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In higher plants, CO2 fixation occurs predominantly in meso-phyll cells of mature leaves. These are net exporters of sugarsand are known as carbon sources. Heterotrophic cells inroots, reproductive structures, storage and developing organs relyon a supply of sugars for their nutrition; these are known as car-bon sinks (net importers). Mechanisms must exist to ensure thatall sink tissues receive an adequate supply of sugars for growthand development, and sugar transporters play a pivotal role in themembrane transport of sugars and their distribution throughoutthe plant (Fig. 1).

Long-distance transport of carbohydrates between sources andsinks occurs in specific cells of the vascular system, the phloemsieve elements (Fig. 1). During their development, sieve elementsextend longitudinally, degrade most of their organelles, includingvacuoles, ribosomes and nuclei, and form large, plasma mem-brane-lined pores in their terminal cell walls, the sieve plates. Theloss of organellar structures in sieve elements is paralleled by anextreme increase in organelle density in the phloem companioncells. Sieve elements and companion cells are intimately con-nected by numerous branched plasmodesmata and form the so-called sieve elementcompanion cell complex (SECCC). Animportant function of companion cells is the supply of energy andproteins to the sieve elements.

Phloem sap in sieve elements moves by bulk flow with rates ofup to 1 m per h. At the source, accumulation of sugar inside theSECCC (at a concentration of several hundred mM to 1 M)results in the osmotic uptake of water, forcing sap to flow alongthe sieve tube. Unloading of sugar at the sink results in loss ofwater from the sieve tube and thus the gradient of pressure ismaintained. Sucrose represents the main form of reduced carbontransported in sieve elements, although some plants can alsotransport raffinose, stachyose and polyols. These solutes are less

subject to metabolism than glucose. After its synthesis, sucrosecan pass the entire route from the mesophyll cells to the sieve

elementcompanion cell in the symplast, moving from cell to cellvia plasmodesmata (symplastic loading; Fig. 1). However, fre-quently, sucrose is released from the mesophyll cells and activelyloaded from the apoplast into the SECCC (apoplastic loading).Plasma membrane sucroseH symporters are fundamental to thisprocess. Unloading of sucrose at the sinks might also occur eithersymplastically or apoplastically. The route depends on species(both pathways might operate in the same organism), organ ortissue, and developmental stage. Sink cells either import sucrosefrom the apoplast directly via sucrose transporters or, alternatively,sucrose can be hydrolysed to glucose and fructose by cell-wall-bound invertases and taken up via monosaccharide transporters.

Plants appear to have several monosaccharide and disaccharidetransporters to coordinate sugar transport in diverse tissues, at dif-ferent developmental stages and under varying environmentalconditions. The nomenclature in the literature for plant sugartransporters has become rather confusing with SUT and SUCbeing used for disaccharide transporters, and STP, MST, HEXand ST being used for monosaccharide transporters. Here we willrefer to disaccharide transporters as DSTs and refer to monosac-charide transporters as MSTs. Some of the physiological func-tions of these sugar transporters, as suggested from work at themolecular level, will be discussed. Other proteins that have beenimplicated in the transport of sugars [e.g. sugar-binding protein,SBP (Ref. 1)] will not be considered here.

Multi-gene families for sugar transporters

In Arabidopsis, 14 putative MST genes have been identified todate2 and at least seven DST genes can be found in Arabidopsisdata libraries. Heterologous expression in yeast or Xenopusoocytes has been carried out for some of the family members, andevidence suggests that they function as proton symporters38. Gen-

erally the DSTs are highly specific for sucrose, although somehave been shown to transport maltose9. Their Km values are in the

