologous systems exhibit apparent
Km values of 2–8 mM sucrose [17,18].
The SUT2 and SUT4 transporters which encompass both
monocot and dicot members demonstrate a lower affinity
for sucrose with reported Km values of 4–20 mM. Structu-
rally, the dicot members of the SUT2 Clade possess an
elongated central loop, approximately 60 amino acids in
length, not present in the monocot members and found to
have no influence upon transport kinetics [19]. The
SUT2 transporters have been localised to SE plasma
membranes in tomato [10], plantain (PmSUC3 [20])
and Arabidopsis (AtSUC3 [21]). They have been reported
in a number of vegetative sinks [20,21] as well as devel-
oping seeds [22].
Members of the SUT4 subfamily of sucrose transporters
have been identified in the chloroplast fraction (AtSUT4
[23], the vacuole (AtSUT4, HvSUT2 [24]) and at the
plasma membrane (StSUT4 [25]). With the exception of
DcSUT1, the members of the SUT4 subfamily catalyse
sucrose uptake with low affinity.
Sucrose transporters such as AtSUC2 [26], do not trans-
port sucrose exclusively, but transport maltose and other
glucosides such as arbutin, salicin, a-phenylglucoside,
b-phenylglucoside, a-paranitrophenylglucoside, b-para-
nitrophenylglucoside, paranitrophenyl-b-thioglucoside,
turanose and a-methylglucoside with lower affinity.
Another member of the SUT1 subfamily of sucrose
transporters AtSUC9, transports glucosides such as heli-
cin, salicin, arbutin, maltose, fraxin, esculin, turanose and
a-methyl-D-glucose. Monocotyledonous SUT1 members
grouped into Clade 3, HvSUT1 and ShSUT1 demon-
strated much higher specificity for sucrose as a substrate
[27].
What is the physiological role of vacuolar
sucrose transporters?
Sucrose accumulating species like Beta vulgaris and Sac-
charum officinarum use the vacuole of storage cells as a
sucrose depot. It has been shown that vacuolar sucrose
transporters, acting as sucrose/H+ antiporters, play a key
role in sucrose import into vacuoles [28,29].
Members of the SUT4 subfamily of sucrose transporters
are functional in sucrose uptake at the plasma membrane
of yeast cells (StSUT4 [11], HvSUT2 [30], AtSUT4 [11],
Current Opinion in Plant Biology 2010, 13:288–298
DcSUT1 [31]) or at the plasma membrane of Xenopus
oocytes (LjSUT4 [32]). Nevertheless, three of the SUT4
members were recently assigned to the vacuole tonoplast
according to the localisation of GFP fusions (AtSUT4
[24], HvSUT2 [24], and LjSUT4 [32]). Targeting to the
plasma membrane was suggested to be a consequence of
mis-targeting because of heterologous over-expression.
Not all the members of the SUT4 subfamily of sucrose
transporters have been localised to the vacuole as shown
by GFP fusion and western blot analysis in the case of
StSUT4 [25], which is in agreement with its capacity to
catalyse sucrose uptake at the yeast plasma membrane
[11]. As all three vacuolar sucrose transporters function as
sucrose proton symporters rather than antiporters, it was
postulated that they are most likely involved in sucrose
efflux from the vacuole [33]. Despite strong evidence for
transporters functioning on the tonoplast as sucrose/H+
antiporters to load sucrose into the vacuole, genes encod-
ing these proteins remain to be identified (see summary in
Figure 2).
Regulation of sucrose transport at a cellular
level
Sucrose supply to terminal sink organs and apical mer-
istems is crucial for the energy status and the control of
flowering or tuber onset [25,34], thereby affecting crop
yield. Tight regulation of sucrose allocation is required to
modulate carbon allocation in response to changing
environmental conditions. Sucrose transporters are tightly
regulated at various levels, allowing adaptation to external
stimuli such as temperature, light regime, photoperiod,
pathogen attack or other stresses. Plasticity of the potato
SUT1 activity over one order of magnitude was recently
demonstrated by measurements in yeast [35] and sup-
ports the observed 10-fold increase in sucrose export from
leaves of potato plants over-expressing a bacterial pyr-
uvate decarboxylase (PDC) [36]. The plasticity of phloem
loading activity was demonstrated in response to defolia-
tion in Lolium perenne [37]. Defoliation induced changes
in the kinetic parameters of sucrose transport. A decrease
in Km followed by an increase of Vmax was observed, which
cannot be explained simply by de novo synthesis of
LpSUT1 transporters.
