Journal of Experimental Botany, Vol. 50, Special Issue, pp. 935–953, June 1999
Update on sucrose transport in higher plants
Christina Ku ¨hn1, Laurence Barker, Lukas Bu ¨rkle and Wolf-Bernd Frommer
Pflanzenphysiologie, ZMBP–Centre of Plant Molecular Biology, Universita ¨t Tu ¨bingen, Auf der Morgenstelle 1,
D-72076 Tu ¨bingen, Germany
Received 10 August 1998; Accepted 30 November 1998
of water and mineral salts taken up by the root system
and transported via the xylem network, while non-green
tissues depend on the carbon supply deriving from meta-
bolic source organs via the phloem. The existence of a
well co-ordinated long-distance transport network was a
prerequisite for the evolutionary development of higher
land plants. To understand carbon allocation throughout
the whole plant, it is necessary to describe the phloem
network in more detail (Behnke, 1989).
Sucrose as the major transported form of fixed carbon,
must be translocated from the sites of synthesis, i.e.
the green tissues, to the sites of consumption and
storage, i.e. the non-green cells and organs. For apo-
plasmic transport, carrier-mediated processes are
required at the plasma membrane. Functional comple-
mentation of modified yeast strains has enabled the
isolation and characterization of a large family of suc-
rose carriers (SUT) from a wide variety of species.
In Xenopus oocytes, electrophysiological methods
demonstrated that the SUTs function as proton
co-transporters. Localization studies show that at
least SUT1 is present at the plasma membrane of
enucleated sieve elements, indicating macromolecular
transport of its mRNA or protein from the companion
cell to the sieve element. Inhibition of the transport
activity in several transgenic plant species proves that
SUT function is essential for long-distance transport.
Further experiments will be required to assign specific
functions to the other members of the SUT family.
The route of photosynthetic carbon through the plant
Fixation of CO2takes place in the chloroplasts of meso-
phyll cells, mainly in the palisade parenchyma of mature
leaves by the Calvin cycle. Net products of this cycle are
triose phosphates which can be fed into several biosyn-
thetic pathways, e.g. starch, lipid or amino acid biosyn-
thesis in chloroplasts or sucrose and amino acid synthesis
in the cytosol. Various biosynthetic pathways in different
compartments of mesophyll cells compete with each other
for triose phosphates (Schulz et al., 1993). According to
the requirements of the whole plant, the direction of
biosynthesis is determined by the exchange rate of triose
phosphates across the inner chloroplastidic membrane
which depends on the transport activity of the Triose-
Phosphate-Translocator (TPT) located in the inner envel-
ope. First identified in spinach leaves as a 29 kDa protein,
the TPT works as an antiporter mediating the export of
3-phosphoglycerate as triose phosphates from the chloro-
plast matrix in exchange for inorganic phosphate from
the cytosol (Flu ¨gge et al., 1989). The availability of
inorganic phosphate depends mainly on cytosolic sucrose
synthesis, which releases inorganic phosphate in several
steps. In simple terms, a decrease in sucrose synthesis
therefore leads to reduced levels of inorganic phosphate,
thus down-regulating triose phosphate export, which leads
to the deposition of transitory starch in the chloroplast.
The TPT appears to be a well-regulated membrane protein
Key words: Sucrose, transport, sucrose carriers, proton
co-transporters, plasma membrane, sieve elements, com-
In contrast to unicellular organisms such as bacteria,
many fungi and unicellular green algae, higher plants are
able to develop highly differentiated tissues that fulfil
specific functions. These specializations accompany a loss
in autonomy making it indispensable for different cell
types to collaborate closely with one another even over
long distances. Phloem and xylem elements form a capil-
lary network connecting metabolic sink and source
organs. Thus green tissues are dependent on the supply
1 To whom correspondence should be addressed. E-mail: firstname.lastname@example.org
© Oxford University Press 1999
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Ku ¨hn et al.
allowing for the adaptation of leaf carbon metabolism to
the momentary requirements for transient storage or
long-distance transport of photosynthates (Flu ¨gge et al.,
In most plants, sucrose is the main transport form of
photoassimilates, in contrast to hexoses that do not
circulate over long distances as in the animal kingdom.
Sucrose moving from source to sink organs has to over-
come several membranes involving specific sucrose car-
riers. This paper focuses on this particular group of
membrane transporters in vascular land plants.
The nucleus disintegrates either by pycnosis or by
chromatolysis (Behnke and Sjo ¨lund, 1990; Eleftheriou,
1990; Evert, 1990) and the tonoplast undergoes selective
autophagy. The fragments of the tonoplast membrane
associate with other remnants of the endomembrane
system and are assumed to reorganize to form the parietal,
agranular SE-specific sER, which is seemingly free of
ribosomes. The hypothesis of reorganization needs further
confirmation by localization of tonoplast-specific proteins
in the sER membrane system in mature SEs.
In SEs, two types of plastids can be observed: the
so-called S-plastids containing large starch granules and
the P-plastids with proteinaceous inclusions which are
present in parietal positions in SEs. The starch granules
present in S-plastids of SEs are spherically shaped and
rich in amylopectin. The content of P-plastids may play
a role in sieve pore plugging (‘two component glue’, see
Knoblauch and van Bel, 1998). Mature SEs are sur-
rounded by a plasma membrane and are considered to
be living cells, still having the capacity to plasmolyse in
hyperosmotic media, although they do not have vacuoles.
Deprived of essential organelles, SEs lose their autonomy
during maturation, suggesting that one important task of
the CCs’ numerous ribosomes and mitochondria is the
supply of compounds to the highly specialized SEs (for a
review see Sjo ¨lund, 1997).
The ultrastructure of phloem cells appears to reflect
the function of these cells. Thus, in the past, several
anatomical features of phloem cells have been correlated
with different phloem functions, such as phloem loading,
unloading, or retrieval of translocated assimilates.
A further ultrastructural hint for the specific task
performed by phloem cells comes from freeze–fracture
analysis of Streptanthus callus SE plasma membranes.
The internal and external face of phloem cell plasma
membranes show differing densities of intramembraneous
particles (IMP). The distribution of IMP within the two
membrane faces differs between SEs and parenchyma
cells. In parenchyma cells, the ratio of IMP at the
cytoplasmic (P-face) to that of the external (E-face) is
approximately 1051 (PF5EF). This relationship is shifted
to about 151 in SEs. The high particle density of the SE
E-face seems to be a morphological manifestation of
intensive active transport across the plasma membrane of
SEs. IMPs are thought to be the sites of proton-pumping
ATPases and specific carriers for sucrose or amino acids
(Sjo ¨lund and Shih, 1983a).
The postulation that, in some species, phloem loading
occurs directly at the plasma membrane is supported by
the anatomy of the modified ER in SEs. A modified
agranular ER resides as a parietal anastomosing system.
The function of the close spatial relationship between
plasma membrane and ER is thought to provide a micro-
cotransport through the plasma membrane, spatially sep-
Phloem and xylem form collateral bundles. The pro-
tophloem elements arise from procambial strands and are
only functional in proximity to meristematic apices.
Functionality is then taken over by the metaphloem
elements within and beyond the extension zone. Meta-
phloem elements arise from procambial tissue, or in the
case of secondary phloem elements, from the cambium
(Esau, 1969; Behnke, 1989).
The phloem of angiosperms comprises several cell types:
the phloem sap conducting sieve elements (SEs), the
companion cells (CCs) and the phloem parenchyma cells.
In their mature form, SEs are interconnected via sieve
pores at their terminal ends. SEs and CCs develop by
asymmetric cell division from a common mother cell. In
contrast to the sieve tube member, the CC retains its
capacity for further divisions or redifferentiation. During
maturation, SEs undergo selective autophagy, and the
plasmodesmata (PD) at the poles widen to form sieve
pores. Sieve pores arise during cytokinesis from primary
PD through cell wall disintegration. The resulting large
pores allow free movement of solutes in the phloem
translocation stream through sieve plates. The ER cis-
ternae play an important role in the formation of sieve
pores in dicotyledons, as does the deposition of callose.