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Sugar transporters in higherplants a diversity of roles

and complex regulationLorraine E. Williams, Remi Lemoine and Norbert Sauer

Sugar-transport proteins play a crucial role in the cell-to-cell and long-distance distribution ofsugars throughout the plant. In the past decade, genes encoding sugar transporters (or carri-ers) have been identified, functionally expressed in heterologous systems, and studied withrespect to their spatial and temporal expression. Higher plants possess two distinct families ofsugar carriers: the disaccharide transporters that primarily catalyse sucrose transport and themonosaccharide transporters that mediate the transport of a variable range of monosaccha-rides. The tissue and cellular expression pattern of the respective genes indicates theirspecific and sometimes unique physiological tasks. Some play a purely nutritional role andsupply sugars to cells for growth and development, whereas others are involved in generatingosmotic gradients required to drive mass flow or movement. Intriguingly, some carriers mightbe involved in signalling. Various levels of control regulate these sugar transporters duringplant development and when the normal environment is perturbed. This article focuses onmembers of the monosaccharide transporter and disaccharide transporter families, providingdetails about their structure, function and regulation. The tissue and cellular distribution ofthese sugar transporters suggests that they have interesting physiological roles.


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0.31.0 mM range9. The MSTs have broader substrate specificity,transporting a range of hexoses and pentoses with Km values for thepreferred substrate being typically 10100 M (Ref. 2). MSTs andDSTs share little homology at the amino acid level, although thereare structural similarities (Fig.2). They are thought to be members ofthe major facilitator superfamily10,11. Whereas DST genes appear tobe specific for plants, numerous genes that are homologous to theMSTs are found in bacteria, fungi and mammals (Fig. 3).

Diverse locations for sugar transporters

Plant cells appear to possess sugar transporters tailored to meettheir specific requirements at particular stages of development

(Fig. 4). Only a few DSTs and MSTs havebeen localized precisely at the membranelevel12,13. Many authors have simplyassumed that these proteins are localized atthe plasma membrane, because they aretargeted to this membrane in transgenicyeast. Detailed studies are required to con-

firm this for each family member. Some ofthe more interesting physiological func-tions of a range of sugar transporters, assuggested from work at the molecularlevel, are discussed below.

Phloem-associated sucrose transporters

In apoplastic phloem loading, a DST proteinat the plasma membrane of phloem cells accu-mulates sucrose in the SECCC to drive long-distance transport (Figs 1 and 4). In someplants these sucrose transporters have beendetected in sieve elements (Ref. 12), whereasothers have been observed in companion

cells14,15. This might be explained by speciesdifferences, but recent work in Plantago hasshown that there are sucrose transporters spe-cific to either companion cells or sieve el-ements (R. Stadler et al., unpublished). All ofthese transporters result from gene transcrip-tion in the companion cell, and it will beimportant to determine the signals and mech-anisms that regulate their final destination. InSolanaceae, SUT1 (DST) mRNA is localizedin the sieve elements, suggesting that tran-scription occurs in the companion cell andmight be followed by the transportation ofmRNA through the plasmodesmata and trans-lation within the sieve elements12.

In Solanaceous species, antisense studieshave shown that SUT1 (DST) is indeedessential for phloem loading and long-dis-tance transport16,17. Potato plants with drasti-cally lowered expression of SUT1 (DST)had a reduced tuber yield (size and number),and mature leaves accumulated sugarsbecause of impaired export16,17. This wasconfirmed in tobacco, where strong anti-sense plants had a dwarf phenotype, andsugar export from leaves was also drasti-cally impaired18. In wild-type plants,lengthy dark exposure leads to starch degra-dation in leaves and subsequent exportationof sucrose to sink organs. However, in anti-sense plants, starch remains in the leaves

and this is related to impaired sucrose export. Phloem-localizedSUT1 (DST) homologues might play an additional role in both theretrieval of sucrose leaking from sieve elements along the translo-cation pathway and possibly in catalysing the export of sucrosefrom the phloem in sinks19 (Fig. 1). Moreover, the same transportersare not always confined to the phloem but are also present at lowerlevels in other leaf cells where they might function in retrieval 17,20.