A novel phloem-specific transmembrane protein, Tie-
dyed 1 (Tdy1), found exclusively in grasses promotes
phloem loading without affecting the phloem unloading
capacity [38]. Further analysis of this fascinating maize
protein may help to dissect the differences between
loading and unloading activities of sucrose transporters.
Regulation of transport activity by
Phosphorylation?
Phosphorylation is likely to be a crucial tool for the
regulation of sucrose transport. Use of the protein phos-
phatase inhibitor ocadaic acid, affected mRNA abun-
dance, transcription rate and activity of BvSUT1 [39],
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 Sucrose transporters Kühn and Grof 291

Figure 2

Intracellular localisation of sucrose transporters supported by biochemical analysis, immunolocalisation or marker gene evidence. Within the cell,
sucrose/H+ symporters have been localised to the plastid (AtSUT4 [16]), the tonoplast membrane (AtSUT4, HvSUT2 [17]) and the plasma membrane
(SUT1 Clade members including AtSUC1, AtSUC2 and StSUT1 [6–11], SUT2 Clade members including LeSUT2 [7], PmSUC3 [13], AtSUC3 [14] and
SUT3 Clade members, OsSUT1 [16], TaSUT1 [15]). Energy-independent sucrose transport mediated by facilitators has been reported on the tonoplast
membrane in sink storage cells [89] and function as effluxers on the plasma membrane of legume seed coats ([5,69]) and root tips [90]. There is also
strong biochemical evidence of a proton coupled antiport mechanism operating on the plasma membrane of bean seed coats [91,92] as well as on
tonoplast membranes [89]. Currently, functional characterisation of cloned higher plant sucrose transporters has failed to identify sucrose/H+
antiporters.

whereas protein kinase inhibitors had no effect on tran-
scription or activity [40]. Direct evidence for the phos-
phorylation of the N-terminus of a sucrose transporter was
first shown for AtSUC5 [41]. Mass spectrometric analysis
of the AtSUC1 protein revealed phosphorylation of the
serine residue at position 20 as well as threonine at
position 393 [42,43].
Redox-dependent targeting and dimerisation
For many members of the MFS it has been shown that
their function is coupled to their oligomeric state.
Whereas the structure of the lactose permease LacS from
Escherichia coli was resolved at 3.5 Å to be monomeric [3],
the lactose permease LacY from Streptococcus thermophilus
was shown to be active in its dimeric form as revealed by
biochemical methods [44]. Both LacY subunits function-
ally interact in vivo as well [45].
Sucrose transporters might also be functionally depend-
ent on their quarternary structure, since StSUT1 from
potato as well as LeSUT1 from tomato were shown to
dimerise in a redox-dependent manner and GFP fusion
constructs show increased plasma membrane targeting in
an oxidative environment [35]. Blue native PAGE, as well
as SDS-PAGE under non-reducing conditions and immu-
noprecipitation revealed the ability of the SUT1 proteins
from potato and tomato to form dimers in yeast and in
plants [35]. Biochemical studies confirmed the capacity of
SUT1 to form a dimer in plants, yeast cells and in Xenopus
oocytes in a redox-dependent manner. The spinach
sucrose transporter SoSUT1 also migrates in a homo-
dimeric complex under native-like conditions if over-
expressed in transgenic potato plants [46] leading to
increased sucrose uptake capacity [47]. Further investi-
gation will be required to determine if redox-dependent
targeting and dimerisation of SUT1 has physiological
consequences on carbohydrate partitioning in planta.