During cell division of their common mother cell, SEs
and CCs remain in close symplasmic contact by numerous
asymmetrically branched PD and behave as a single
functional unit, which has led to the term sieve element–
companion cell complex (SECCC). During SE differenti-
ation the cell wall thickens and autolytic degradation
processes break down a large part of the SE cytoplasmic
content such as nucleus, tonoplast, dictyosomes, and most
of the ribosomes. Cell wall thickening of the SE could be
a prerequisite necessary for the increased turgor pressure
during active translocation in mature SEs. Sieve areas in
lateral and terminal walls (sieve plates) do not undergo
cell wall thickening. In mature SEs, only a few plastids,
mitochondria and a modified ER persist, mostly in pari-
etal positions. There is experimental evidence that mito-
chondria are metabolically active even in mature SEs
(McGivern, 1957; Lee et al., 1971; Moniger et al., 1993).
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Sucrose transport in higher plants
arated from the rapid translocation stream in the SE
lumen (Sjo ¨lund and Shih, 1983b). For a recent review
about the relationship between phloem anatomy and
function, see Schulz (1998).
still unknown how they are synthesized and metabolized.
The structural P-proteins, major components of the
phloem exudate in dicotyledons have been shown to
be stable, at least over a 72 h period in cucurbits
(Dammenhofer et al., 1997). However, as evidenced by
enzyme activities, the protein concentration in exudates
of non-cucurbits remains constant over many hours of
exudation (Becker et al., 1971). The question is, where
the synthesis of SE specific proteins takes place? It is
likely that these proteins are synthesized in CCs and
subsequently translocated via PD into the SE. This hypo-
thesis is supported by the finding that P-protein PP2
mRNA is found in CCs, whereas PP2 protein is present
in SEs and CCs (Bostwick et al., 1992; Dannenhofer et
al., 1997). Synthesis of P-proteins from Cucurbita maxima
occurs in CCs, as shown by microautoradiography
(Nuske and Eschrich, 1976).
Most of the phloem proteins are probably synthesized
in CCs and trafficked through PD into the SEs. It has
been shown that several phloem proteins from Ricinus
communis and Cucurbita maxima, e.g. glutaredoxin and
cystatin, are able to interact with mesophyll PD to
increase their size exclusion limit (SEL) (Balachandran
et al., 1997). Surprisingly, Ishiwatari and coworkers were
able to identify thioredoxin h as the major protein in the
rice phloem sap, probably due to the absence of p-
proteins from many monocots (Ishiwatari et al., 1995).
P-proteins are reportedly absent from many monocots
(Cronshaw, 1981). Co-injection experiments in rice with
fluorescently labelled dextrans demonstrated that thiore-
doxin h can mediate its own cell-to-cell transport through
PD by modifying the plasmodesmal SEL values to greater
than 9.4 kDa, (Ishiwatari et al., 1998). It has been argued
that this reductase could play a role in repair of other
phloem proteins (Raven, 1991), or as a regulator of
phloem-specific enzymes. By promoter-reporter gene
fusions, Ishiwatari and coworkers were able to show that
the thioredoxin promoter drives reporter gene mRNA
accumulationin SEs, whereas
b-glucuronidase (GUS) reporter protein was not detected
in SEs, but in the neighbouring CCs (Sasaki et al., 1998).
The phloem sap not only contains proteins, but also
different mRNA species. Besides thioredoxin mRNA,
several other mRNAs have been detected in the phloem
sap of rice by RT-PCR, e.g. actin mRNA, whereas
detection of cystatin mRNA failed (Sasaki et al., 1998).
Fisher et al. (1992) collected phloem proteins of wheat
using radiofrequency microcautery and analysed the turn-
over of about 100 soluble phloem proteins by 35S-
methionine labelling. From a total of almost 200 soluble
proteins, they were able to separate about 100 polypep-
tides by two-dimensional gel electrophoresis, which turned
over rapidly. The analysis of rice phloem sap by SDS-
PAGE indicated that it contains over 150 different pro-
teins (Nakamura et al., 1993). After application of (c-
Sieve element proteins
Besides ions and metabolites, the phloem sap contains a
distinct set of SE-specific proteins. Using the insect laser
technique, Nakamura et al. (1993) collected a set of
proteins from the rice phloem sap, the composition of
which remained stable over a 6 d period. This surprising
finding suggests that some of the SE proteins are subject
to constant de novo synthesis. The most abundant of the
phloem proteins are the structural P-proteins occurring
in either crystalline (P-protein bodies) or filamentous
form (P-protein tubules and filaments) in the SEs
(40–100 mg mg−1
(Eschrich, 1975). P-protein filaments, which may play a
role in plugging sieve pores, are composed of PP1, a
filamentous protein of 90–100 kDa, and PP2, a phloem
lectin of 23–28 kDa with haemagglutinating properties,
that binds to PP1 as a dimer (for review, see Cronshaw
and Sabnis, 1990). PP2 mRNA from cucurbits has been
localized by RNA in situ hybridization exclusively in CCs,
whereas PP2 protein has been detected in both SEs and
CCs (Bostwick et al., 1992).
The identification of structural phloem proteins was
successful by the use of monoclonal antibodies against
purified SEs isolated from Streptanthus callus cultures
(Sjo ¨lund, 1990). One of the antibodies interacts specific-
ally with a SE specific b-amylase of 57 kDa (Wang et al.,
1995a). Antibodies against P-proteins also gave positive
signals (Toth and Sjo ¨lund, 1994; Toth et al., 1994).
Soluble phloem proteins which are present in lower
abundance in the phloem sap are still being identified
(Marentes and Grusak, 1998). The term ‘sieve tube
exudate proteins’ (STEPs) has been introduced to describe
the diversity of unknown phloem proteins (Sakuth et al.,
1993). The soluble proteins could be involved in sieve
tube plugging, SE maintenance or information transfer
between sink and source organs (Raven, 1991). Ubiquitin
and chaperones have been detected in the phloem sap of
Ricinus (Schobert et al., 1995) and the polyubiquitin
cDNA was found in a cDNA library from the phloem of
pine (Alosi-Carter et al., 1995). Ubiquitin and chaperones
may be involved in the degradation of phloem proteins
in enucleate SEs, explaining the high selectivity of the
autolytic degradation processes occurring during SE
Stability and turnover of SE proteins
Although it has been known for many years that enucleate
SEs contain soluble proteins at low concentration, it is
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Ku ¨hn et al.
32P)ATP to leaf blades, the authors observed a light-
dependent phosphorylation and dephosphorylation of
different phloem proteins. Proteins in the rice phloem sap
were also phosphorylated in vitro. It has been hypothes-
ized that phosphorylation of phloem proteins is part of a
The presence of ubiquitin and chaperones in the phloem
sap (Schobert et al., 1995), as well as the presence of
thioredoxin h disulphide-reductase as a potential repair
enzyme or regulatory enzyme (Ishiwatari et al., 1995),
are hints that SEs have the capacity to metabolize pro-
teins. Phloem exudate collected from different species by
the aphid method was shown to have the ability to
like ATP, very similar to those synthesized after the whole
phloem is incubated with 32PO3−
that phosphorylating enzymes are present in the phloem
sap which had been deprived of mitochondria by centrifu-
gation (Becker et al., 1971). Neumann and Wollgiehn
found as early as 1964, that mature SEs of Vicia faba are
able to incorporate 3H-phenylalanine (Neumann and
Wollgiehn, 1964). Thus it seems possible that phloem
proteins are not only turned over in CCs, but to a certain
extent in mature SEs as well.
The mobility of phloem proteins was confirmed by
interspecific and intergeneric graft experiments (Golecki
et al., 1998). Sieve pores do not hinder the phloem
translocation of proteins, and soluble phloem proteins
Interestingly, stock-specific proteins have been detected
by immunolocalization after grafting, not only in the SE
of the scion, but also in the CCs, arguing for the capacity
of macromolecules such as proteins to traffic through the
Pore-Plasmodesmata-Units connecting SEs with CCs
(PPUs, see below) in both directions. Thus it seems that
macromolecular trafficking via PPUs is bi-directional.
(Mu ¨nch, 1930). The model of mass flow-driven sucrose
translocation would require the osmotic isolation of the
conducting elements of the phloem, namely the SECCC.
According to a more realistic model of Mu ¨nch’s theory,
sucrose is lost by diffusion during transport towards the
sink organs, requiring an active retrieval mechanism along
the translocation path. Loss of sucrose by diffusion
depends strongly on the flow rate: the higher the rate of
translocation, the lower the loss of sucrose by diffusion
into the tissue surrounding the SECCC.
