The Plant Cell, Vol. 11, 707–726, April 1999, www.plantcell.org © 1999 American Society of Plant Physiologists
The Dual Function of Sugar Carriers: Transport and
Sugar Sensing
Sylvie Lalonde,a Eckhard Boles,b Hanjo Hellmann,a Laurence Barker,a John W. Patrick,c Wolf B. Frommer,a,1
and John M. Warda
aCenter
for Plant Molecular Biology (ZMBP), University of Tübingen, Auf der Morgenstelle 1, D-72076 Tübingen, Germany
für Mikrobiologie, Heinrich-Heine-Universität Düsseldorf, Universitätsstrasse 1, Geb. 26.12.01, D-40225
Düsseldorf, Germany
cDepartment of Biological Sciences, University of Newcastle, New South Wales 2308, Australia
bInstitut
INTRODUCTION
SUGAR TRANSPORT SYSTEMS IN HIGHER PLANTS
Sucrose and its derivatives represent the major transport
forms of photosynthetically assimilated carbon in plants.
Sucrose synthesized in green leaves is exported via the
phloem, the long-distance distribution network for assimilates, to supply nonphotosynthetic organs with energy and
carbon resources. Sucrose not only functions as a transport
metabolite but also contributes to the osmotic driving force
for phloem translocation (mass flow) and serves as a signal
to activate or repress specific genes in a variety of different
tissues.
The long-distance transport of sucrose depends on a
family of proteins that act as sucrose carriers. The analysis
of transgenic plants impaired in sucrose transporter expression has demonstrated that sucrose transporter1 (SUT1) is
essential for sucrose translocation in potato and tobacco.
These results, together with the localization of SUT1 to sieve
elements (SEs), indicate that phloem loading occurs in SEs
by transmembrane uptake of sucrose directly from the apoplasm.
The sucrose transporters identified so far arise from a single gene family. Some of the newly identified members of
the family are involved in specific functions, such as nutrition of developing seeds or pollen. Physiological and molecular studies show that sucrose transport is highly regulated
at multiple levels of biological organization and in response
to changing sucrose concentrations. Thus, one of the most
exciting topics in the regulation of sucrose transport is signal perception. By analogy to yeast, in which members of
the sugar transport family serve as sugar sensors, we propose that members of the plant sugar transporter family play
a direct role in the signal transduction responsible for regulation of sugar transport and, thus, metabolism in general.
Plant Anatomy: Vascular Tissues
1To
whom correspondence should be addressed. E-mail frommer@
uni-tuebingen.de; fax 49-7071-29-3287.
Nonphotosynthetic tissues and organs, including the entire
below-ground portion of the plant, need to be supplied with
energy and fixed carbon. Sugars, synthesized in the mesophyll cells, serve as the major exported photosynthetic
product. To accommodate long-distance transport of sugars from source (net exporting) to sink (net importing)
organs, a vascular network—the phloem—has evolved in
land plants. The most abundant compound in the phloem
sap of most plant species is the disaccharide sucrose
(Zimmermann and Ziegler, 1975). For a minority of plant
species, the principle translocated sugars fall into two
main groups: the sugar alcohols (mannitol and sorbitol)
and the raffinose series (raffinose, stachyose, and verbascose) (Zamski and Schnaffer, 1996). In most cases in
which such sugars predominate, however, sucrose is also
present.
With the exception of a few well-studied species, our
knowledge of phloem sap composition is limited to crude
analyses (Zimmermann and Ziegler, 1975) derived from
stem incision experiments in which sugars present as storage compounds in stems may contaminate phloem sap
samples. Therefore, accurate and less invasive techniques,
such as in vivo NMR (Köckenberger et al., 1997) or positronemitting tracer imaging system (Hayashi et al., 1997), will be
required for a more accurate understanding of phloem sap
composition.
The phloem of angiosperms consists of several types of
cells that are closely associated with the xylem within the
vascular bundle. The structure and development of the
phloem has been reviewed recently (Sjölund, 1997; Ward et
al., 1998; Oparka and Turgeon, 1999, in this issue). The actual conduits in phloem consist of two ontogenetically related cell types: companion cells (CCs) and SEs. These two
cells are highly modified and well interconnected by plasmodesmata. SEs, for instance, lose their nuclei, vacuoles,
and many other organelles during maturation and form
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tubes of living cells connected by sieve pores. CCs, which
are characterized by dense protoplasm, retain a nucleus and
numerous mitochondria and are thought to provide functions essential for the survival of SEs via plasmodesmatal
links (Lucas et al., 1993).
The complete physical pathway of sucrose transport from
source to sink is not completely elucidated for any plant,
and important differences may exist among species. From
the point of sucrose synthesis in the mesophyll, the route to
the SE involves several cell types: neighboring mesophyll
cells, bundle-sheath cells, phloem parenchyma, and CCs.
Cell-to-cell movement of sucrose is considered to occur via
plasmodesmata from the point of synthesis up to the SE/CC
complex which, in many species, is not well connected to
the surrounding cells (Gamalei, 1989). Two principal routes
for the delivery of sucrose into the SE/CC complex have
been proposed: (1) transporter-mediated export from mesophyll cells, apoplasmic diffusion through the cell-wall continuum, and subsequent carrier-mediated transport across the
SE/CC plasma membrane; and (2) direct symplasmic cellto-cell diffusion via plasmodesmata. The extent to which
plants utilize either of these pathways and whether plants
can switch between these pathways is a question currently
under active investigation.
Symplasmic Transport
Figure 1 also schematizes the possibility that each transport
process outlined above could alternatively take place symplasmically. Based on the systemic movement of plant virus
in phloem, plasmodesmal connections between the SE/CC
complex and surrounding cells are present even in Solanaceous species which are classified as type 2a (van Bel and
Apoplasmic Transport
Plants that primarily utilize an apoplasmic phloem loading
mechanism require the transmembrane transport of sucrose
and other solutes into the phloem. For such plants, as schematized in Figure 1, we can predict a minimum of five sucrose transport activities along the translocation path. In
leaves, the first transport step must be release of sucrose
into the cell wall directly from the mesophyll cell (Figure 1,
transporter 1). Mechanistically, this first transporter could be
a facilitator or an antiporter. Such sucrose efflux systems
have been described biochemically (see Delrot, 1989; Laloi
et al., 1993). Subsequently, at least one transporter is required for uptake into the phloem (Figure 1, transporter 2).
These loading processes are required at various stages of
development, such as during germination for sugar export
from leaves or for mobilization of stored carbon, events that
might require distinct transporters. Reuptake of sucrose
along the translocation pathway is necessary to allow solute
exchange with the phloem, for example, in stems (Figure 1,
transporter 3; Minchin and Thorpe, 1987).
In sink tissue, unloading can occur either by transmembrane export of sucrose (Figure 1, transporter 4) or through
plasmodesmata. Sucrose efflux transporters involved in
phloem unloading have been postulated to function as facilitators or as proton antiporters (Walker et al., 1995). Sucrose
in the apoplast of sink tissue can be taken up directly (Figure
1, transporter 5) or through the hydrolysis of sucrose into
glucose and fructose by invertase followed by hexose uptake (Figure 1, transporter 6).
Figure 1. Long-Distance Sugar Transport by the Phloem.
From its point of synthesis in the mesophyll, sucrose may be loaded
into the SE/CC complex either through plasmodesmata or via the
apoplasm. The apoplasmic loading mechanism requires sucrose export (1) from the mesophyll or the vascular parenchyma and reuptake (2) into the SE/CC complex. Hydrostatic pressure drives
phloem sap movement toward sink tissue. Passive leakage can take
place along the path (indicated by wavy arrows). Reuptake (3) also
occurs along the path of the phloem. Apoplasmic phloem or postphloem unloading necessitates a sucrose exporter at the sink tissue
(4). Import of sucrose and other solutes into sink tissue may occur
through plasmodesmata or sucrose transporters (5). In addition to
plasmodesmal and transporter-mediated uptake, cells in the sink
may take up sucrose, subsequent to its hydrolysis by an apoplasmic
invertase, as hexoses (6). The vacuolar transport system could
consist of a H 1/sucrose antiporter for uptake and a uniporter for
release.