Sugar transporters in roots

Roots represent heterotrophic carbon sinks and can be divided

into zones of cell division, elongation and maturation. AtSTP4(MST), a monosaccharide transporter fromArabidopsis, is found

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Fig. 1. The contribution of sugar transporters to long-distance sugar transport between sourcesand sinks. Long-distance transport of sucrose (S) between sources and sinks occurs in sieveelements of the phloem, which constitute part of the vascular system (path). Sucrose is trans-ported in the phloem sap by bulk flow. In the source leaf, sucrose can pass the entire route fromthe mesophyll cells (source cell) to the sieve elementcompanion cell in the symplast, movingfrom cell to cell via plasmodesmata (P). However, in many species, sucrose leaves the symplastat some point, possibly via sucrose efflux carriers (red circle), and is actively accumulated fromthe apoplast into sieve elements and/or companion cells by plasma membrane protonsucrosesymporters (purple and dark-blue circles, respectively). Energization is via the proton-motiveforce generated by the plasma membrane H-ATPase (black square). Passive influx of waterinto the sieve tubes presumably occurs via water channels. Expression of sucrose carriers(light-green circle) along the path has been related to a function for retrieving sucrose leakedfrom the phloem. Unloading of sucrose into sink cells might occur symplastically via plas-modesmata or sucrose might be delivered to the apoplast via a sucrose efflux carrier (pink cir-cle). Here, it is either taken up directly by plasma membrane sucrose transporters (yellowcircle), or first hydrolysed to glucose (G) and fructose (F) by the cell-wall invertase (dark-green

elipse) then taken up via plasma membrane monosaccharide transporters (light-blue circle).

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only at the root tip, probably in the rootmeristem21 (Fig. 4). This indicates that partof the post-phloem transport inArabidopsisroots occurs apoplastically and that the roleof AtSTP4 (MST) is to import hexoses gen-erated from sucrose hydrolysis by cell-wallinvertase following phloem unloading. In

Medicago truncatula, the gene for themonosaccharide transporter, Mtst1 (MST),is only expressed in cells immediatelybehind the root apical meristem, in cellswithin the elongation zone and possibly inthe zone of cell division22. Elongating cellshave a high requirement for hexoses as pre-cursors for macromolecular synthesis andto allow them to maintain osmotic pressureduring elongation22. Mtst1 (MST) is alsoexpressed in primary phloem fibres where itmight provide hexoses for cell wall biosyn-thesis and deposition22.

Sucrose transporters have also been

detected in particular cells of the root:DcSUT2 (DST) is expressed in storageparenchyma tissues of carrot tap-rootswhere it seems to import sucrose for stor-age23. This and other DST homologueshave also been detected in phloem cells ofthe root, where they might retrieve sucroseinto the phloem or possibly catalyse theefflux of sucrose from the phloem19.

A role for sugar transporters in developing

and germinating seeds

The developing embryo is symplastically iso-lated from maternal tissues and is reliant onthe import of sugars from the surroundingapoplastic space. Sugars are required forembryo development and for the depositionof storage compounds necessary for germi-nation. DSTs and MSTs have been identifiedin Vicia faba, Pisum sativum andHordeumvulgare (Refs 2426). In Vicia, VfSTP1(MST) is expressed in the embryo cotyledonepidermal cells. Expression is confined to epi-dermal regions covering the mitotically activeparenchyma, indicating that this transporterserves to supply substrate for metabolism24.During later stages of embryo development,VfSTP1 (MST) is replaced by the sucrosetransporter VfSUT1 (DST)24. VfSUT1 (DST)expression is highest in epidermal cells withtransfer-cell morphology and with storageactivity in the underlying parenchyma, indi-cating that the encoded transporter is respon-sible for providing substrate for the synthesisof storage compounds24.

Certain seeds accumulate storage reserves in the endosperm dur-ing development. Upon germination, these are hydrolysed and theproducts, including sugars, are released into the apoplastic space(Fig. 5). In germinating seeds ofRicinus communis, a sucrose car-rier,RcSUT1 (DST), is expressed at high levels in both the coty-ledon epidermal cells that are situated adjacent to the endosperm

and also in the phloem

13

. This suggests that the epidermal cells ini-tially accumulate sucrose from the apoplast and from here sucrose

is transferred symplastically to the phloem region. The high expres-sion ofRcSUT1 (DST) in the phloem indicates that sugars arereleased into the apoplast before active loading by this transporter.