Models of phloem loading
into a series of organic compounds Two mechanisms of phloem loading are discussed: (1)
the symplasmic path via PD, connecting mesophyll cells
and the conducting elements of the phloem and (2) the
apoplasmic route, in which sucrose is first exported into
the apoplast and is then taken up into the SECCC by an
energy-dependent transport system. Plants appear to show
preferences for different types of transport molecules
based on their mode of phloem loading (van Bel and
Anatomical features have been used to categorize plant
species based on their mechanism of phloem loading
(Gamalei, 1989; van Bel, 1993; Flora and Madore, 1996).
According to the plasmodesmal frequency between the
SECCC and the surrounding cells of minor veins, where
phloem loading is thought to take place, plants can be
classified into three groups: open type I minor veins have
multiple PD between the SECCC and phloem paren-
chyma, bundle sheath or mesophyll cells. CCs are often
modified into intermediary cells, and phloem loading is
thought to occur symplasmically. The best example of a
type I minor vein configuration are cucurbits (e.g.
Cucurbita melo with extensive IC configuration). In these
species, galactosyl oligosaccharides such as stachyose,
raffinose and verbascose rather than sucrose are the
principal transport sugars (Gamalei, 1985; Bachmann et
al., 1994). In the latter case the osmotic potential per
loaded carbon atom is lower than that of sucrose, allowing
only reduced translocation rates. This results in a higher
energy loss due to retrieval of diffused photoassimilates,
but at the same time requires less energy for phloem
loading per carbon atom, thus potentially leading to a
more or less comparable energy balance. A physiological
hint for symplasmic carrier-independent phloem loading
is the insensitivity toward thiol group-modifying agents
such as p-chloromercuribenzene-sulphonic acid (PCMBS)
or N-ethylmaleimide (NEM) (Giaquinta, 1976; Delrot et
al., 1980; van Bel et al., 1994).
In minor veins classified into the primitive closed type
IIa group (e.g. Nicotiana tabacum), symplasmic connectiv-
ity of the SECCC is low to moderate, whereas in type IIb
(e.g. Vicia faba, Fabaceae) the SECCC is almost sym-
plasmically isolated from the surrounding cells, making
4. Thus it was concluded,
SE plasma membrane.
Sucrose as the main transport molecule
Most plants use sucrose as the transport metabolite for
long distances. Physicochemical properties of the sucrose
molecule could be one reason for this preference. Even
in solutions of high concentration, such as phloem sap,
with a sucrose concentration in the range of 200 to
1600 mM, viscosity is relatively low allowing high translo-
cation rates (0.5 to 3 m h−1). An additional advantage
of sucrose over reducing sugars is the chemical stability
of the non-reducing disaccharide. Furthermore, sucrose
creates a high osmotic potential per carbon atom, in the
phloem sap, a key parameter for translocation efficiencies
within long tubes (van Bel, 1996).
The translocation rates in the phloem are thought to
be driven by mass flow, due to water molecules entering
the phloem with sucrose loading and thereby creating an
osmotic pressure gradient along the transport route
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Sucrose transport in higher plants
it indispensable to include an apoplasmic step in the
process of phloem loading. In a number of ‘apoplasmic’
species, prominent transport carbohydrates are sugar
alcohols like mannitol and sorbitol (Loescher, 1987).
These plants often show a modification of either the CCs
or the parenchyma cells of minor veins, to transfer cells.
However, the significance of the classification has been
criticized (Turgeon, 1996). A number of type I plants,
especially trees, were shown mainly to transport sucrose.
Furthermore, the bias towards having monotypic families
is due to the type of analysis, in most cases only a single
species was analysed per family. Thus, a generalization
of the correlation between structure and the loading
mechanism requires further analysis, i.e. antisense repres-
sion of sucrose transporters in a variety of species
belonging to different structural categories.
Transfer cells are characterized by numerous cell wall
invaginations, allowing up to a 20-fold increase in the
plasma membrane surface area (Pate and Gunning, 1972;
Gunning, 1977; Bonnemain et al., 1991). The presence of
transfer cells in specific areas seems to correlate with the
existence of intensive solute fluxes between symplasm and
apoplasm (Gunning, 1977; Offler et al., 1989). Transfer
cells exist either as modified CCs (type A) with high
cytoplasmic density and cell wall invaginations all over
the cell, or as modified phloem parenchyma cells (type
B), with polarized invaginations that are highest at the
opposite side to the SECCC. It has been shown that the
transfer cell wall is pectin-rich and can be highly hydrated,
a phenomenon which facilitates solute uptake from the
apoplasmic space. Appearance of transfer cell modifica-
tion in minor veins correlates with the sink–source trans-
ition of young leaves, an indication that the increase in
the plasma membrane surface area is important for
apoplasmic phloem-loading processes (Turgeon, 1996).
Embryonal transfer cells of Vicia faba show a polarized
organization, with the localization of wall ingrowths at
one pole of the cell and PD at the other pole (Offler et
al., 1989; Bonnemain et al., 1991). This polarized organ-
ization is accompanied by an asymmetric distribution of
the plasma membrane bound H+-ATPase (Bouche ´-Pillon
et al., 1994). Proton pumps are more numerous in the
area of plasma membrane infoldings where active nutrient
uptake is assumed to take place (Harrington et al.,
1997a). ATP hydrolysis by an ATP-energized proton
efflux pump provides a gradient for inward proton
coupled substrate transport across the loading membrane
of phloem cells (Baker, 1978). It is thus likely that in
closed type IIb plant species, the main solute fluxes occur
at the membranes of transfer cells.
The best example of plants showing a type IIb minor
vein configuration with the development of transfer cell
anatomy, are species belonging to the Faboidae family.
Sucrose is the major transport form of photoassimilates
in these plant species. Sucrose uptake into the SECCC
can be inhibited by PCMBS treatment suggesting that
membrane proteins are involved in an active transport
process (Delrot et al., 1980).
Species belonging to the intermediate type I-IIa group
are considered to be symplasmic and apoplasmic loaders
at the same time (e.g. Catharanthus roseus, which has
both CCs and ICs in the minor vein phloem and which
translocates sucrose as well as raffinose within the
The Solanaceae family represents a polytypic family.
Datura belongs to the intermediate type I-IIa among the
Solanaceae (1–10 PD mm−2 interface), whereas Nicotiana
tabacum and Solanum tuberosum belong to the primitive
closed type IIa (with 0.08 PD mm−2 and 0.12 PD mm−2
interface, respectively) (Gamalei, 1991).
Physiological and anatomical classification of uptake
do not always agree. Recently, it was published that
sucrose uptake in peach can be abolished by PCMBS
treatment indicating an apoplasmic uptake system.
However, based on anatomical criteria, the transport
system had been considered to be a symplasmic one.
These findings make it imperative to re-evaluate the
methods used for classification.
Both classification by anatomical characteristics as well
as inhibitor studies using PCMBS have been discussed
controversially. Classification according to simple numer-
ical data of plasmodesmal frequency implies that PD are
holes allowing the diffusion of various substances includ-
ing macromolecules. Recent studies revealed that PD are
dynamic, complex structures, through which the transport
of macromolecules is highly regulated (Lucas et al., 1993;
van Bel and Oparka, 1995). Gamalei and coworkers
found that temperature-induced ER rearrangement cor-
relates with an inhibition of photosynthate transport and
starch accumulation in plants with a symplasmic minor
vein configuration (Gamalei et al., 1994). Another interes-
ting finding which indicates how important PD are for
the mode of phloem loading, is demonstrated in a maize
mutant with an abnormal accumulation of starch and a
lack of phloem export, both of which indicate a disturb-
ance in phloem loading. Russin and co-workers could
show ultrastructurally, that the PD between bundle-
sheath and phloem parenchyma cells were covered by
wall material, and that the path thus was discontinuous.
Moreover, the suberin lamellae in the outer and radial
walls of the bundle sheath cells forms a barrier for
apoplasmic solutes (Russin et al., 1996).
On the other hand, inhibitor studies or fluorescent dye
microinjection for determining the plasmodesmal SEL
are indirect or invasive techniques, and it can not be
excluded that observed phenomena are due to secondary
effects of the treatment.