Sugar Transport and Sugar Sensing
Gamalei, 1992). To achieve the pressure difference required
for mass flow, the plasmodesmata must normally be closed.
The systemic spread of silencing signals via the phloem
(Voinnet et al., 1998) indicates that plasmodesmata can be
gated open by endogenous plant factors. Symplasmic
routes have been identified in the root by determination of
dye coupling by using small cytoplasmic fluorescent dyes
(Wright and Oparka, 1997).
Interestingly, despite the presence of plasmodesmata
along the entire length of the transport path, efflux occurs
only in restricted regions, such as the region behind the root
tip. It is possible that plants may utilize different mechanisms of phloem unloading in different tissues or may even
be able to switch between apoplasmic and symplasmic
mechanisms depending on growth conditions. Besides
these plasma membrane transporters, uptake and release
systems are required for subcellular compartments, especially the vacuole, which serves as a transient buffer for sugars and other metabolites (Figure 1; Marty, 1999, in this
issue).
The Physics of Mass Flow
Uptake of sucrose into the SEs is believed to increase the
hydrostatic pressure difference between the ends of the
phloem conduits so as to drive the mass flow movement of
the phloem sap. The velocity of translocation in the phloem
is relatively high, ranging from 0.5 to 3 m hr21 (Köckenberger
et al., 1997). The phloem, then, contains an osmotic pump
whose efficacy rests primarily on the cooperative functions
of three types of plasma membrane proteins: (1) H1/sucrose
symporters that accumulate osmotically active sucrose to
molar concentrations in the phloem; (2) H 1-ATPases that
provide the energy necessary for active transport; and (3)
water transporters, potentially aquaporins, that take up water derived from the xylem (for a discussion of aquaporins,
see Chrispeels et al., 1999, in this issue; for a discussion of
H1-ATPases, see Sze et al., 1999, in this issue). Osmolytes
other than sucrose, such as potassium and amino acids,
also contribute to the driving force of the sap flow, and the
simultaneous withdrawal of osmolytes and water at sink tissues further increases hydrostatic pressure differences. An
essential prerequisite for the resulting osmotic pump is that
the SE/CC complex be osmotically isolated from neighboring cells. Specifically, if phloem cells are connected to
neighboring mesophyll cells, such intercellular connections
must be tightly regulated. Differences in the connectivity
among different cell types in leaves are in fact discernable
and result in the classification of plants as either apoplasmic
or symplasmic loaders (van Bel, 1993). Furthermore, evidence for the regulated opening of plasmodesmata has
been provided (Oparka and Prior, 1992; Oparka et al.,
1994).
Of the numerous components required for long-distance
photoassimilate transport (Figure 1), only proton-coupled
709
sucrose and monosaccharide uptake transporters have
been identified at the molecular level. It is unknown whether
sucrose release is also proton coupled or if the release carriers are related in sequence to the uptake transporters (Ward
et al., 1998). The sucrose binding protein, which in many
cases colocalizes with the sucrose transporter, might be responsible for facilitated diffusion of sucrose (Overvoorde et
al., 1996; Harrington et al., 1997) and may represent a second sucrose transporter class.
SUGAR TRANSPORTERS
Monosaccharide Transporters
Monosaccharide transport activities have also been identified in a variety of plant species (Maynard and Lucas, 1982;
Getz et al., 1987; Gogarten and Bentrup, 1989; Tubbe and
Buckhout, 1992). Substrates that are efficiently transported
include b-D-glucose, 3-O-methyl b-D-glucose, 2-deoxy
b-D-glucose, a-D-mannose, and b-D-fructose, whereas
b-L-glucose and b-D-ribose are poor substrates for transport (Gogarten and Bentrup, 1989). Plant monosaccharide
transporters were first cloned from Chlorella kessleri by
exploiting their rapid induction following the addition of
hexoses to the growth medium. Specifically, differential
screening of cDNAs from autotrophic versus heterotrophic
cells enabled the cloning of the first plant hexose transporter gene (HUP1; Sauer and Tanner, 1989). In contrast to
the yeast hexose transporters (HXTs), which function as
uniporters, the C. kessleri hexose transporter is a symporter (Sauer et al., 1990a; Aoshima et al., 1993). Despite
this difference in the transport mechanism, yeast and C.
kessleri transporter genes are homologous, encoding proteins composed of 12 putative membrane-spanning domains. At least three hexose transporters are known to
exist in C. kessleri (Table 1). The functional proof that these
genes encode hexose transporters derives from heterologous expression of the plant genes in yeast (Sauer et al.,
1990a).
The cloning of higher plant monosaccharide transporters
was accomplished by heterologous hybridization (Sauer et
al., 1990b). The monosaccharide transporter family in Arabidopsis, as shown in Table 1, contains in excess of 26 genes,
and multiple genes have been isolated from other species.
STP1 was characterized by heterologous expression in
Xenopus laevis oocytes and shown to function as a proton
symporter (Aoshima et al., 1993; Boorer et al., 1994). The
expression patterns of various plant monosaccharide transporters suggest that these membrane proteins function in
hexose uptake in sink tissues (Sauer and Stadler, 1993).
Analysis of expression also shows that plant monosaccharide transporters are highly regulated, such as in response
to pathogen infection or after wounding (Truernit et al.,
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The Plant Cell
Table 1. Monosaccharide Transporter Gene Family in Plants
Species
Arabidopsis thaliana
Gene Name
AtSTP1
AtSTP3
AtSTP4
ERD6
AtSUGTRPR
ATAP22.19
Fi8E5.100a
T10M13.6a
T01O24.7a
F3O9
T20F21.7
AtFCA6
F1N21.10
T22H22.15
T4B21.9
T4B21.10
T7A14.10
T30D6.1
MKD15.12a
TACK11J9.5a
T14N5.7a
F7G19.20a
F7G19.23a
F9D12.9a
F9D12.17a
F23E12.140a
Beta vulgaris
BvMST1
BvMST2
BvMST3
Chlorella kessleri
CkHUP1
CkHUP2
CkHUP3
Lycopersicon esculentum LeMST1
Medicago truncatula
MtST1
Nicotiana tabacum
NtMST1
Picea abies
PaMST1
Petunia 3 hybrida
PMT1
Prunus armeniaca
APR MST1
Saccharum subsp
ScfGLUTRAB
Ricinus communis
RcSTC
RcHEX6
RcSTA
Vicia faba
VfHext
Vitis vinifera
VvHEXTRAN
VvHEXOSET
a Amino
Accession Length
Number
(Amino Acids)
X55350
AJ002399
X66857
D89051
Z50752
Z99708
AL022603
AF001308
AC002335
AC006341
AC006068
Z97341
AC002130
AC005388
AF118223
AF118223
AC005322
AC006439
AB007648
AB012239
AB012239
AC000106
AC000106
AF077407
AF077407
AL022604
U64902
U64902
U43629
X55349
X66855
X75440
AJ010942
U38651
X66856
Z83829
AF061106
AF000952
L21753
L08196
L08188
L08197
Z93775
Y09590
AJ001061
522
514
514
496
734
493
508
513
521
518
522
582
453
483
434
442
623
508
514
515
525
454
490
507
526
729
549
545
490
534
540
534
523
518
523
513
510
475
518
523
510
522
516
519
519
acid sequences are deduced from genomic sequence.
1996), thus allowing flexible reallocation of fixed carbon. The
expression of monosaccharide transporters in sink tissue
also supports an apoplasmic mechanism for phloem or
postphloem unloading (Sauer and Stadler, 1993). In this
way, plant sink tissues may acquire hexose in a manner similar to that employed by yeast that use an extracellular
invertase to hydrolyze external sucrose. One requirement
for this mechanism in plants is the coexpression of plant
invertases and monosaccharide transporters (Ehness and
Roitsch, 1997).