A variety of roles for sugar transporters in floral organs

Developing pollen grains are strong sinks that require carbohy-

drate import from the apoplast during maturation, germinationand growth. The Arabidopsis monosaccharide transporter gene,

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Fig. 2. Topological models of the disaccharideHsymporter, (a) PmSUC2 [disaccharidetransporter (DST)] and (b) the monosaccharideH symporter, NtMST1 [monosaccharidetransporter (MST)]. MSTs and DSTs have predicted molecular masses of ~55 kDa andhydrophobicity analysis indicates that they are highly hydrophobic integral membrane pro-

teins. They share little homology at the amino acid level, although there are structural simi-larities and they are thought to be members of the major facilitator superfamily. In this family,it is proposed that the twelve transmembrane -helical structure has evolved from an ances-tral six-transmembrane-segment transporter gene following gene duplication and fusion10.Family members generally possess a large central loop between transmembrane domains sixand seven (the length of this loop varies in members of the DST and MST families).


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Fig. 3. Phylogenetic analysis for (a) monosaccharide transporters (MSTs) and (b) disaccharide transporters (DST). (a) Sugar-transport pro-teins homologous to lower and higher plant monosaccharide transporters are found in prokaryotes, fungi and mammals, indicating that thecorresponding genes form an ancient gene family. Monosaccharide transporters from one species, such as the Arabidopsis AtSTPs, do notform a single subcluster within the higher plant subfamily, suggesting that several independent genes already existed at the beginning of or