In symplasmic models, sucrose transport through PD
has to overcome a concentration gradient. It is still not
fully understood how the sieve tube system from sym-
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Ku ¨hn et al.
plasmic phloem loaders can increase its already high
osmotic potential by additional solute uptake. Sucrose/
proton cotransport is supposed to be unnecessary, as
sucrose does not have to cross membranes; storage in the
vacuole or regulation at the tonoplast membrane is not
possible since SEs do not have vacuoles. Nevertheless the
existence of a symplasmic connection between mesophyll
cells and minor veins has been demonstrated, e.g. by the
dye tracer method in the symplasmic loader Ipomoea
tricolor (Madore et al., 1986). Solutions for the energy
problem in symplasmic loaders have been proposed by
several authors (Turgeon and Beebe, 1991; Gamalei et
Turgeon proposed the polymerization trap hypothesis
of symplasmic loaders (see below) (Turgeon, 1991). An
alternative theory for the mechanism of symplasmic
phloem loading has been proposed by Gamalei (Gamalei,
1985; Gamalei et al., 1994). In intermediary cells of
symplasmic species, a vesicular labyrinth seems to change
in volume during the transit of photosynthate. Thus, it
could be possible to keep the concentration gradient low
between the cytoplasm of mesophyll cells and phloem
cells just by subcellular compartmentation of the trans-
ported sugars. The energy needed for the accumulation
of sugars in this vacuolar-vesicular endoplasm is compar-
able to that invested for apoplasmic loading (van Bel,
1996). For an extensive review on the role of PD in
symplasmic phloem loading, see Turgeon (1996).
to a specific physiological task. One example is the PD
of CCs, modified into intermediary cells, which can be
found in many cucurbits and in several other families;
another are the PD between SEs and CCs. These two
special cases of asymmetrically branched PD will now be
Pore-plasmodesma units (PPUs)
These plasmodesmal structures are branched at their CC
end and single where they join the SE and frequently
contain a large central cavity. As the nature of these PD
differs to most, having a pore-like orifice at their SE end,
they have been designated pore-plasmodesma units
(PPUs) (van Bel, 1996). They differ from PD between
parenchyma cells in organization and diameter and appar-
ently also in regulation. Whereas the SEL of PD is about
800–1000 Da, which is similar to that reported for animal
gap junctions (Spray and Bennett, 1985), SELs of PPUs
seem to have much higher limits. The SEL of PPUs in
the fascicular phloem of Vicia faba has been determined
using fluorescent dextrans to be at least 10 kDa (Kempers
and van Bel, 1997).
PPUs seem to be permanently open. In other tissues,
closure of PD in response to wounding by microinjection
has been observed, while PPUs seemed to be unable to
close (Kempers and van Bel, 1997). It would be interes-
ting to investigate whether viral movement proteins,
which spread specifically via the phloem, are able to
modify the molecular exclusion limit of these structures.
The role of plasmodesmata in phloem loading
Intermediary cell plasmodesmata
One problem in studying the role of PD is that they
constitute extremely small functional units and the reso-
lution of electron microscopes is limited. Electron micro-
graphs are only static images of fixed cells, whereas PD
appear to be dynamic and highly regulated devices, which
are able to open and close according to the environmental
conditions (Kragler et al., 1998).
Methods like High Resolution Scanning Electron
Microscopy (CLSM), microinjection of fluorescent dyes,
GFP-tagged virus movement, biolistic bombardment or
immunolocalization of plasmodesmal components could
help understand plasmodesmal functioning. Recently, the
association of cytoskeletal elements like actin or myosin-
like proteins with plasmodesmal structures was shown in
higher plants and in Chara corallina (White et al., 1994;
Blackman and Overall, 1998; Radford and White, 1998).
It is hypothesized that these cytoskeletal elements could
play a role in the targeting and transport of macro-
molecules through PD. They could also play a role in
cell-to-cell transport by interaction with the ER tubule
within PD, either by rearranging it, or by moving it
through the PD.
In some cases the structure of PD is closely connected
Minor vein CCs modified into intermediary cells (IC)
can be found in plant species that are mostly described
as symplasmic phloem loaders (Cucurbitaceae). IC are
connected with surrounding cells, namely the phloem
parenchyma or bundle sheath via numerous asymmetric-
ally branched PD. The neck region of these special PD
(having more branches at their IC end) is narrower at
the IC end, allowing them to act as a size discrimination
filter. The polymerization trap model (Turgeon and
Gowan, 1990), which illustrates one possible mechanism
of symplasmic phloem loading, is based on a selective
filtration by these narrowed sphincter regions of PD.
Thus the size discrimination function of PD inhibits
diffusion back into the bundle sheath/mesophyll area of
raffinose and stachyose, both of which are larger sugar
molecules, synthesized from sucrose after symplasmic
loading into the IC. Enzymes involved in raffinose or
stachyose synthesis have been immunolocalized to inter-
mediary cells (Holthaus and Schmitz, 1991; Beebe and
Turgeon, 1992). The galactosyl-oligosaccharides are sub-
sequently loaded (again via PD) into the SE. To maintain
a low sucrose concentration in the cytoplasm of IC and
a sucrose concentration gradient between bundle sheath
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Sucrose transport in higher plants
and IC, sucrose is removed from the cytoplasm by
subcellular compartmentation or by storage in the vacu-
ole. Ultrastructural analysis of the IC revealed that they
are highly vacuolated compared to normal CCs.
the phloem, an apoplasmic invertase could be involved
in sucrose degradation and the sucrose cleavage prod-
ucts could be imported via monosaccharide trans-
porters (Turgeon, 1989; Wright and Oparka, 1989).
expressed in sink tissues have been isolated from
Arabidopsis and tobacco (Sauer et al., 1990; Sauer and
Stolz, 1994). However, active monosaccharide transport
has also been detected in plasma membrane vesicles from
sugar beet leaves (Tubbe and Buckhout, 1992). The
function of these transporters might be to prevent accu-
mulation of hexoses in the apoplast. Furthermore, under
certain conditions, source tissues can switch to sink
function. Typical examples are responses to wounding or
pathogen infection, where dramatic reallocation of nutri-
ents is required to sustain defence and repair responses.
In agreement with this, the expression of a monosacchar-
ide transporter is up-regulated locally in leaves after
wounding by pathogen infection (Truernit et al., 1996).
The mechanisms of phloem unloading are less well charac-
terized than the mechanisms of phloem loading. It is
assumed that the path of unloading can not only vary
between species, but also in a tissue-dependent or even
developmentally regulated manner (Turgeon, 1989). The
coexistence of several unloading mechanisms in one
organism (or in one sink organ) was discussed. In tomato
fruit, for example, it is possible that there is a develop-
mental switch from symplasmic to apoplasmic phloem
unloading (Miron and Schaffer, 1991; Offler and Horder,
1992; Ruan and Pattrick, 1995).
The efficiency of phloem unloading depends, among
other factors, on the sink strength of the corresponding
tissue. The sink strength is determined by the activity of
enzymes involved in sucrose catabolism and/or starch
Three different models of phloem unloading are discus-
sed. In sink organs, the assimilate concentration is higher
in the phloem than in the surrounding sink tissue, thus
unloading by facilitated diffusion along a concentration
gradient would be one possibility. In order to maintain a
constant concentration gradient, sucrose is either con-
verted into osmotically less efficient storage molecules
such as starch or amino acids, or is cleaved or stored in
subcellular compartments, e.g. in the vacuole.
Phloem unloading in seeds is well characterized. In most
species, the embryonal tissue is symplasmically isolated
from the maternal tissue, a strong indication for apo-
plasmic solute transport into the seeds (Thorne, 1985).
Detailed studies regarding the role of osmotic pressure in
the regulation of phloem unloading in seeds were per-
formed by Patrick (1993). A detailed description of the
pathway and mechanism cannot be covered in this review.
Furthermore, several excellent reviews have been pub-
lished recently on this topic (Offler et al., 1989; Patrick,
1997; Weber et al., 1998).
Tubers Sink leaves
Symplasmic phloem unloading via PD has been postu-
lated for sink leaves of sugar beet (Schmalstig and Geiger,
1985, 1987) and tobacco (Turgeon, 1987), as unloading
cannot be inhibited by thiol-group modifying agents
Using non-invasive imaging techniques, Roberts and
coworkers compared phloem unloading of the membrane-
impermeant, fluorescent solute carboxyfluorescein (CF)
with that of a green fluorescent protein (GFP)-tagged
potato virus X in sink leaves of Nicotiana benthamiana.
Unloading of both solute and virus occurred predomi-
nantly from the class III vein network, a highly branched
veinal system found between class II veins. The minor
veins (classes IV and V) played no role in solute or virus
import. During the sink–source transition, phloem
unloading of CF was inhibited from class III veins before
the cessation of phloem import through them, suggesting
a symplasmic isolation of the phloem in class III veins
before its involvement in export (Roberts et al., 1997).