The sugar permease family in yeast contains 34 genes
(André, 1995; Nelissen et al., 1997; reviewed in Boles and
Hollenberg, 1997), with 20 members belonging to the HXT
subfamily (HXT1-17, GAL2, SNF3, and RGT2). The individual
HXTs differ considerably with respect to their kinetic properties, with Km values for glucose uptake ranging from 1 mM for
HXT7 to 100 mM for HXT1 (Reifenberger et al., 1997). The expression of HXT genes is regulated by glucose concentration, and the transporter homologs SNF3 and RGT2 function
as sensors (see below).
Sucrose Transporters and SUT Genes
Sucrose transport activities have been described in a wide
variety of systems (Maynard and Lucas, 1982; Giaquinta,
1983; reviewed in Bush, 1993; Ward et al., 1998). To clone
plant sucrose transporters, a yeast strain was generated
that was unable to hydrolyze extracellular sucrose but was
capable of metabolizing internal sucrose due to the presence of a plant-derived sucrose synthase activity (Figure
2). The strain was, furthermore, deficient in maltose utilization, a safeguard against side activities of the yeastendogenous maltose transport systems. The resulting
yeast cells grow inefficiently on media containing 0.5%
sucrose as the sole carbon source and were consequently
used to clone plant sucrose transporters from spinach and
potato by functional complementation (Riesmeier et al.,
1992, 1993).
Detailed transport studies using radioactive tracers have
subsequently allowed determination of kinetic properties,
pH optima, inhibitor sensitivity, and substrate specificity of
various SUT genes. All plant sucrose transporters identified
so far are energy dependent and sensitive to protonophores, indicating that they function as proton symporters.
The Km for sucrose, in all cases, was found to be in the
range of 1 mM (Riesmeier et al., 1993; Lemoine et al., 1996).
Similar results were obtained for the Arabidopsis sucrose
transporters SUC1 and SUC2.
The SUT genes encode highly hydrophobic proteins. They
consist of 12 membrane-spanning domains and are distantly related to the hexose transporter family found in many
organisms, such as yeast and plants (reviewed in Ward et
al., 1997; Rentsch et al., 1998). As for the monosaccharide
transporters, sucrose transporters have been characterized
by the two-electrode voltage clamp method in X. laevis oocytes (Boorer et al., 1996; Zhou et al., 1997). The stoichiometry of H1/sucrose cotransport was determined to be 1:1,
consistent with stoichiometric estimates obtained earlier in
plasma membrane vesicles from sugar beet leaves (Bush,
1990; Slone et al., 1991). The SUT family thus corresponds
to the protonophore-sensitive high-affinity component of
Sugar Transport and Sugar Sensing
711
Figure 2. A Yeast System for Functional Cloning of Sucrose Transporters.
Wild-type yeast (Saccharomyces cerevisiae) utilizes sucrose primarily through activities of an extracellular invertase and hexose transporters in
the plasma membrane (left). A yeast strain (SUSY7; Riesmeier et al., 1992) was constructed in which the cytosolic and extracellular invertases
were genetically knocked out (middle). A plant sucrose synthase expressed in the cytosol allows growth on sucrose as the sole carbon source
only if a sucrose transporter is expressed in the plasma membrane (right). The ability (1) or inability (2) of the yeast strains to grow on sucrose or
glucose is shown. fruc, fructose; gluc, glucose; INV, invertase; suc, sucrose; SUC2, invertase gene; SUSY, sucrose synthase; SUT1, sucrose
transporter 1 gene.
sucrose-uptake kinetics measured in plants (Maynard and
Lucas, 1982).
CELLULAR LOCALIZATION OF SUT1 IN THE PHLOEM:
CCs AND SEs
Based on the transport mechanism (H1 symport) of SUT1, it
was expected that the transporter would be involved in
phloem loading and thus should be present at the plasma
membrane of SE/CC complexes. In situ hybridization indeed
demonstrates that SUT1 transcripts are phloem associated
(Riesmeier et al., 1993), and the promoters of tomato SUT1
and Arabidopsis SUC2 genes direct the expression of reporter genes in leaf, stem, and root phloem (Truernit and
Sauer, 1995; A. Weise, B. Hirner, J.M. Ward, and W.B.
Frommer, unpublished results). Hence, SUT1 (or SUC2 from
Arabidopsis) might play a role not only in phloem loading but
also in retrieval of sucrose leaking from sieve tubes along the
translocation pathway (Figure 1, transporter 3).
To determine expression at the cellular level, immunolocalization studies have been applied to five species. In Plantago
major and Arabidopsis, immunofluorescence with specific
antibodies detects SUC2 in CCs (Stadler et al., 1995; Stadler
and Sauer, 1996). By contrast, immunolocalization using immunofluorescence and silver-enhanced immunogold staining assign SUT1 to the plasma membranes of enucleate SEs
of tobacco, potato, and tomato (Kühn et al., 1997). The differences in sucrose transporter localization observed in Arabidopsis and P. major compared with tomato, potato, and
tobacco may be due to differences in loading mechanisms.
However, the transporters studied in Arabidopsis and P.
major do not appear to be orthologs of SUT1, which may remain to be identified in those species. This would be consistent with a stepwise manner of sucrose loading, whereby
different carriers operate in CCs (SUC2) as opposed to SEs
(SUT1); such a scenario is suggested by physiological analyses (Roeckl, 1949).
In situ hybridization experiments at the electron microscope level corroborate the localization of SUT proteins to
SEs in a remarkable manner. Specifically, Solanaceous
SUT1 mRNA localizes mainly to SEs, primarily at the orifices
of plasmodesmata (Kühn et al., 1997). In addition, antisense
inhibition of SUT1 expression using a CC-specific promoter
(from the RolC gene) produces strong phenotypic effects
in transgenic plants due to inhibition of sucrose export
from leaves (Kühn et al., 1996). These results indicate that
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transcription of the SUT1 gene occurs in CCs and, in conjunction with high turnover rates of mRNA and protein, provide strong evidence for targeting of plant endogenous
mRNA, and potentially SUT1 protein, through the plasmodesmata that interconnect CCs and SEs.
These data may seem surprising at first sight; however,
trafficking of RNA is known to occur in Drosophila and X.
laevis during oogenesis and in neurons (St. Johnston, 1995).
In maize, moreover, mRNA and protein produced from the
KNOTTED-1 gene are transported through plasmodesmata
in apical meristems (Lucas et al., 1995). Similarly, microinjection studies in Cucurbita maxima suggest that an RNA
binding protein identified in phloem sap of that species is
capable of trafficking a number of mRNAs intercellularly, including the SUT1 mRNA (Xoconostle-Càzares et al., 1999).
The transport of macromolecules such as mRNAs and proteins through the microchannels of plasmodesmata requires
mechanisms of unfolding (Kragler et al., 1998; see also
Lazarowitz and Beachy, 1999, in this issue). The function of
plasmodesmata thus seems, in this respect and many others, to be highly similar to protein import into organelles
such as plastids (see Keegstra and Cline, 1999, in this issue), mitochondria, and the endoplasmic reticulum lumen
(Vitale and Denecke, 1999, in this issue).
As schematized in Figure 3, two potential pathways for
the targeting of SUT1 can be postulated: either (1) mRNA is
guided as part of a nucleoprotein complex along the cytoskeleton through the phloem plasmodesmata for subsequent translation; or (2) translation is effected in the CCs and
the protein is deposited within the SE at the plasmodesmatal orifices via the endomembrane system (Overall and
Blackman, 1996).
Other phloem proteins alter the size exclusion limit for
plasmodesmata and have been shown to move from cell to
cell (Balachandran et al., 1997; Ishiwatari et al., 1998; see
Lazarowitz and Beachy,1999, in this issue). Various proteins
have been identified in the phloem sap, some of which were
found to be specific for SEs, namely, b-amylase, glutaredoxin, thioredoxin, cyclophilin, protein kinases, ubiquitin,
and P-protein PP2a (Schobert et al., 1995; Wang et al.,
1995; Sjölund, 1997; Szederkényi et al., 1997). The role of
most of these proteins in the phloem is unknown, and their
origins and biosynthesis are not fully understood. The stability of proteins in the phloem also is generally unknown. The
presence of ubiquitin in phloem sap may indicate that protein turnover is occurring. Further research is needed to determine both protein turnover rates in the phloem sap and
protein import rates.