early in higher plant evolution. The less closely related Arabidopsis AtERD6 protein (Accession no. D89051), described as a putative sugartransporter, clusters with the human glucose facilitator. (b) Proteins closely related to higher plant sucrose transporters are not found in bac-teria, fungi or mammals, indicating that plant sucrose-transporter genes evolved comparatively late. Sucrose transporters from Arabidopsiscluster together with sucrose transporters from monocots and from plants with symplastic phloem loading. A functionally uncharacterizedtransporter from Schizosaccharomyces pombe (Accession no. Z99165) shows some similarity, but only in the N-terminal half of the protein.EcMelB (the outgroup) is extremely distantly related to plant sucrose transporters 45. Bootstrap values given at internal nodes indicate the per-centage of the occurence of these nodes in 100 replicates (maximum parsimony) of the data set. The sequence of the E. coli xylose perme-ase (EcXylE; black) and of theE. coli melibiose transporter (EcMelB; black) were used as outgroups in (a) and (b), respectively. Accessionnumbers for nonplant monosaccharide transporter sequences are AmMST1 (Amanita muscaria monosaccharide transporter), Z83828;EcAraE (E. coli arabinose transporter), J03732; EcGalP (E. coli galactose permease), AE000377; EcMelB (E. coli melibiose transporter),K01991; EcXylE (E. coli xylose transporter), P09098; HsGlut1 (Homo sapiens glucose transporter), 87529; ScHXT1 (Saccharomyces cere-visiae hexose transporter), M82963; ScHXT2 (S. cerevisiae hexose transporter), M33270; ScHXT3 (S. cerevisiae hexose transporter),L07080; ScRGT2 (S. cerevisiae hexose transporter-like glucose sensor), Z74186; ScSNF3 (S. cerevisiae hexose transporter-like glucose sen-sor), J03246; SspGTR (Synechocystis sp. glucose transporter), X16472. Maximum parsimony (MP) bootstrap analyses of aligned sequenceswere conducted with the PHYLIP package 3.572c. Addition of taxa was jumbled and repeated three times for each individual bootstrap repli-cation in the MP analysis. Output treefiles were combined with the CONSENSE program and converted into a graphical representation by theTREEVIEW program. Accession numbers of plant sucrose transporters used in this tree are AbSUT1 (Asarina barclaiana, AF191024);AgSUT1 (Apium graveolens, AF063400); AmSUT1 (Alonsoa meridionalis, AF191025); AtSUC1 (Arabidopsis thaliana, X75365);AtSUC2 (A. thaliana, X75382); AtSUC3 (A. thaliana, AC004138); AtSUC4 (A. thaliana, AC000132); AtSUC5 (A. thaliana, AJ252133);AtSUC8 (A. thaliana, AAC69375); AtSUC13 (A. thaliana, AB016875); BvSUT1 (Beta vulgaris, X83850); DcSUT1 (Daucus carota,Y16766); DcSUT2 (D. carota, AB036758); HvSUT1 (Hordeum vulgare, Accession no. not yet available); HvSUT2 (H. vulgare, Accessionno. not yet available); NtSUT1 (Nicotiana tabacum, X82276); OsSUT1 (Oryza sativa, D87819); PmSUC1 (Plantago major,X75764); PmSUC2 (P. major, X75764); SoSUT1 (Spinacea oleracea, X67125); StSUT1 (Solanum tuberosum, X69165); VfSUT1(Vicia faba, Z93774). Accession nos of plant monosaccharide transporters used in this tree are AtSTP1 (A. thaliana, X55350); AtSTP2(A. thaliana, AJ001362); AtSTP3 (A. thaliana, AJ002399); AtSTP4 (A. thaliana, X66857); AtSTP6 (A. thaliana, AC013454); AtSTP7(A. thaliana, AF001308); AtSTP8 (A. thaliana, AF077407); AtSTP9 (A. thaliana, AC007980); AtSTP10 (A. thaliana, AB025631); AtSTP11(A. thaliana, AB007648); AtSTP12 (A. thaliana, AL022603); AtSTP13 (A. thaliana, AF077407); AtSTP14 (A. thaliana, AC004260);CkHUP1 (Chlorella kessleri, Y07520); CkHUP2 (C. kessleri, X66855); CkHUP3 (C. kessleri, X75440); LeMST1 (Lycopersicumesculentum, AJ010942); MtMST1 (Medicago truncatula, U38651); PaMST1 (Picea abies, Z83829); PhPMT1 (Petunia hybrid, AF061106);RcHEX1 (Ricinus communis, L08197); RcHEX6 (R. communis, L08188); RcSTC (R. communis, L08196); SspSGT2 (Saccharum hybrid,L21753); VfMST1 (V. faba, Z93775); VvMST1 (Vitis vinifera, AJ001061).


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AtSTP2 (MST), is expressed after meiosisof the pollen mother cell at the time whenthe uninucleate microspores are develop-ing27. This correlates with the time whencallose surrounding the microspores isdegraded. After this, AtSTP2 (MST)mRNA and protein are rapidly degraded27.

Thus, AtSTP2 (MST) could serve in theuptake of glucose (resulting from callosedegradation) and also other monosaccha-rides such as xylose, mannose or galactose(from degradation of other cell-wall com-ponents) into the symplastically isolated,developing male gametophyte27.

Carbohydrates are also required to sup-ply energy for pollen germination andpollen-tube growth. PhPMT1 (MST), aputative hexose transporter gene in Petu-nia, is expressed specifically in matureanthers and pollen, and not in any other flo-ral or vegetative tissues28. Thus, in this

species, sucrose might be hydrolysed toglucose and fructose by a cell-wall inver-tase before uptake by PhPMT1 (MST) inthe growing pollen tube28. A similar local-ization has been shown for theArabidopsisAtSTP4 (MST) monosaccharide trans-porter21 (Fig. 4); however, its function isunclear because in this species (and inmany others) sucrose is the preferred car-bon source during pollen germination andgrowth in vitro. Recent studies describingthe expression of the sucrose transportergenes,AtSUC1 (DST) in germinatingAra-bidopsis pollen (Fig. 4) andNtSUT3 (DST)in tobacco pollen, are consistent withthis29,30. Interestingly, AtSUC1 (DST)mRNA was detected in developing pollenwhereas the protein was only found afterpollen germination, indicating that expres-sion might be translationally regulated andinduced during germination29.