After apoplasmic, carrier-mediated sucrose release from
The symplasmic connections between the conducting
phloem cells and the storage parenchyma cells of potato
tubers are numerous, thus indicating that symplasmic
phloem unloading is possible (courtesy of A van Bel,
personal communication, depicted in Frommer and
Sonnewald, 1995). Investigations with fluorescent dyes
indicate that metabolites can also be loaded from the
apoplasmic space into the parenchyma cell cytosol by
endocytosis (Oparka and Prior, 1988). Nevertheless, suc-
rose transport activities, which can be inhibited by
application of PCMBS have been detected in potato
tubers (Wright and Oparka, 1989). As mentioned above,
sucrose transporter proteins from higher plants are sensit-
ive towards thiol-group modifying agents such as PCMBS
(Giaquinta, 1976; Delrot et al., 1980). Expression of a
yeast invertase in the apoplast of potato tubers led to a
reduced number of tubers, but simultaneously to an
increase in tuber yield (Heineke et al., 1992), indicating
that during unloading sucrose is at least partially released
into the apoplasmic space. It cannot be excluded that so
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Ku ¨hn et al.
far unknown sucrose carriers or mechanisms, are involved
in this process (Oparka et al., 1992).
Structure of sucrose transporters
Amino acid sequence comparison of the two sucrose
transporters StSUT1 and SoSUT1 which were isolated
by yeast complementation, show 83% similarity and 68%
identity (Riesmeier et al., 1993). Their predicted molecu-
lar mass is about 54 kDa, while hydrophobicity analysis
indicates a structure for an integral membrane protein
with 12 putative transmembrane domains, with a central
hydrophilic loop, resulting in the characteristic 6-loop-6-
cotransporters (Henderson, 1990; Kaback, 1992). This is
the characteristic feature of the family of the so-called
major facilitator superfamily (MFS) (Marger and Saier,
1993). The second loop of the transporters contains a
highly conserved motif (RXGRR), which can be found
at the same position in the E. coli lactose permease
(Henderson, 1990). Other structural motifs have been
described in detail (Ward et al., 1998).
Several studies regarding phloem unloading in roots came
to the same observation, that unloading in this tissue
occurs symplasmically (Dick and ap Rees, 1975; Farrar,
1985, 1992; Warmbrodt, 1987).
Unloading of a fluorescent dye in Arabidopsis roots
was visualized using confocal laser scanning microscopy
(CLSM) to occur only at the root tip, from SEs of the
protophloem. Unloading of the fluorescent dye could not
be observed in other regions of the root, where SEs of
the metaphloem are active (Oparka et al., 1994).
These results are consistent with the frequency of PD
in both regions of the root: the SECCC of the so-called
transport phloem (metaphloem) is symplasmically almost
isolated from the surrounding tissue (van Bel, 1993). It
can not be excluded, that in this region of the phloem,
carrier-mediated apoplasmic sucrose unloading takes
place. Schulz (1994) found in pea cotyledons that
unloading of 14C-labelled sucrose occurs mainly along
the elongation zone at the root tip, a region which
exclusively contains mature SEs of the protophloem.
These data suggest that symplasmic unloading from cells
of the protophloem is the most important pathway of
assimilate unloading in the root.
Biochemistry of SUT1-mediated sucrose uptake
Sucrose transport characteristics of StSUT1 and SoSUT1
were first determined in yeast cells by 14C-labelled sucrose
uptake studies. Sucrose uptake was pH-dependent, with
a Kmof 1.5 mM and 1 mM sucrose for SoSUT1 and
StSUT1, respectively. Uptake can be inhibited by maltose
(Kmof 5 mM for SoSUT1 and 10 mM for StSUT1), by
protonophores such as 2,4-dinitrophenol (2,4-DNP) and
carbonyl-cyanid-m-chlorophenylhydrazone (CCCP), and
by agents covalently modifying specific amino acid res-
idues such as PCMBS and diethylpyrocarbonate (DEPC).
The effect of PCMBS can be partially reversed by the
addition of dithiothreitol (DTT) (Riesmeier et al., 1992,
1993). These data were in accordance with previous
measurements using leaf discs and plasma membrane
vesicles (Giaquinta, 1976; Delrot et al., 1980) and were
confirmed by Lemoine et al. (1996) with potato plasma
membrane vesicles (for reviews see Delrot, 1989; and
The transport mechanism of StSUT1 was measured
electrophysiologically in Xenopus oocytes using the
2-electrode voltage clamp and radiotracer flux method.
SUT1 mediated sucrose-dependent inward currents and
displayed Michaelis-Menten-type kinetics with a 1:1
H+/sucrose stoichiometry (Boorer et al., 1996). The
stoichiometry is in accordance with measurements using
plasma membrane vesicles from sugar beet (Bush, 1990;
Slone et al., 1991) or electrophysiological measurements
with AtSUC1 from Arabidopsis (Zhou et al., 1997). The
affinities of SUT1 for H+ and sucrose were voltage-
dependent. A model can be deduced from the electro-
physiological data, in which protons bind to StSUT1
before sucrose and then both ligands are transported
simultaneously across the membrane.
Characterization of sucrose transporters
Complementation of yeast is a powerful tool to isolate
plant membrane proteins (Frommer and Ninnemann,
1995). At first appearance, Saccharomyces cerevisiae is
unsuitable for isolating plant sucrose transporters by
complementation due to the excellent growth of baker’s
yeast on sucrose-containing media. This is due to the
secretion of an invertase which cleaves sucrose extracellu-
larly. Thus, wild-type yeast was modified by deleting the
secreted invertase activity and simultaneously inserting
the potato sucrose synthase gene, thereby enabling yeast
cells to metabolize ingested sucrose. Using this comple-
mentation system, it was possible to isolate cDNAs of
two plant sucrose transporters from spinach and potato
(Riesmeier et al., 1992, 1993). The yeast complementation
system also allowed the biochemical characterization of
SUT-mediated sucrose uptake (see below).
Heterologous screening of cDNA or genomic libraries
was successfully used to identify homologous genes from
other species, as well as to show the presence of more
than one carrier within a single species. Detailed sequence
comparisons and phylogenetic studies show that, in most
cases, gene amplifications must be relatively old, thus
predicting specific functions for the individual members
of the family (Rentsch et al., 1998).
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Sucrose transport in higher plants
Physiological role of SUT1 in Solanaceae
ultrastructurally (Schulz et al., 1998). In antisense plants,
starch grains were prominent throughout the mesophyll
and bundle sheath cells, but decreased in number and
size in phloem parenchyma and CCs. Also oleosomes
were found in the mesophyll and vascular parenchyma
cells, indicative of a universal build-up of assimilates in
the leaf at the border of the SECCC.
The observed effects of the CC-specific inhibition, qual-
itatively evoking the identical distribution of starch as
the constitutive SUT1-inhibition, emphasize that the loca-
tion of the bottleneck of phloem loading is at the SECC
boundary. It can not be excluded that pre-phloem loading
occurs by symplasmic transfer of assimilates from the
mesophyll up to the SECC boundary, but thereafter
assimilates are released into the apoplast, and are sub-
sequently loaded into the SECCC. Taken together, the
effects observed in antisense plants demonstrate that
SUT1 is essential for sucrose loading into the phloem via
an apoplasmic route and also possibly in inter-mesophyll
transport as well.
An alternative way to check the physiological role of
sucrose transporters could be the analysis of knock-out
mutants which can be identified, for example, by screening
T-DNA tagged Arabidopsis mutants by PCR (Krysan et
al., 1996). So far, no successful identification of sucrose
transporter mutants has been described.