Mature SEs are living cells despite the fact that they lack
a nucleus and many other organelles (Sjölund, 1997). SEs
are thought to be dependent on CCs for many cellular
functions, but the extent of this dependence cannot be
determined until the actual metabolic capabilities of SEs
are better understood. For example, it is not clear whether
SEs contain plasma membrane proton pumps. In CCs, on
the other hand, the expression of the H 1-ATPase–encoding AtAHA3 gene has been demonstrated (DeWitt and
Sussman, 1995; see Sze et al., 1999, in this issue). If SEs
do in fact contain an H 1-ATPase, then the supply of ATP
to SEs through plasmodesmata would be presumably important. Consistent with this, phloem sap has been shown
to contain concentrations of ATP in the range of 1 mM
(Kluge et al., 1970). Additionally, the biogenesis of any
ATPase in SEs may be dependent on a supply of mRNA or
protein from CCs, by analogy to SUT1 biogenesis (Kühn et
al., 1997). On the other hand, if SEs do not contain a proton pump or if the proton motive force to drive phloem
loading is generated only in CCs, then plasmodesmatal
connections are important for the propagation of this driving force (for both electrical coupling and a pathway for
protons) into SEs (van Bel, 1996). In addition, trafficking of
proteins, nucleic acids, and other molecules through plasmodesmata connecting CCs and SEs is important for
Figure 3. SUT1 Biosynthesis.
In Solanaceous species, SUT1 protein is located in the SE plasma
membrane (PM), while transcription occurs in CCs. There are two
possible pathways: SUT1 mRNA may be delivered through plasmodesmata (pd) by an RNA transport mechanism. Alternatively,
SUT1 translation may take place in CCs and delivery to SEs may occur via the plasma membrane or endosomal membranes that are
continuous through plasmodesmata. These pathways are not exclusive and could function in parallel. ER, endoplasmic reticulum; sER,
sieve element reticulum.
Sugar Transport and Sugar Sensing
long-distance signaling and to coordinate development at
the whole-plant level in response to environmental factors,
nutrients, and water availability (reviewed in Mezitt and
Lucas, 1996).
IN VIVO EVIDENCE OF SUT1 TRANSPORTER FUNCTION
If sucrose transport mediated by SUT1 is essential for
phloem loading, a reduction in transport activity should affect carbon partitioning and photosynthesis. In SUT1 antisense plants (Riesmeier et al., 1994; Kühn et al., 1996), leaf
sucrose and starch content is five- to 10-fold higher than in
the wild type, and the increase in hexose content is even
greater. In addition, SUT1 antisense plants grow at markedly
retarded rates, producing crinkled leaves that exhibit chlorosis and accumulation of anthocyanins. Development of the
phenotype depends on the length of the photoperiod and
light intensity (Kühn et al., 1996).
A similar accumulation of soluble carbohydrates occurs
when petioles of potato leaves are cold girdled so as to
block phloem translocation (Krapp et al., 1993). Enhanced
partitioning into insoluble carbohydrates is also found in a
number of studies in which heat girdling is used (Grusak et
al., 1990, and references therein). A direct comparison of
antisense repression and cold girdling at the ultrastructural
level demonstrates that both treatments equally evoke the
accumulation of assimilates in all leaf tissues up to the
SE/CC complex. However, microscopy reveals that antisense inhibition of loading produces a persistently high
sugar level throughout the leaf, whereas cold girdling leads
to localized patches containing high sugar and lipid levels
(Schulz et al., 1998).
Efflux measurements of carbohydrates from excised
leaves of antisense plants show strong reduction in phloem
transport (Riesmeier et al., 1994). With less carbohydrate
transport to sinks, the plants have reduced root growth and
tuber yield, phenotypic qualities also observed in transgenic
potato plants in which apoplasmic loading is prevented by
the overexpression of a yeast invertase in cell walls of leaves
(Heinecke et al., 1992; Riesmeier et al., 1994). In tobacco,
antisense repression of SUT1 also leads to dramatic growth
retardation and accumulation of carbohydrates in leaves
(Bürkle et al., 1998). The export of recently fixed 14CO2 is
blocked to almost nondetectable levels even in plants inhibited to an intermediate degree, and stronger inhibition was
found to be lethal. Thus, proton-coupled carriers seem to be
indispensable for phloem loading at least in Solanaceous
species.
Comparable effects were observed in potato plants in
which SUT1 was expressed in antisense orientation under
control of the CC-specific RolC promoter (Kühn et al., 1996).
It was, however, not possible to estimate the control coefficient of SUT1 because the actual amount of SUT1 protein
713
and sucrose transport activity in the phloem was masked by
low levels of SUT1 expression presumably in mesophyll
cells (Lemoine et al., 1996). The effects observed are therefore in agreement with expected results that SUT1 transcription in CCs is essential for phloem loading.
It remains unclear whether antisense repression also affects other members of the SUT gene family. A complete
analysis of the role of individual members of the gene family
will require approaches such as the use of “knockout” mutants in Arabidopsis. The potential of this approach for
studying transport has been elegantly demonstrated in the
case of potassium channels (Krysan et al., 1996; Gaymard
et al., 1998; Hirsch et al., 1998; see also Chrispeels et al.,
1999, in this issue). Identification of “knockout” mutants in
sugar transport is in progress in several research laboratories.
SUCROSE TRANSPORTERS IN PHLOEM AND
POST-PHLOEM UNLOADING
As detailed above, sucrose and hexoses have to be imported into sink tissues in roots, pollen, seeds, and elsewhere. SUT1/SUC2 expression has indeed been found in
these tissues (Riesmeier et al., 1993; Truernit and Sauer,
1995). However, the direct function of such phloem-associated H1/sucrose symporters in sink tissues remains unclear. In several plant species, such as tomato, tobacco,
potato, Arabidopsis, P. major, Ricinus communis, Vicia
faba, carrot, rice, and pea, additional sucrose transporter
genes have been identified, as listed in Table 2 (Gahrtz et
al., 1994, 1996; Sauer and Stolz, 1994; Harrington et al.,
1997; Hirose et al., 1997; Bürkle et al., 1998; Shakya and
Sturm, 1998; Tegeder et al., 1999). Several of these genes/
proteins show highly specific expression patterns. For example, in Plantago, SUC1 is expressed in young ovules
(Gahrtz et al., 1996), and sucrose transporter transcripts
can be detected in the transfer cells of cotyledons from Vicia seeds and pea (Table 2; Harrington et al., 1997; Weber
et al., 1997; Tegeder et al., 1999). Interestingly, these carriers are also expressed in source leaves, indicating a dual
function in both phloem loading in leaves and in seed import.
Other members of the SUT family are required in unloading zones, such as pollen, ovules, and roots. A pollenspecific sucrose transporter has been identified in tobacco
(R. Lemoine, L. Barker, L. Bürkle, C. Kühn, M. Regnacq, C.
Gaillard, S. Delrot, and W.B. Frommer, unpublished data).