Regulation via protein–protein interactions
The ability of SUT1 to form homodimers was shown by a
split-ubiquitin system in yeast [48], as well as by split YFP
in plants [35]. The sucrose transporter SUT1 has been

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292 Physiology and metabolism
demonstrated to form functional dimers [46] and was also
detected in the detergent-resistant membrane (DRM)
fraction from potato [35]. Concentration of plasma mem-
brane proteins in raft-like microdomains is suspected to
be important for oligomerisation, function, signalling,
endocytosis and/or degradation of membrane proteins
[49,50]. The question of whether DRM-association is
involved in dimerisation, internalisation or degradation
of sucrose transporters remains to be answered.
In a recent approach using a combination of the split-
ubiquitin yeast two hybrid, immuno-coprecipitation and
bimolecular fluorescence complementation assays,
specific interaction between a sucrose transporter
MdSUT1 and a sorbitol transporter MdSOT6 from apple
(Malus domestica) was demonstrated. Interaction with the
ER-anchored plant cytochrome b5 MdCYB5 was shown
to increase the affinity of the sugar transporters in yeast.
Whereas the yeast cytochrome b5 ScCYB5, which also
interacts with the sugar transporters, had no effect on the
affinity [51]. Here again, plasticity of sugar transporter
activity is demonstrated and interaction with an ER-
anchored protein indicates that protein–protein inter-
actions of sucrose transporters are not restricted to the
plasma membrane.
Regulation at the post-transcriptional level
Interestingly, the members of the SUT2 and SUT4
family are expressed at a very low level in Solanaceous
species and were shown to be regulated at the post-
transcriptional level [52]. In Arabidopsis microRNAs tar-
geted against seven out of nine different sucrose trans-
porter genes have been identified, with the exception of
AtSUT2 and AtSUT4 [53]. A regulatory function is
proposed for SUT2 and SUT4 proteins, a very different
role to that of SUT1 proteins. StSUT4 may act as an
inhibitor of SUT1, since StSUT4-RNAi plants display a
similar phenotype to SUT1 over-expressing plants in-
cluding early flowering [25].
The role of sucrose transporters in
autotrophic tissues (leaves)
Sucrose biosynthesis occurs in the leaf mesophyll cyto-
plasm, but considerable amounts of sucrose have also
been measured in organelles such as vacuoles or plastids
[54]. Sucrose may have several possible fates once
released into the leaf apoplasm from the mesophyll cell.
Sucrose may be accumulated in the guard-cell apoplast in
a light-dependent manner and influence stomatal aper-
ture [55,56]. Alternatively, the observed accumulation of
starch in epidermal cells in response to sucrose transporter
inhibition indicates that sucrose may also be sequestered
by these cells under particular conditions [57]. The bulk
of the sucrose released into the leaf apoplasm, however, is
actively loaded into SE–CC complexes by a proton sym-
port mechanism in apoplasmic loading species (reviewed
in [58]). The transport mechanism(s) responsible for this
Current Opinion in Plant Biology 2010, 13:288–298
key step of sucrose efflux from the mesophyll or phloem
parenchyma cells remain unknown.
During the night, starch breakdown in chloroplasts is the
major source of carbon for sucrose biosynthesis in the
cytosol and maltose is considered the principal carbon
form exported from the chloroplast [59]. A plastidic mal-
tose transporter, Mex1, was found to be essential for the
conversion of starch to sucrose and supports this predo-
minant route of carbohydrate export during the night [60].