Inhibition of SUT1 expression in potato and tobacco
(Riesmeier et al., 1994; Ku ¨hn et al., 1996; Bu ¨rkle et al.,
1998) using the antisense approach led to comparable
defects in transgenic plants. The antisense plants showed
increased concentrations of soluble sugars and starch in
their source leaves, as expected for a block in the transport
of sucrose into the phloem cells. Sucrose and starch were
increased 5–10-fold and hexoses even more. Phos-
phorylated hexoses and other intermediate metabolites of
the sucrose biosynthetic pathway were unchanged in these
plants compared to wild-type plants. The leaves developed
a characteristic phenotype which could be related to a
change in osmotic conditions within the leaf tissue due
to the accumulation of carbohydrates. Development of
this phenotype strongly depends on the light period and
intensity (Ku ¨hn et al., 1996). A similar accumulation of
soluble carbohydrates was found when phloem transport
was inhibited by treatments like heat- or cold-girdling
(Grusak et al., 1990; Krapp et al., 1993). The leaves of
tobacco antisense plants showed an impaired ability to
export recently fixed 14CO2and were unable to export
transient starch during extended periods of darkness,
leading to an accumulation of soluble carbohydrates and
a reduction in photosynthetic activity. Autoradiographs
of leaves showed a heterogenous pattern of CO2fixation
which is maintained even after 24 h of darkness, sug-
gesting that movement of photosynthate between meso-
phyll cells may also be impaired (Bu ¨rkle et al., 1998).
Transgenic plants with a reduced amount of sucrose
carrier mRNA showed a reduction in the development of
the root system and delayed or impaired flowering, and
in potato antisense plants, tuber yield was dramatically
Antisense inhibition of SUT1 expression using the
CC-specific rolC promoter led to similar effects in trans-
genic potato plants (Ku ¨hn et al., 1996). It is interesting
that sucrose uptake in plasma membrane vesicles isolated
from constitutively inhibited potato antisense plants was
shown to be significantly reduced, whereas sucrose uptake
by vesicles isolated from phloem-specifically inhibited
antisense plants was not reduced compared to wild-type
plants (Lemoine et al., 1996). The uptake measurements
correlate with Western blot data, in which the amount of
SUT1 protein was not reduced in rolC plants, whereas
almost no SUT1 protein could be detected in constitutive
antisense plants. The authors concluded that SUT1 may
also be expressed to low levels in cells other than phloem
cells, masking the actual amount of sucrose transport and
SUT1 protein in the phloem. So far, it was not possible
to define the control coefficient of SUT1, which would
indicate the significance of the transporter in the process
of phloem loading.
Both sets of potato antisense plants have been analysed
Localization of SUT1 in the phloem
Tissue-specific Northern blot analysis revealed the main
expression of SUT1 in mature leaves and, to a lower
extent, in sink organs. GUS reporter gene expression
under the control of the LeSUT1 promoter drives expres-
sion in potato plants in the phloem (Hirner, unpublished
results). The SUT1 expression pattern was comparable
to the analogous transporter AtSUC2 from Arabidopsis
thaliana (Truernit and Sauer, 1995). GUS staining was
also found in the transport and delivery phloem such as
the vasculature of potato tubers, suggesting a role of
SUT1 not only in phloem loading, but also in retrieval
during long-distance transport and in phloem unloading
in sink organs. These expression data have been confirmed
by RNA in situ hybridization (Riesmeier et al., 1993).
To dissect out the role of the transporter in different
plant organs, tissue-specific promoters have been used to
decrease SUT1 expression either in the phloem (rolC
promoter) or in potato tubers (B33 patatin promoter).
Several independent transformant lines showed reduced
SUT1 mRNA levels if antisense expression was under the
control of either the rolC or the patatin promoter (Ku ¨hn
et al., 1996). The rolC promoter has been shown to drive
CC-specific expression in transgenic tobacco plants
(Ku ¨hn et al., 1996). Efficient antisense inhibition of SUT1
using this CC-specific promoter, together with the pheno-
typical symptoms of these antisense plants, indicates that
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Ku ¨hn et al.
SUT1 mRNA transcription takes place in CCs. To deter-
mine expression at the cellular level, immunolocalization
immunofluorescence and silver-enhanced immunogold-
staining, detected SUT1 in plasma membranes of enuc-
leate SEs of tobacco, potato and tomato (Ku ¨hn et al.,
1997). SUT1 was found both in adaxial (inner) and
abaxial (external) phloem in leaves and stems, respect-
ively. The protein was not only found in minor veins of
source leaves but also in stems, petioles and roots.
Interestingly, SUT1 could only be detected in the SE of
the root metaphloem and not in the protophloem SE,
which are not accompanied by CCs, but which are highly
connected by PD to their surrounding cells. This is in
agreement with the finding that unloading from pro-
tophloem SEs is thought to occur symplasmically (Oparka
et al., 1994). In situ hybridization at the EM level also
showed that SUT1 mRNA localizes to both SEs and
CCs, and is preferentially associated with the orifices of
the PD. The mRNA localization, together with the
CC-specific antisense inhibition of SUT1, indicate that
transcription of SUT1 mRNA occurs in CCs. A con-
sequence of the differential distribution of SUT1 mRNA
and protein is that either the mRNA or the protein has
to be translocated via the specific pore plasmodesma units
(PPU) from the CC into the SE, and that phloem loading
with sucrose occurs directly at the plasma membrane of
SEs. Trafficking of macromolecules through PD is a well-
known phenomenon for viral cell-to-cell movement in
plants, which is usually facilitated by the interaction of
viral movement proteins with plasmodesmal components
(Lucas and Gilbertson, 1994; Almon et al., 1997). It has
also been described for endogenous plant proteins, e.g.
the transcription factor KNOTTED1 (Kn1) (Lucas et
al., 1995). In several cases, both protein and mRNA are
transported from cell to cell. The mRNA molecules could
be guided to the PPUs by the help of cytoskeletal compon-
ents, whereas the SUT1 protein could be targeted to the
SE either as part of the ER or as part of the plasma
membrane, both of which are continuous through the PD
(Overall and Blackman, 1996).
Asymmetric mRNA distribution and polarized trans-
port of mRNA within and between cells has been observed
for example during Drosophila oogenesis (St Johnston,
1995). If SUT1 mRNA is translocated, then it has to be
translated in the SE, which lose the majority of their
ribosomes during maturation. In 1964, Neumann and
Wollgiehn studied the incorporation of 3H-uridine and
3H-phenylalanine into young nucleated and mature enuc-
leated SEs from Vicia faba. They could detect 3H-uridine
incorporation into RNA molecules only in the early
stages of SE differentiation but, in contrast, could detect
3H-phenylalanine incorporation into proteins even after
the disintegration of the SE nucleus (Neumann and
Wollgiehn, 1964). It will therefore be essential to
re-evaluate the paradigm of the absence of ribosomes in
mature SEs, using immunolabelling techniques for
Interestingly, SUT1-protein is also present in young,
still nucleated SEs found in elongating internodes (Ku ¨hn
et al., 1997) (Fig. 1). This finding fits nicely with older
reports that these cells may already be active in sugar
transport (Schumacher, 1933; Lackney and Sjo ¨lund,
1991). It would be interesting to answer the question of
the half-life of the transporter. Prolonged dark treatment
of potato plants led to a rapid decrease in StSUT1 protein
and investigations using cycloheximide as a translational
inhibitor indicate a high turnover rate, i.e. within a few
hours. A more detailed determination of the half-life will
help to elucidate at which stage of development SEs start
to be dependent upon protein or RNA imported from
Sucrose transporters belong to a large family
By heterologous screening of cDNA or genomic libraries
using the transporters isolated by yeast complementation
as probes, it was possible to identify several other sucrose
transporter genes from a variety of plants (Fig. 2). As
for monosaccharide transporters, sucrose transporters
also seem to belong to a large gene family. Several sucrose
transporters are known from Lycopersicon esculentum
(LeSUT1, LeSUT2 and LeSUT4: L Barker, unpublished
results), from Nicotiana tabacum (NtSUT1: (Bu ¨rkle et al.,
1998); NtSUT3: R Lemoine, unpublished results), Beta
vulgaris (BvSUT1: accession number 1076257) and
Plantago major (PmSUC1 and PmSUC2: Gahrtz et al.,
1994). The search for new sucrose transporters from
Arabidopsis thaliana is facilitated by the Arabidopsis
genome project: so far at least six different sucrose
Fig. 1. Immunolocalization of StSUT1 in young still nucleated SEs
right after asymmetric cell division from the neighbouring CC. Nuclei
are stained with DAPI. Even at this early stage of SE differentiation,
SUT1 is already detectable in the plasma membrane of SEs, which at
this stage are still autonomous.
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Sucrose transport in higher plants
isolated seeds (Harrington et al., 1997b; Weber et al.,
1997; Tegeder et al., 1999).