Within sink tissues, sucrose transporters could function in
direct transport into sink cells or in sucrose retrieval. This
latter function could control sink strength. Osmotic regulation, especially that involved in regulation of phloem or postphloem unloading, has been discussed in detail by Patrick
(1997). Carriers in source tissue for efflux from mesophyll,
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The Plant Cell
Table 2. Sucrose Transporter Gene Family in Plants
Species
Gene Name
Accession Number
Length (Amino Acids)
Localizationa
Arabidopsis thaliana
AtSUC1
AtSUC2
AtSUT2
AtSUT4
AtSUT5
AtSUT8
BvSUT1
DcSUT1a
DcSUT1b
DcSUT2
LeSUT1
X75365
X75382
AC004138
AC000132
AB016875
AC005398
X83850
Y16766
Y16767
Y16768
X82275
513
512
594
511
492
493
523
501
501
515
510
SoL, SiL, Ro, Flb, phloemc
SoL, SiL, Flb, CCs
NtSUT1
OsSUT1
X82276
D87819
507
537
Pisum sativum
PsSUT1
AF009922
524
Plantago major
PmSUC1
X84379
503
Solanum tuberosum
PmSUC2
StSUT1
X75764
X69165
510
516
Spinacea oleracea
Ricinus communis
Vicia faba
SoLSUT1
RcRSC1
VfSUT1
X67125
Z31561
Z93774
525
533
523
Beta vulgaris
Daucus carota
Lycopersicon
esculentum
Nicotiana tabacum
Oryza sativa
SoL, Stb
St, TP, Fl, Stb
CCs,b SEb,d, phloemc
SoL, Ro, St, SiL, Flb
Pa, LS, LBb
Sp, E, Rab
Fl, SoL, Ro, St, Sb
TC, Sp, SCb, TCe, Spe
Fl, V, Fl, St, SiL, SoL, Rob
Young ovulese, CCd
SoL, St, Ro, Fl, SiL, Frb, CCd
SoL, Ro, Flb
Phloemc, abaxial phloeme
SoLb
C, Ro, Hb, E, SiL, SoLb
C, SC, Po, SoL, Ro, SiLb, TCe
aC,
cotyledon; CC, companion cell; E, endosperm; Fl, flower; Fr, fruit; H, hypocotyl; LB, leaf blade; LS, leaf sheath; Pa, panicle; Po, pod; Ra, rachis; Ro, root; S, seed, SC, seed coat; SE, sieve element; SiL, sink leaf; SoL, source leaf; Sp, spikelet; St, stem; TC, transfer cell; TP, tap root; V,
vascular bundle. Expression of mRNA or localization has been demonstrated using several techniques:
bRNA gel blot analysis.
cPromoter–b-glucuronidase fusion.
dImmunolocalization.
eIn situ hybridization.
carriers in sink tissues for efflux from phloem and postphloem, and carriers involved in transient storage in vacuoles have yet to be identified (Figure 1).
SENSING MECHANISMS IN SUGAR TRANSPORT
A common misconception is that transport processes, especially sugar transport in higher plants, are constitutive and
that biosynthetic activities in the source and catabolic activities in the sink are the key factors controlling allocation of
carbohydrates. Carbohydrate export rate is increased 10-fold
in plants overexpressing pyruvate decarboxylase (Tadege et
al., 1998), indicating a large potential for upregulation.
Transporters, however, are located in strategic positions
along metabolic pathways, and thus an effective regulatory
mechanism would be to control uptake and efflux directly.
Indeed, there is strong evidence that sugar transport regulates the distribution of assimilates within the plant through
various macromolecular signaling events.
In the simplest sensing scenario, cells would contain only
an intracellular receptor for a sugar metabolite. Such cells,
whether located in source or sink tissues, could modulate
metabolic processes, such as photosynthesis or carrier
gene expression. However, due to intracellular metabolism,
the effector cells involved in these processes must be able
to differentiate between biosynthesis and transport, and
therefore both intra- and extracellular concentrations of sugars need to be sensed. Furthermore, provided that the cell
has a spectrum of carriers of varying affinity and capacity for
sugar, extracellular sensors, as shown in Figure 4, can adjust sugar uptake to match requirements, for example, by
inducing high-affinity uptake systems at low external concentration.
In principle, multiple sensors could be utilized, some for
Sugar Transport and Sugar Sensing
715
high-affinity responses and others for adaptation to highflux requirements. Because the plasma membrane has a
limited capacity for protein content, this signal may at the
same time lead to an increase in the turnover of low-affinity
systems. Increased turnover of transporters can also be
controlled via an internal sensor, thus decreasing import if
intracellular concentrations exceed the requirements.
Although such regulatory networks could also be effective
in unicellular organisms like yeast or algae, intercellular
transport in higher plants is more complicated. This is because at least two cellular activities—export from one cell
and import into the adjacent cell—have to be integrated. Little is known about the molecular mechanisms involved in
sugar sensing in relation to transport in higher plants. Yeast
could thus serve as a model to help uncover the regulatory
networks in higher plants.
YEAST AS A MODEL OF SUGAR SIGNALING
The yeast Saccharomyces cerevisiae contains a large spectrum of .200 integral membrane proteins, many of which
Figure 5. Sugar Signal Transduction in Saccharomyces cerevisiae.
HXT-type transporters mediate glucose uptake. Hexokinase PII
(HXK2) functions in cytosolic sugar signaling, resulting in transcriptional regulation of enzymes and transporters necessary for sugar
utilization. The SNF3 (high affinity) and RGT2 (low affinity) glucose
receptors sense the external glucose concentration. These are homologous to HXT-type transporters but contain a C-terminal extension that functions in signaling. The SNF3 and RGT2 signaling
pathways affect transcriptional regulation of high-affinity and lowaffinity/high-capacity hexose transporter genes, respectively. See
text for details.
Figure 4. Model for Metabolite Sensing by a Combination of Internal and Membrane-Bound Receptors.
In addition to an internal receptor (see text), membrane-bound receptors are used to sense external sugar concentrations. Such sensors trigger a signaling cascade regulating transporter biogenesis
and insertion or degradation of proteins at the plasma membrane. In
this scenario, low sugar concentrations activate a sensor to induce
sugar transporter genes (preferentially high affinity). This enables
more efficient sugar uptake. If, on the other hand, internal sugar
concentration becomes too high, the intracellular sensor may either
repress transporter transcription or trigger inactivation via endocytosis and degradation of the transporter, thus reducing the influx. Induction of low-affinity/high-capacity transporters could increase
uptake at higher external concentrations.
are clearly involved in transmembrane solute transport. For
example, yeast contains .20 permeases for amino acid
transport (André, 1995; Nelissen et al., 1997) and .20 permeases for sugar transport (André, 1995; Boles and
Hollenberg, 1997). The redundancy of transport systems
suggests that complex regulatory networks are absolutely
necessary to control the uptake of nutrients in response to a
rapidly changing external environment. As shown in Figure
5, yeast has developed a two-pronged regulatory system to
ensure coordination between the supply of sugars from the
environment and the enzymatic machinery of the cells: (1)
the extracellular concentration of sugars is sensed and
sugar transport activity is regulated accordingly; (2) sugar
transport activity determines the flux of sugars into the cell,
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The Plant Cell
subsequently generating intracellular signals for further
regulatory processes.
In S. cerevisiae, multiple transport systems for glucose are
regulated at the transcriptional level in response to the external concentration of glucose. For example, HXT2 and
HXT7 serve as high-affinity glucose transporters and are induced only by low levels of glucose but repressed at high
levels, whereas HXT1 functions as a low-affinity transporter
and is induced only by high concentrations of glucose
(Özcan and Johnston, 1995; Boles and Hollenberg, 1997).
Consequently, sensors of extracellular glucose that respond
not only to the kind of carbon source in the medium but also
to its concentration are required. Once inside the cell, glucose
is phosphorylated by three different kinases: HXK1, HXK2,
and GLK1. Finally, it is converted through the glycolytic
pathway mainly into ethanol. By contrast to the uptake of
glucose, the regulation of the intracellular glucose concentration, phosphorylation, and subsequently, the regulation of
flux through glycolysis must be controlled by intracellular
signals (Boles et al., 1997). Furthermore, the expression of
genes for the utilization of alternative carbon sources like sucrose or galactose, and genes involved in gluconeogenesis,
must be shut off in the presence of sufficient amounts of the
preferred carbon source, glucose. This is achieved through
a mechanism known as glucose (or carbon) catabolite repression (Ronne, 1995; Gancedo, 1998).
The glucose signal that triggers induction of hexose transporter genes is generated by the hexose sensors SNF3 and
RGT2. On the other hand, the signal that triggers glucose repression is somehow connected to the kinase activity of
HXK2 (Ma et al., 1989; Rose et al., 1991). In principle, there
are two possibilities for sensory proteins to detect signaling
molecules. First, sensors might act as receptors, binding the
triggering molecule (e.g., glucose) and transducing the signal via other proteins. Second, sensors might behave like
enzymes or transporters and undergo structural changes so
as to monitor the presence or absence of the triggering
compound directly. Flux measurements by such a sensor
protein would involve the recognition of the velocity of the
enzymatic reaction as the ratio of active to free enzyme.