Once loaded into the SE–CC complex, the long distance
transport of concentrated sucrose is likely to require
energised reloading along the entire length of the axial
pathway from source to sink. Although an AtSUC2 null
allele mutant was reported to produce fertile seed despite
the absence of the sucrose transporter SUC2 considered
crucial for sucrose allocation, the overall health of the
plant was severely compromised [61]. Phloem unloading,
the processes involved in transport of sucrose from the
SE–CC complex to sites of utilisation or storage, may be
via one of three pathways, namely symplasmic, apoplas-
mic or a combination of the two. The delivery of sucrose
to growth sinks is via the symplasm, whereas apoplasmic
unloading is typically from the SE–CC complex to the
surrounding vascular parenchyma or ground tissues of
stems and roots, which may function as temporary storage
sinks. Apoplasmic unloading may be followed by sucrose
cleavage catalysed by apoplasmic invertases, resulting in
an increased sucrose concentration gradient between
source and sink [62]. As in the case of potato plants,
hexose transporters became highly relevant for the effi-
cient carbohydrate uptake by the corresponding sink
parenchyma cells and thereby influence sink strength
[63].
A mandatory apoplasmic step is evident within seeds at
the maternal/filial interface [22] and interfaces between
tissues of different genomes such as mycorrhiza. In crops
which are harvested for high sugar concentrations in their
storage organs such as fleshy fruits, apoplasmic unloading
is followed by a loading step into the sink cells [64]. In
some sinks which accumulate high concentrations of
sugars such as the culm of sugarcane, a symplasmic
transport pathway may be followed with the concentrat-
ing step taking place on the tonoplast membrane [18].
Sucrose transporters are essential for phloem
loading from the apoplasm
Dicotyledonous members of the phylogenetic SUT1
Clade and monocotyledonous members of the SUT3
Clade play essential roles in apoplasmic loading of SE–
CC complex as indicated by the analysis of transgenic and
mutant plants [65–68].
The key and contrasting physiological roles they perform
are highlighted by the result of reverse genetic
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approaches in maize and rice. In maize, leaves of sut1
mutant plants demonstrated reduced sucrose export,
accumulated high levels of carbohydrate and exhibited
chlorosis and early senescence. The plants also exhibited
reduced stature and altered biomass partitioning,
delayed flowering as well as stunted tassel development
[68].
Antisense suppression of OsSUT1 led to reduced grain
filling and final grain weight as well as impaired germina-
tion and growth of seed arising from transformed plants
attributed to the reduced remobilisation of sucrose from
starch endosperm in the developing seedlings of trans-
formed plants [65,69].
The marked impact on both vegetative and reproductive
organs in maize as compared with the restricted impact
upon the grain alone in rice may reflect the exertion of
primary control over photoassimilate distribution by the
sink. As no photosynthesis measurements were reported
for the sut1 maize mutant the phenotypic changes could
be affected by signals originating in the sink and impact-
ing upon carbon reduction in the leaves. If sucrose were
loaded from the apoplasm in maize leaves rather than
symplasmically as suggested for rice, the signal conduit/
transducer may be the sucrose transporter on the SE and/
or CC plasma membrane.
The sucrose transporter from maize, ZmSUT1, has been
reported to be capable of reversed transport under con-
ditions where the free energy of the transmembrane
sucrose gradient exceeds that of the opposing pmf
[70]. Sucrose transporters may experience such con-
ditions in planta during apoplasmic loading and phloem
unloading in vegetative sinks possessing high levels of
invertase in the extracellular space [71]. In contrast to
what was observed in rice as well as in sugarcane, the
analysis of the sut1 mutant plants from maize strongly
suggest a crucial role for ZmSUT1 in efficient phloem
loading [68].
Cellular location of sucrose transporters in
the SE/CC complexes
Since SUT1 mRNA was found in SEs and CCs of potato
and the use of a CC-specific rolC promoter successfully
inhibited its expression [72] it can be concluded that the
transcription of the SUT1 gene occurs in CCs.
The SUT1 protein however was localised only in the SEs
of the phloem and in guard cells. Immunolocalisation of
SUT1 in guard cells corroborates SUT1 promoter reporter
gene fusions showing promoter activity not only in the
phloem, but also in guard cells and trichomes [73]. A
SUT1–GFP fusion protein localised the SUT1 protein
not only at the plasma membrane of infiltrated tobacco
leaf epidermal cells, but co-localises strikingly with a
fluorescently labelled ER-tracker [35].