The carrot transporters DcSUT1 and DcSUT2 are
differentially expressed: DcSUT1 was only found in the
green parts of the plant with highest expression levels in
the lamina of source leaves; it was diurnally regulated,
indicating a role in phloem loading. In contrast, DcSUT2
expression was mainly found in sink organs and had no
diurnal expression pattern. This carrot transporter may
be involved in the loading of sucrose into storage paren-
chyma cells (Shakya and Sturm, 1998).
In Plantago and Arabidopsis, immunofluorescence with
specific antibodies detected the SUT1 homologue termed
SUC2, in CCs (Stadler et al., 1995; Stadler and Sauer,
1996). The AtSUC2-promoter drives expression of the
GUS reporter gene in the phloem cells of exporting leaves,
but also in sink organs such as roots, sepals and filaments
of flowers and in young siliques of transgenic Arabidopsis
plants (Truernit and Sauer, 1995). A potential role in
phloem loading and unloading has been discussed as in
the case of SUT1.
Whereas PmSUC2 is mainly expressed in the loading
phloem of source leaf minor veins, PmSUC1, is expressed
in young ovules (Gahrtz et al., 1996) and also in leaf
vascular bundles. The cell specificity of PmSUC1 and
PmSUC2 was shown immunocytologically: PmSUC2,
which is thought to be responsible for phloem loading
was localized to CCs, while PmSUC1 antibodies labelled
starch-containing cells of developing seeds, putatively the
endosperm and the SEs of the transport phloem in petioles
(Stadler et al., 1998).
These data suggest, that in Plantago, phloem loading
occurs in CCs, whereas the main retrieval function during
long-distance transport is localized directly at the SE
plasma membrane. Another possibility is stepwise phloem
loading through several different cells involving two suc-
rose transporters working in parallel with varying cell
It could be possible that different sucrose transporters
are localized in different cell types, allowing a division of
labour, or a phloem loading mechanism which occurs in
several steps in several cells. This was first suggested in
1949 by physiological analyses showing a stepwise sucrose
gradient (different sucrose concentrations) in different
phloem cells (Roeckl, 1949). A stepwise mechanism of
phloem loading could involve several sucrose transporters,
which are so far not characterized in detail, nor localized
at the cell-specific level in all species.
Fig. 2. Computer-aided homology analysis by PHYLIP (Felsenstein,
1993) of aligned sucrose transporters from tobacco (NtSUT1: Bu ¨rkle
et al., 1998), potato (StSUT1: Riesmeier et al., 1993), spinach (SoSUT1:
Riesmeier et al., 1992); tomato (LeSUT1, LeSUT2, LeSUT4 L. Barker,
unpublished results), Arabidopsis (AtSUC1; AtSUC2: Sauer and Stolz,
1994); Plantago (PmSUC1; PmSUC2: Gahrtz et al., 1994, 1996),
Ricinus (RcSUT1: Weig and Komor, 1996), sugar beet (BvSUT1,
accession number 1076257), rice (OsSUT1: Hirose et al., 1997), fava
bean (VfSUT1: Weber et al., 1997), and carrot (DcSUT1, DcSUT2:
Shakya and Sturm, 1998). The numbers indicate the occurrence of a
branch in 100 bootstrap replicates of a given data set. OsSUT1 was
used as the outgroup.
transporters have been isolated (AtSUC1 to AtSUC2:
Sauer and Stolz, 1994; AtSUT2–7: J Ward, unpublished
results; Michel et al., 1998). Recently, the cDNAs of two
sucrose transporters from carrot have been characterized
(Daucus carota: DcSUT1 and DcSUT2, Shakya and
Additionally, SUT1 homologues were found in Ricinus
communis (RcSUT1: Weig and Komor, 1996), Oryza
sativum (OsSUT1: Hirose et al., 1997), Vicia faba
(VfSUT1: Weber et al., 1997), Pisum sativum (PsSUT1:
Tegeder et al., 1999), Apium graveolens (AgSUT1:
Noiraud et al., 1998), and grape (Vitis vinifera: Picaud et
Some of these transporters show very specific expres-
sion patterns. NtSUT3 is expressed exclusively in pollen,
suggesting an important role in pollen loading. In Vicia
seeds, cross-hybridization with sucrose transport genes
could be detected in the transfer cells of cotyledons
responsible for sucrose loading into the symplasmically
Efflux of sucrose into the apoplast
Characterization of the isolated sucrose transporters has
increased the amount of information about the mechan-
ism of phloem loading that is now available. However,
what still remains unanswered, is how sucrose exits the
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Ku ¨hn et al.
mesophyll cells (its site of synthesis) and enters the
apoplast. Sucrose efflux into the apoplast prior to phloem
loading could occur from the mesophyll cells or directly
at the interface of the SECCC. Mechanistically, the release
carrier could be a facilitator or an antiporter. Although
a so-called ‘efflux’ carrier was biochemically characterized
from the plasma membranes of Beta vulgaris, the corres-
ponding gene has not been isolated (Laloi et al., 1993).
Characteristics obtained argue for the existence of a
passive sucrose efflux system that is different from the
sucrose/H+ symport responsible for phloem loading. The
existence of efflux carriers has also been postulated in
unloading processes, where sink cells take up sugars from
the apoplast (Patrick and Offler, 1995; Wang et al., 1995b;
McDonald et al., 1996). It is still a matter of debate
whether these carriers function as facilitators or as sucrose
proton antiporters. To date, none of these carriers have
been identified at the molecular level (Patrick and
responsible for a low-affinity sucrose uptake system (Ripp
et al., 1988; Warmbrodt et al., 1989; Grimes et al., 1992).
SBP is a hydrophilic protein, containing an N-terminal
putative membrane spanning domain. The majority of
the protein is located extracellularly, the N-terminal
domain anchoring it to the membrane (Grimes et al.,
1992; Overvoorde and Grimes, 1994). As the protein has
been localized to the plasma membrane of cells with
sucrose uptake capacity, the SEs in spinach and sugar
beet but primarily the CCs in soybean (Warmbrodt et
al., 1989), one assumes that this protein might be involved
in sucrose transport, while its biochemical properties
indicate that it may encode the linear component of
sucrose uptake observed in many transport studies. SBP
is able to mediate radiolabelled sucrose uptake on its own
in the SUSY7 mutant (Overvoorde et al., 1996).
Interestingly, one of two polypeptides purified by sucrose
affinity chromatography from the plasma membranes of
sugar beet leaves, exhibited sucrose transport activity
after reconstitution into proteoliposomes (Li et al., 1994).
As heteromeric structures have been reported for mamma-
lian amino acid transporters (Bertran et al., 1992), one
could postulate that SBP may have a regulatory role in
phloem sucrose transport through interaction with SUT1.
sucrose/H+ cotransporters in the plasma membrane of
Vicia faba transfer cells in developing seeds, and in
cotyledons of Vicia faba (Harrington et al., 1997a; b). In
developing seeds of Pisum sativum, SBP was localized
exclusively in cotlydon epidermal transfer cells, whereas
PsSUT1 and the H+-ATPase were primarily in epidermal
transfer cells, but were also localized to storage paren-
chyma cells (Tegeder et al., 1999) Coexpression of SUT1
and SBP in oocytes might be a suitable approach to test
the hypothesis that SBP also has a regulatory function.
Other proteins complementing sucrose uptake
Complementation of the artificial yeast mutant SUSY7
with a potato cDNA expression library did not allow the
identification of new sucrose transporter genes other than
the already known SUT1. However, a number of plant
genes have enabled the mutant to grow on sucrose,
including PCP1, that shares significant homologies with
zinc finger-containing transcriptional regulators (Ku ¨hn
and Frommer, 1995) and, interestingly, a soybean sucrose
binding protein (SBP) (Overvoorde et al., 1996). The
phenotype observed in yeast expressing one of these
proteins mimicked the functional complementation by a
sucrose transporter. Therefore, it may be concluded that
these proteins suppress the phenotype of SUSY7 by
transcriptional activation of an otherwise inactive endo-
genous sucrose transporter. The presence of such endo-
postulated (Khan et al., 1973; Santos et al., 1982) which,
however, have never been demonstrated at the molecular
level. With the completion of the yeast genome sequencing
project and subsequent classification of all of the open
reading frames corresponding to proteins of the major
facilitator family (Nelissen et al., 1997), characterization
of potential sucrose transporters at the molecular level
has been simplified. That no sucrose transporter has thus
far been identified in Saccharomyces cerevisiae, is no
reason to suggest its absence. As no sucrose transport
occurs under normal growth conditions, but is only
induced in certain circumstances, the transporter(s) may
be structurally sufficiently different from the known plant
sucrose transporters, that no homology is identifiable.