SUGAR SENSORS: A NEW PERSPECTIVE
OF TRANSPORTERS
Cell Surface Sugar Sensors
In Escherichia coli, it has long been known that glucose
sensing is mediated through glucose phosphorylation during transport by the phosphotransferase system (Postma et
al., 1993). However, no related proteins have yet been detected at the plasma membrane of eukaryotic cells. Glucose
sensing in yeast seems to involve plasma membrane proteins that resemble glucose transporters but additionally
possess large cytoplasmic signaling domains (Özcan et al.,
1996a). A similar mechanism has been discovered recently
for amino acid sensing (Didion et al., 1998; Iraqui et al.,
1999) and might be a general phenomenon not restricted to
yeast.
In yeast, SNF3 appears to be a sensor of low levels of glucose and mainly regulates expression of high-affinity glucose transporters, whereas RGT2 appears to be a sensor of
high glucose concentrations that regulates expression of
low-affinity glucose transporters. Additionally, SNF3 is required at high levels of glucose for repression of the
high-affinity transporters HXT2, HXT6, and HXT7 (Liang and
Gaber, 1996; Vagnoli et al., 1998). Dominant mutations in
both RGT2 and SNF3 that lead to the generation of signals
in the absence of glucose have been identified (Özcan et al.,
1996a). Despite the homology of SNF3 and RGT2 to glucose
permeases, these transmembrane proteins do not seem to
be able to mediate significant glucose transport (Liang and
Gaber, 1996; Özcan et al., 1998). The large C-terminal extension of SNF3 (303 amino acids) contains two nearly identical repeats of 25 amino acids. One of these repeats is also
present in the 218–amino acid C-terminal extension of RGT2
and in RAG4 (GenBank accession number Y14849) from
Kluyveromyces lactis, which contains a 250–amino acid
C-terminal extension and controls the expression of the lowaffinity glucose transporter RAG1 (Chen et al., 1992). In
Neurospora crassa, the glucose sensor RCO3 contains a
119–amino acid C-terminal extension that is dissimilar to
that of SNF3, RGT2, and RAG4 (Madi et al., 1997).
From mutational analyses, yeast glucose sensors appear
to function as two interacting domains (Özcan et al., 1998;
Vagnoli et al., 1998): the C-terminal extensions that are required for the transmission of the glucose signal, and the
membrane-spanning domain necessary for glucose recognition. Because the glucose transporters HXT1 and HXT2 can
be converted into glucose sensors by fusion to the SNF3 C
terminus, it is tempting to speculate that the glucose sensors act as glucose transporters with a very low glucose
transport capacity (i.e., too low to support growth of mutants that lack glucose transporters), which transduce the
glucose signal by a conformational shift during glucose
transport.
Another protein (SSY1) that appears to function as an
amino acid sensor has recently been identified in yeast.
SSY1 shows the features typical of the SNF3/RGT2 pair: a
transmembrane domain related to amino acid permeases, a
long cytoplasmic extension (in this case located at the N terminus of the protein), a low transcription rate, and a low
coding probability (André, 1995; Didion et al., 1998; Iraqui et
al., 1999). SSY1, rather than being a transporter, controls
the transcription of genes encoding amino acid permeases
and seems to respond to changes in the extracellular concentration of various amino acids (Didion et al., 1998; Iraqui
et al., 1999). The amino acid sequence of the cytoplasmic
extension of SSY1 shows no significant similarities to those
of SNF3 and RGT2.
Sugar Transport and Sugar Sensing
The only intermediate components so far known to be involved in glucose-induced signal transduction in yeast are
the transcription factor RGT1 (Özcan et al., 1996a) and
SCFGrr1, a ubiquitin protein ligase complex including the
F-box protein GRR1, SKP1, and CDC53 (Li and Johnston,
1997; Skowyra et al., 1997). RGT1 is a zinc cluster protein
that binds directly to promoters of the HXT genes (Özcan et
al., 1996b). It acts as a repressor of HXT genes in cells
growing without glucose and as a transcriptional activator of
HXT1 in cells growing on high levels of glucose. Repression
of transcription by RGT1 is mediated by the SSN6-TUP1
complex, whereas RGT1-mediated induction is independent
of these proteins (Figure 5).
The SCFGrr1 protein complex is required for regulation of
RGT1 activity (Özcan and Johnston, 1995) mediating the
signal generated by SNF3 to inhibit the RGT1 repressor
function in response to low levels of glucose. It is also required for conversion of RGT1 into an activator triggered by
RGT2 in the presence of high levels of glucose. Ubiquitination of RGT1 or its regulator may target it for protein degradation by the proteasome or directly affect its function.
SCFGrr1 complex may be directly stimulated by glucose (Li
and Johnston, 1997) or may depend on glucose-activated
kinase because target proteins must be phosphorylated to
interact with GRR1 (Skowyra et al., 1997).
A third sensor protein, MEP2, was recently found in S.
cerevisiae to be required for pseudohyphal differentiation in
response to ammonium limitation (Lorenz and Heitman,
1998). Under such conditions, diploid yeast cells differentiate into a filamentous, pseudohyphal growth form. MEP2
belongs to a family of three closely related ammonium permeases (Marini et al., 1997). However, unlike the other two
members of this transporter family, MEP2 serves as both an
ammonium transporter and a component of an ammonium
sensor. mep2 mutant strains have no defects in growth
rates or ammonium uptake, but no longer form pseudohyphal filaments on media containing limiting amounts of ammonium. Unlike the glucose sensor proteins, however,
MEP2 is able to transport its substrate; and as compared
with the other members of the ammonium permease family,
MEP2 contains no significant amino acid extensions on either its N or C terminus.
717
of glucose and is dependent on protein phosphatase 1
(CID1/GLC7). A protein kinase involved in phosphorylation
of HXK2 has not been found, and it is possible that phosphorylation of HXK2 could result from substrate-induced
autophosphorylation (Fernández et al., 1988). It has been reported that HXK2 has a weak protein kinase activity (Herrero
et al., 1989; see above). Moreover, a hxk2 mutant that is not
able to undergo phosphorylation can no longer transduce
the glucose repression signal (Randez-Gil et al., 1998).
These properties might classify HXK2 as an enzyme that additionally, through its enzymatic function, can act as a sensor protein. However, the actual mechanism representing
the on–off switch of the glucose signal is not understood.
The glucose repression signal finally inhibits the protein kinase SNF1/CAT1, a central element in the regulatory process (Figure 5) and highly conserved in eukaryotes. Glucose
inhibition of SNF1 depends on protein phosphatase 1
(GLC7) and its targeting subunit REG1 (Ludin et al., 1998). In
the absence of glucose, SNF1 relieves repression by the
MIG-SSN6-TUP1 complexes (De Vit et al., 1997) but is also
required for the operation of other transcription factors
(Gancedo, 1998).
In accordance with HXK2 being a sensor for glucose, the
triggering of glucose repression in yeast is dependent on
glucose uptake. However, the repression is not dependent
on a specific hexose transporter protein; the glucose repression signal rather correlates with the extent of glucose influx
into cells (Reifenberger et al., 1997). These observations fit
very well with the two-pronged regulatory model described
above: first, glucose transport activity is adjusted to the
extracellular glucose concentration via SNF3 and RGT2;
second, glucose transport activity limits provision of intracellular glucose, which then might act as a substrate for
HXK2 as well as a global glucose signal (Figure 5). In addition, cross-talk between the two different processes might
ensure feedback coordination. Such a function has recently
been assigned to HXK2 which, in addition to carbon catabolite repression, seems also to be involved in glucose induction of HXT gene expression (Randez-Gil et al., 1998).