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Sucrose transporters Kühn and Grof 293
Fusion of SUT1 to GFP or GUS in stably transformed
plants prevented SUT1 localisation in SEs and the repor-
ter genes were detected only in CCs [64,73]. In a more
recent report, the use of the CC-specific AtSUC2 pro-
moter for the expression of proteins of different sizes (up
to 67 kDa) led to non-specific trafficking of proteins into
the SEs [74]. Even the expression of a membrane-
anchored fluorescent protein of 6 kDa containing two
transmembrane domains was detected in the plasma
membrane of SEs in Arabidopsis and tobacco if expressed
under the control of the CC-specific AtSUC2 promoter
[75]. Fluorescence was also detected in vesicle-like
structures in the lumen of SEs suggesting the existence
of vesicle trafficking machinery in mature SEs. Coupling
of SEs and CCs via the desmotubule built by the con-
nected ER cisternae of both cell types has been shown
using ER-specific fluorochromes and the fluorescence
redistribution after photobleaching (FRAP) [76]. ER-
coupling of these two cell types opens up the possibility
of membrane protein exchange between these cells and
based on this knowledge, a model for SUT1 protein
trafficking from CC into the SE has been proposed
(Figure 3).
However, the presence of sucrose transporter transcripts
in the phloem sap, together with the fact that almost the
complete translational machinery including most of the
tRNAs, was detected in mature phloem SEs [77] opens
up the possibility for an alternative pathway of SUT
targeting to the SE plasma membrane assuming that
translation of the SUT transcripts occurs directly in the
SEs. Clearly the dogma that enucleate mature SEs are
devoid of ribosomes and unable to translate proteins must
be reconsidered.
Although there is evidence in Solanaceous species at least,
that phloem loading occurs directly at the plasma mem-
brane of SEs, a recent report using antiserum raised
against a NtSUT1–MPB-fusion protein revealed localis-
ation of SUT1 to CCs and not SEs of Solanaceae [78]. The
conclusions drawn from immunolocalisation experiments
are somewhat conflicting and the definitive resolution of
the question of whether sucrose transport takes place
across the CC or SE plasma membrane must await the
application of novel strategies and technologies.
Roles of sucrose transporters in heterotrophic
tissues
In sinks where sucrose unloading includes an apoplasmic
step, such as developing seeds of leguminous plants [22],
SUT1 has been localised to the phloem. Similarly, in the
grains of barley, rice and wheat, SUT1 is reported to play a
major role at the maternal/filial interface where two essen-
tial transport steps, sucrose efflux and subsequently
sucrose influx, take place. Although energy-independent
effluxers have been identified in developing legume seeds
[17], physiological evidence indicates that energy coupled
Current Opinion in Plant Biology 2010, 13:288–298
294 Physiology and metabolism

Figure 3

Hypothetical model of SUT1 protein targeting through plasmodesmata via the desmotubule. Co-localisation of a SUT1–GFP fusion with an ER-tracker
[35], together with the quantification of plasmodesmal ER-coupling between sieve elements and companion cells [76] opens the possibility to
exchange membrane proteins between SE and CC via the ER. Picture was drawn and kindly provided by Johannes Liesche. This is one of the several
hypothetical pathways of SUT protein targeting to the SE plasma membrane.

membrane carriers may also be operating to mediate
sucrose unloading in cereals and grain legumes [79].
Transgenic plants provide strong evidence of the import-
ance of sucrose transporters in the axial pathway and
terminal sink organs of heterotrophic tissues. Tuber-
specific repression of the potato StSUT1 expression,
localised in SEs leads to retarded development of tubers
when phloem unloading is thought to occur apoplasmi-
cally [80,81]. Conversely, a significant demonstration of
increased sucrose uptake and growth rate of cotyledons
has been reported in developing pea seeds over-expres-
sing the potato StSUT1 [82].