The SBP was isolated from soybean cotyledons using
a photoaffinity labelling technique with a sucrose ana-
logue and has been identified as a potential candidate
was co-localized with
Stability and regulation of sucrose transporter
The activity of sucrose transporter proteins could be
regulated at different levels: at the transcriptional or the
post-transcriptional level, which includes mRNA stability,
protein targeting and modification. It is obvious for
sucrose proton symporter proteins that their activity
strongly depends on the proton motive force which is
established be H+-ATPases. Therefore, the regulation of
sucrose uptake or efflux also includes the regulation of
ATPases. Thus, it is important to discriminate between
direct regulatory effects on sucrose transporters and indir-
ect effects via ATPase activity.
Transcriptional regulation of the enzymes involved in
sucrose and starch biosynthesis seems to be well
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Sucrose transport in higher plants
co-ordinated and depends on the corresponding light
conditions, the developmental stage and the nutritional
status. Thus, the expression profile of the sucrose trans-
porter mRNAs from potato and Arabidopsis is under
developmental control and follows the sink-to-source
transition (Riesmeier et al., 1993; Truernit and Sauer,
The efflux of 14C-labelled sugars and the concentration
of soluble sugars and starch in source leaves is diurnally
regulated in potato and tobacco with a maximum rate at
the end of the light period (Heineke et al., 1994). In
accordance with these export data, the sucrose transporter
SUT1 from tomato and potato is diurnally regulated as
well (Ku ¨hn et al., 1997). It can not be excluded that the
light-induced increase of SUT1 transcripts is based on a
circadian regulation of the transporter. However, also
phytohormones such as auxin and cytokinin have been
shown to increase the rate of phloem loading (Lepp and
Peel, 1970; Patrick, 1976). Harms et al. (1994) showed
that the transcript levels of the potato sucrose transporter
StSUT1 can be increased after application of phytohor-
mones to detached leaves. The effect of auxin (2,4-D)
and cytokinin (BAP) was also detectable on the protein
level (C Ku ¨hn, unpublished results). It can be excluded
that the phytohormones act indirectly via promotion of
the H+-ATPase, since the transcript level of the potato
H+-ATPases PHA1 and PHA2 was shown to be
unchanged after hormone application (Harms et al.,
1994). Hormone regulation of sucrose uptake has been
reviewed by Ward et al. (1998).
In contrast to Harms et al. (1994) who found that the
sucrose transporter StSUT1 from potato is not influenced
at the transcriptional level by application of various
sucrose concentrations, Chiou and Bush (1998) identified
sucrose as a signalling molecule in a previously unde-
scribed signal-transduction pathway that regulates the
sucrose symporter from sugar beet. Sucrose symporter
activity of sugar beet declined in plasma membrane
vesicles isolated from leaves fed exogenous sucrose via
the xylem transpiration stream, due to a decrease in
symporter message levels, suggesting a drop in transcrip-
tional activity or a decrease in mRNA stability. The
decrease in sucrose transporter mRNA levels was revers-
ible and it is discussed that a sucrose-sensing pathway
can modulate transport activity as a function of changing
sucrose concentrations in the leaf (Chiou and Bush, 1998).
This regulation pathway could be an example of ‘sink
regulation’, in which decreasing sink demand led to
increased sucrose concentrations in the phloem, down-
regulating the sucrose symporter. Such a sink regulation
has already been described for photosynthetic genes
(Krapp et al., 1993) and invertases (Roitsch et al., 1995).
One of the most common types of post-translational
regulation of protein activity involves phosphorylation/
dephosphorylation. Very recently, it was shown that
sucrose and valine uptake in leaf discs from Beta vulgaris
can be inhibited by application of okadaic acid (OA), an
inhibitor of protein phosphatases 1 and 2a (Roblin et al.,
1998). These observations were confirmed by measuring
direct uptake into PMV prepared from leaves infiltrated
with OA to exclude possible secondary effects by OA.
H+-ATPase activity was unaffected by OA treatment,
and the amount of transporter proteins did not decrease
as shown by specific antibodies. Roblin and coworkers
therefore suggest that OA acts directly on the activity of
the sucrose and valine transporters by maintaining them
in a phosphorylated form and thus inactivating them. As
mentioned above, phosphorylating enzyme activities
which might be involved in phosphorylation of sucrose
transporters in the SEs have been detected in the phloem
sap (Nakamura et al., 1993).
Targeting of transporters to the plasma membrane
Plant transporters that complement yeast mutants defi-
cient in nutrient uptake must be located in the plasma
membrane. In analogy to membrane protein targeting in
yeast, one might assume that it involved import into the
ER membrane and transfer via the Golgi apparatus and
secretory vesicles to a plasma membrane destination. If
Fig. 3. Confocal imaging of the localization of GFP-tagged LeSUT1
expressed in the yeast strain SUSY7 (Riesmeier et al., 1992). Note that
LeSUT1 is only partially targeted to the plasma membrane of yeast
cells, while some molecules are retained in some perinuclear structures
that are probably ER cisternae. The few molecules that reach the
plasma membrane are sufficient to complement this sucrose uptake-
deficient yeast strain.
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Ku ¨hn et al.
Fig. 4. Model explaining the possible translocation pathway of sucrose during pre-phloem loading and sucrose import into the sieve-element-
companion cell complex, which occurs directly at the plasma membrane of SEs as it has been elucidated in solanaceous plants.
the proteins are not recognized correctly by the yeast
targeting machinery, they may reach their final destination
via unspecific mechanisms (Frommer and Ninnemann,
1995). Studies examining the expression of tomato SUT1
as a translational fusion with GFP in the SUSY7 mutant,
revealed that only a portion of the expressed protein
reaches its plasma membrane destination (C Ku ¨hn,
unpublished results) (Fig. 3). A large proportion remains
within the cell, forming a strongly labelled perinuclear
ring. Antibody detection of the SUT1 transporter revealed
no difference in its localization whether SUT1 was
expressed alone or as a fusion with GFP. Thus, fusing
GFP to the SUT1 protein causes no targeting problems
for the yeast secretory pathway. As the expression of
both of these constructs is able to complement the growth
of SUSY7 on sucrose, the small fraction of the SUT1
protein reaching the plasma membrane is sufficient for
Nakamura et al., 1993). Thus the main prerequisites for
SE specific turnover and degradation are present.
Secondary effects via regulation of ATPases
Many secondary active transport processes across mem-
branes depend on the activity of H+-ATPases. Therefore,
ATPases are a primary target for regulation. Several
factors can regulate ATPase activity. The H+-pumping
activity is regulated via an autoinhibitory domain in the
C-terminal region of the enzyme (Palmgren et al., 1990).
The fungal toxin fusicoccin strongly stimulates H+-
ATPase activity via binding to a protein belonging to the
14-3-3 family, which interacts directly with the autoinhibi-
tory domain of the enzyme (Oecking et al., 1994; Jahn et
al., 1997). Anaerobiosis probably acts at the level of ATP
supply for the H+-ATPase (Giaquinta, 1977; Servaites et
al., 1979; Thorpe et al., 1979; Maynard and Lucas, 1982).
Salicylic acid (SA) inhibited both valine and sucrose
uptake in sugar beet leaf discs in a concentration-
dependent manner. SA acts specifically, but does not
affect the amount of sucrose transporter mRNA or pro-
tein. It has been discussed whether SA affects sugar and
amino acid uptake via inhibition of the H+-ATPase
energizing these processes (Bourbouloux et al., 1998).
Inhibition studies using cycloheximide show that the half-
life of protein turnover is in the range of a few hours
(Ku ¨hn et al., 1997). The turnover rate of the H+-ATPase
from maize has been shown to be very high, in the range
of 12 min after auxin treatment (Hager et al., 1991). The
high turnover rate of these proteins indicates that specific
mechanisms are involved possibly requiring ubiquitin-
ation and internalization by endocytosis, as found for
several yeast plasma membrane transport proteins or
mammalian glucose transporters (Hare, 1990; Hein et al.,
1995). In the phloem sap, ubiquitin was shown to be one
of the major proteins (Schobert et al., 1995). The presence
of ATP and phosphorylating enzyme activities in the
phloem sap has also been shown (Becker et al., 1971;
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