SUGAR-MEDIATED REGULATION OF SINK AND
SOURCE GENES
Intracellular Sugar Sensing: Enzymes as Sensors
In the triggering reaction of glucose repression in yeast,
HXK2 seems to play an important and probably more direct
role. Mutations in HXK2 abolish glucose repression of invertase and other glucose-repressed genes (Entian, 1980). The
catalytic and regulatory functions of HXK2 are inseparable
from glucose repression and inversely correlated to its
sugar-phosphorylating activity (Ma et al., 1989; Rose et al.,
1991). HXK2 exists in a dimeric–monomeric equilibrium that
is affected by phosphorylation (Randez-Gil et al., 1998). In
vivo, dephosphorylation of HXK2 is promoted upon addition
A large spectrum of genes is regulated by sucrose and
monosaccharides (reviewed in Thomas and Rodriguez, 1994;
Koch, 1996). The interplay of regulatory processes interconnected with sugar regulation provides the plant with valuable mechanisms to adjust to environmental conditions and
also to control developmental and physiological processes
(e.g., photosynthesis and flowering) (Bernier et al., 1993;
Jang and Sheen, 1994; Corbesier et al., 1998). Carbohydrate-responsive genes can be classified as initiating “feast
or famine” responses. Genes for photosynthesis and resource mobilization are induced by carbohydrate depletion
718
The Plant Cell
(the famine response), whereas increasing sugar concentrations stimulate gene expression for utilization and storage
(the feast response) independently of location (i.e., in source
or sink tissues) (Rocha-Sosa et al., 1989; Müller-Röber et al.,
1990; Sheen, 1990; Graham et al., 1994; Jang and Sheen,
1994; Thomas and Rodriguez, 1994; Koch, 1996).
Sucrose, as the principal transport form of sugars, can
specifically control the expression of a number of genes.
Examples of sucrose-regulated genes include an Arabidopsis leucine zipper gene, ATB2, and the RolC promoter from
Agrobacterium (Smeekens and Rook, 1997; Yokohama et
al., 1997). Externally supplied sucrose exceeding concentrations of 25 mM lead to a repression of ATB2 transcription
(Rook et al., 1998). In sugar beet, high sugar concentrations
lead to a repression of sucrose transport activity, correlating
with a reduction in steady state mRNA levels of BvSUT1
(Chiou and Bush, 1998); glucose and fructose affect transport activity to a lesser extent. Sucrose can repress transcription of photosynthetic genes encoding, for example,
chlorophyll a/b binding protein (CAB), ribulose-1,5-bisphosphate carboxylase/oxygenase (Rubisco), and plastocyanin.
Sucrose-uncoupled (sun) mutants have been identified, in
which sucrose concentration is uncoupled from the repression of such genes (Dijkwel et al., 1996, 1997). Taken together, these studies indicate the presence of sucrosespecific signal perception and transduction processes in
which both internal and external sensors might be involved.
Glucose-specific responses have also been described
(Thomas and Rodriguez, 1994; Koch, 1996). Moreover, glucose and sucrose seem to control different pathways.
Whereas glucose favors cell division, sucrose relates to
storage compound accumulation in seeds (Weber et al.,
1998).
A specific hexose-sensing system in which hexokinase
plays a central role, potentially as an intracellular sensor,
has been identified in the repression of typical “famine”
genes (Figure 6; Sheen, 1990; Graham et al., 1994; Jang and
Sheen, 1994). Specifically, nonmetabolizable glucose analogs (e.g., 6-deoxyglucose or 3-O-methylglucose) that are
taken up into cells but are not metabolized by hexokinase
do not repress gene induction in photosynthetic or glyoxylate cycles. Only substrates of hexokinase that are taken
up and phosphorylated mimic glucose-specific repression
(Graham et al., 1994; Jang and Sheen, 1994). Additionally,
phosphorylated hexoses do not alter gene expression, but
inhibition of hexokinase blocks the 2-deoxyglucose– and
mannose-dependent repression.
Thus, hexokinase activity per se is involved in sensing, a
finding that is further strengthened by studies of transgenic
Arabidopsis plants in which the expression of the hexokinase-encoding genes AtHXK1 and AtHXK2 had been
prevented (Jang et al., 1997). In antisense plants, the glucose-dependent repression of typical famine genes, such as
Rubisco and CAB, is impaired, thereby leading to reduced
sensitivity to high external glucose concentrations. Interestingly, Arabidopsis plants overexpressing a yeast HXK gene,
thus bypassing sugar flux through the plant’s endogenous
hexokinases, behave similarly to the AtHXK antisense plants
(Jang et al., 1997).
These data support a direct role for hexokinase itself in
signaling in addition to its kinase activity. However, the situation seems to be more complex. Transgenic tobacco
plants overexpressing a yeast invertase in the cytosol, apoplasm, or vacuole all accumulate elevated levels of hexoses.
However, only in plants with apoplasmic or vacuolar invertase expression was gene expression repressed by the elevated sugar content (Herbers et al., 1996). Furthermore,
because the introduction of sugar phosphates into cells by
electroporation does not modify the expression of carbohydrate-responsive genes (Jang and Sheen, 1994), it seems to
be the flux of sugars undergoing phosphorylation that is
sensed rather than the mere internal concentration of sugar
phosphates.
A more recently identified hexokinase-independent glucose-signaling system, schematized in Figure 6, seems to
be preferentially responsible for controlling “feast” and
pathogen-related gene expression. In photoautotrophic
Chenopodium rubrum cell suspensions, the expression of
invertase and sucrose synthase genes is induced upon
treatment with 6-deoxyglucose (Godt et al., 1995; Roitsch et
al., 1995). In transgenic Arabidopsis, 3-O-methylglucose activates a patatin class I promoter fused to b-glucuronidase,
which suggests that the sensing mechanism for this nonphosphorylatable analog occurs before hexokinase in the
signaling pathway.
Martin et al. (1997) have identified several Arabidopsis
mutants with reduced sugar response (rsr) that harbor a
patatin promoter–b-glucuronidase construct. These mutants, in which the patatin promoter does not respond to
sugars, offer a good model for studying hexokinase-independent sugar sensing. Specifically, despite high intracellular concentrations of hexoses caused by specific enzyme
inhibitors, patatin expression was downregulated strongly,
thereby supporting a model in which extracellular concentrations or fluxes are sensed at the cell exterior (Müller-Röber
et al., 1990; Zrenner et al., 1995). As in the case of the hexokinase-dependent sensing mechanism, fluxes are more important than steady state levels of carbohydrate to initiate a
response. Studies on sugar-induced pathogen-related genes,
moreover, provide strong evidence for the existence of
sensing mechanisms, located at the plasma membrane,
which might correspond to the RGT2/SNF3-type sensing
system present in yeast.
Despite the central importance of sugars as key regulators of gene expression, very little is known about the signal
transduction mechanisms in which they take part. Several
studies have provided evidence that mechanisms similar to
yeast phosphorylation events are involved in sugar-specific
signal transduction cascades. Several kinase genes have
been found in plants with homology to SNF1 of which some
complement the snf1 yeast mutant. In vivo function has
been demonstrated in transgenic potato plants expressing
Sugar Transport and Sugar Sensing
719
Figure 6. Current Representation of Sugar Sensing in Plants.
Monosaccharide transporters allow the uptake of hexose analogs useful for probing the sugar signaling pathway. 6-Deoxyglucose and 3-O-methylglucose can be transported but are not substrates for hexokinase; therefore, signal pathways requiring hexokinase activity are not triggered by
these analogs, whereas genes like patatin class I, invertase, or sucrose synthase genes are induced via a hexokinase-independent pathway.
Mannose and 2-deoxyglucose serve as substrates for hexokinase and can thus repress photosynthetic genes via the hexokinase-dependent
pathway. Sucrose can be metabolized and hexoses used in the hexokinase-dependent pathway.
an SNF1-related protein kinase gene in antisense orientation
such that a decrease in sucrose synthase expression is observed in tubers (Halford and Hardie, 1998). Rubisco gene
repression and invertase gene induction by sugars involve
the action of both kinases and phosphatases (Ehness et al.,
1997). Also, in the case of the regulation of sporamin and
b-amylase gene expression, the involvement of protein
phosphorylation is likely inasmuch as treatment with specific
inhibitors of kinases and phosphatases reduces sugar-spe-
cific induction (Ohto and Nakamura, 1995; Takeda et al.,
1994).