The role of SUT2 proteins in the development
of pollen and pollen tubes
Sucrose transporters encoded by SUT2 subfamily mem-
bers are not only present in phloem SEs but are also
expressed in sink tissues such as pollen and in growing
pollen tubes [20,83]. Inhibition of LeSUT2 in transgenic
tomato plants led to a reduced pollen viability, pollen
tube growth and a reduced sucrose uptake of pollen tubes
grown in vitro [83], suggesting a key role in pollen de-
velopment and pollen tube loading. In addition to hexose
uptake in growing pollen tubes, sucrose uptake clearly
seems to be of some significance and the sink specific
sucrose transporter NtSUT3, has been identified in
tobacco pollen [84].
SUTs and sucrose play a role in whole plant
developmental phenomena
Flowering and tuberisation represent switches from vege-
tative to reproductive stages of development, both being
controlled by the photoperiodic pathway. Tuberisation in
potato plants is initiated by short days and an analogy
between the floral induction pathway in short day plants

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and the tuberisation pathway in potato plants has been
postulated [85].
Downregulation or over-expression of sucrose transporter
genes affects both flowering [27,86,87] and tuberisation,
as well as the shade avoidance syndrome in potato plants
[25], suggesting that phytochrome-dependent or photo-
period-dependent induction of tuberisation and flowering
share a similar mechanism and that sucrose plays an
essential role in it.
The SUT4 protein is likely to play a key role as, in addition
to early flowering, StSUT4-RNAi plants exhibit higher
tuber production, and reduced sensitivity towards light
enriched in far-red wavelengths (i.e. in canopy shade).
Inhibition of StSUT4 led to tuber production in the strict
photoperiodic potato subsp. andigena even under non-
inductive long-day conditions. Accumulation of soluble
Figure 4
Hypothetical model for StSUT4 connecting phytochrome B-dependent
signalling to phytohormonal responses. The model was adapted
and modified from [85]. Sucrose efflux is increased in SUT4-inhibited
plants and sucrose content in sink organs such as the shoot apical
meristem and in vitro grown microtubers is increased compared to
WT plants. Therefore, and because SUT1 over-expressing plants
display a very similar phenotype to SUT4-inhibited plants, it is
assumed that SUT4 may act as an inhibitor of SUT1. The mechanism
of SUT4-mediated inhibition on SUT1 activity requires further
investigation. Modified sucrose partitioning might represent the long
distance signal connecting light information from leaves (potentially
involving phytochrome B) to phytohormonal responses involving the
ethylene and the GA-dependent pathway. Experimental support came
from [25] and unpublished data.
www.sciencedirect.com
Sucrose transporters Kühn and Grof 295
sugars and sucrose efflux from leaves of transgenic plants
are modified in StSUT4-RNAi plants, leading to modified
sucrose levels in sink organs such as tubers and shoot
apices. In wild-type plants, StSUT4 expression is induced
by gibberellins and ethephon, and external supply of
gibberellic acid leads to even more pronounced differences
between wild-type and StSUT4-RNAi plants with regard
to tuber yield and internode elongation, indicating a reci-
procal regulation of StSUT4 and gibberellins [25].
It is proposed that StSUT4 is controlled by phytochrome
B and that sucrose potentially links light quality percep-
tion via phytochromes, to GA signals regulating tuberisa-
tion (Figure 4).
Future perspective
Depending on their localisation, sucrose transporter
proteins fulfil different, potentially even antagonistic
functions in sink and source tissues. The fact that sucrose
transporter protein-interacting partners are not exclu-
sively restricted to the plasma membrane compartment,
together with the observation of brefeldin A-induced
internalisation of the sucrose transporter SUT1 argue
for dynamic subcellular localisation of sucrose transpor-
ters. Retrograde as well as anterograde transport of
sucrose transporters within cells might represent an
important feature to trigger the sucrose conductance of
a given membrane by modifying the number of transpor-
ter proteins in the plasma membrane.
Acknowledgements
We would like to thank Johannes Liesche for experimental and art work.
Financial support came from DFG (SFB 429, SPP1108) to CK. We
gratefully acknowledge critical reading of the manuscript by John Patrick
and Thomas Buckhout.
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