HORMONAL REGULATION OF SUGAR TRANSPORT
Many studies have provided evidence that sugar transport
can be adapted to the changing needs of the plant. Indeed,
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The Plant Cell
comparison of the transport activities in developing versus
mature leaves has shown that H1/sucrose cotransport is differentially active and develops during leaf maturation (Lemoine
et al., 1992). Hormones such as auxin and cytokinin have
long been known to increase the rate of phloem transport.
Fusicoccin and auxin can rapidly promote sucrose uptake,
whereas abscisic acid acts as an inhibitor (Malek and Baker,
1978; Sturgis and Rubery, 1982; Vreugdenhil, 1983). In
broad bean, the direct promotion of assimilate export by the
application of gibberellin was reported (Aloni et al., 1986).
Phloem loading in isolated bundles of celery seems to be directly affected by gibberellin and auxin (Daie et al., 1986).
However, a principle problem of such studies is the difficulty
to differentiate between effects operating within the network.
Proton-coupled sugar transporters can be regulated in
two major ways: (1) indirectly by regulating H 1-ATPase activity, or (2) more specifically by controlling the expression of
sugar transporters at the transcriptional and post-transcriptional levels. Several factors are known to regulate ATPase
activity and/or transcription: fusicoccin (Oecking et al.,
1997; Baunsgaard et al., 1998), salicylic acid (Bourbouloux
et al., 1998), and anaerobiosis, which probably acts at the
level of ATP supply for the H 1-ATPase (Sowonick et al.,
1974; Giaquinta, 1977; Servaites et al., 1979; Thorpe et al.,
1979; Maynard and Lucas, 1982; see also Sze et al., 1999,
in this issue). Sucrose can also induce accumulation of two
plasma membrane ATPases, LHA4 and LHA2 (Mito et al.,
1996). This induction is dependent on sugar uptake and metabolism, inasmuch as mannitol and 3-O-methylglucose
have no effect. These results suggest that the induction of
expression of H1-ATPase genes by metabolizable sugars
may be part of a generalized cellular response to promote
cell growth in the presence of abundant carbon sources
(Mito et al., 1996).
Potato SUT1 and Arabidopsis AtSUC2 are expressed in
source and sink tissues (Riesmeier et al., 1993; Truernit and
Sauer, 1995). The expression of the sucrose transporter
SUT1 is diurnally regulated at both the mRNA and protein
level (Kühn et al., 1997), in accordance with diurnal regulation of export rates from leaves (Heinecke et al., 1994).
SUT1 mRNA and protein levels can, furthermore, be induced by the addition of auxin and cytokinin to detached
leaves (C. Kühn and W.B. Frommer, unpublished results),
whereas no such effect was observed for either of the two
major H1-ATPase genes expressed in potato leaves (Harms
et al., 1994). Sucrose itself was shown to be involved in regulating sucrose transporter activity, potentially at the transcriptional level (Chiou and Bush, 1998).
Inhibitor experiments indicate that SUT1 activity is also
regulated at the post-translational level by phosphorylation
(Roblin et al., 1998). Protein kinase activities, which might be
responsible for phosphorylation of sucrose transporters in
the SEs, have been detected in the phloem sap (Nakamura
et al., 1993). As described in yeast, sugars may also regulate
the stability of transporters (Jiang et al., 1997). Inhibition
studies using cycloheximide show that the half-life of SUT1
is in the range of a few hours (Kühn et al., 1997). This high
turnover rate may indicate specific mechanisms controlling
the number of active carriers in the plasma membrane and
may suggest involvement of endocytosis, as in the case of
mammalian glucose transporters and yeast amino acid permeases (Hein et al., 1995; Thorens, 1996).
Concerning monosaccharide transport, no clear function
has been demonstrated using antisense or “knockout” strategies. Very little is also known about its regulation. Coordinated regulation of mRNAs for extracellular invertase and a
monosaccharide transporter in C. rubrum has been described (Ehness and Roitsch, 1997). Because sucrose synthase and invertase gene expression is regulated by sugars,
one may expect a complex network coordinating uptake of
both monosaccharides and sucrose with the metabolic
events involving both extracellular and intracellular sensors
as sketched in Figure 6.
PLANT TRANSPORTER FAMILIES IN SUGAR SENSING
Are there known members of the plant transporter families
that could be sensors? Indications, as presented above,
suggest that transporters might be involved in sensing hexoses (Figure 6; Martin et al., 1997). As described above,
such sensors in yeast often contain additional cytosolic domains that are thought to play a role in transmitting the signal. Analysis of the plant monosaccharide transporter MST
family (Table 1) indicates that the Arabidopsis genome contains at least 26 MST genes. Although none of the predicted
AtMST proteins share obvious similarities with the C-terminal extensions found in the yeast RGT2 and SNF3, two Arabidopsis genes (AtSUGTRPR and F23E12.140; Table 1) that
are closely related to each other contain extended central
loops. Additionally, one member of the tomato and Arabidopsis SUT family is characterized by the presence of a long
central loop predicted to be cytosolic (L. Barker, C. Kühn, B.
Hirner, E. Boles, H. Hellmann, A. Weise, J.M. Ward, and
W.B. Frommer, unpublished results). The availability of the
full sequence from Arabidopsis will provide access for more
detailed analysis. Because the putative tomato sucrose sensor colocalizes with SUT1 and because no sucrose transport activity is detectable, one might speculate that it is
involved in controlling the expression and turnover of SUT1
in SEs (Figure 7).
Because transporter-like sensors have also been identified for amino acids and ammonium, one may speculate that
the transporter families also contain respective sensors.
Within the large amino acid transporter families, no homologs containing large cytosolic domains similar to SSY1
have been found to date (Fischer et al., 1998). Because in
the putative yeast ammonium sensor MEP2 no extended
loops or other features that specify it as a sensor have been
identified and because it represents a functional transport
Sugar Transport and Sugar Sensing
721
an essential component responsible for phloem loading, as
was shown by antisense inhibition in transgenic potato and
tobacco. Physiological studies have shown that plant sugar
transport and metabolism are highly regulated by sugars at
the transcriptional and post-transcriptional levels. In yeast,
sugar regulation of transporters is controlled by sensors at
the plasma membrane. The availability of genes for members of the plant MST and SUT family and other phloem
sap-specific proteins provides the tools to further explore
and understand the mechanism and regulation of long-distance transport and its role in sugar sensing and regulation
in plants.
ACKNOWLEDGMENTS
Figure 7. A Potential Sucrose-Sensing Mechanism in SEs.
Solanaceous SUT1 and a sucrose sensor colocalize in SEs (by analogy with yeast SNF3 and RGT2 proteins). The putative sensor regulates SUT1 either directly or via an indirect signaling mechanism
such as phosphorylation. The high turnover rates of SUT1 may indicate that regulation occurs at the level of protein inactivation and
degradation; however, because SUT1 is transcribed in companion
cells, a regulatory mechanism involving transcriptional control is
more complicated but still possible.
We are grateful to Bruno André (Université Libre de Bruxelles, Belgium) for critical reading of the manuscript and helpful discussion.
This work was supported by grants from Deutsche Forschungsgemeinschaft (Grant No. SFB446) and the European Union Biotechnology Program (Grant Nos. BIO4 CT96-0583 and BIO4 CT96-0311)
and by an Alexander von Humboldt fellowship to S.L.
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The Dual Function of Sugar Carriers: Transport and Sugar Sensing
Sylvie Lalonde, Eckhard Boles, Hanjo Hellmann, Laurence Barker, John W. Patrick, Wolf B. Frommer
and John M. Ward
Plant Cell 1999;11;707-726
DOI 10.1105/tpc.11.4.707
This information is current as of July 31, 2017
References
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