AtSUC1 (DST) is also expressed in aring of parenchymatic cells surroundingthe transmitting tissue of the style and inthe epidermal cell layers of the funiculi29.This expression pattern is unlikely toreflect a higher requirement for carbohy-drates by these cells; instead it might indi-cate that AtSUC1 (DST) modulates theavailability of water in this region, whichcould establish a cue for pollen-tube guid-ance towards the ovule29.

In anthers, AtSUC1 (DST) mRNA andprotein were detected in parenchymaticcells surrounding the central vascular bun-dle of anther connective tissue just beforeanther opening by dehiscence29 (Fig. 4).Accumulation of sucrose by AtSUC1(DST) could decrease the water potentialand hence result in water uptake from the adjacent cells of theanther walls29. This would result in dehydration of the endothecium

and an increased tension of its wall thickenings, finally causinganther opening29.

Sugar transporters in plantmicroorganism interactions

Some sugar transporters seem to play a role in certain

plantmicroorganism interactions. The sink-specific, wound-induced monosaccharide transporter, AtSTP4 (MST) is induced

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Fig. 4. Tissue and cellular distribution of various sugar transporters. The tissue or cell-specificexpression of several sugar transporters indicates their specific physiological tasks. For example,sugar transporters have been implicated in processes as diverse as phloem loading and unloading,pollen development and germination, and pathogen interaction. (a) Expression of the sucrosetransporter geneAtSUC2(disaccharide transporter, DST) in the veins ofArabidopsissource leavesindicates a role in phloem loading. The expression is demonstrated by the activity of the reportergene for -glucuronidase (GUS) driven by the AtSUC2 promoter19. In (b), the AtSUC2 (DST)protein was immunolocalized with fluorescent secondary antibodies in companion cells of leafminor veins15. Xylem vessels are identified by the yellow autofluorescence of lignin. (c) Ex-pression of the monosaccharide transporter gene,AtSTP4, fromArabidopsis in root tips is shownby GUSexpression under the control of theAtSTP4 promoter21. The expression of this carrier isalso induced by wounding and pathogen attack. (d)In situ hybridization ofAtSUC1(DST) mRNAon an anther cross-section29. At this stage, the AtSUC1 (DST) protein is detected in the connectivetissue but not in the pollen, suggesting translational regulation. The sucrose carrier AtSUC1 (DST)mRNA fromArabidopis has been identified in the connective tissue of mature anthers and alsoin pollen. In the connective tissue, AtSUC1 (DST) could be involved in the control of antherdehiscence. (e) The monosaccharide transporter AtSTP4 (MST) is detected in pollen tubesgrowing inside the transmitting tissue of the style (longitudinal section through a style). Specificantibodies were used and the fluorescence of the secondary antibodies appears in green.Interestingly, the sucrose transporter AtSUC1 (DST) is also present in germinating pollen 29.

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approximately fourfold in Arabidopsis seedlings infected withAlternaria brassicicola or Fusarium oxysporum, and also in sus-pension-cultured cells ofArabidopsis treated with bacterial orfungal elicitors21. It has been concluded that AtSTP4 (MST) playsa role in the transportation of monosaccharides into the sinktissues and that it responds to an increased demand for carbohy-drate by cells under stress conditions21. Induction ofAtSTP4(MST) expression is also observed during plant and fungalbiotrophic interaction, for example, Arabidopsis infected withthe powdery mildew Erysiphe cichoracearum31. Expression of

AtSTP4 (MST) is induced dramatically in source leaves infectedwith mildew and, although the fungus is confined to epidermalcells, AtSTP4 (MST) expression is induced in many cell typeswithin the leaf following infection (M. Gilbert et al., unpublished).The signalling pathway by which this occurs is unknown, and the

role of this transporter in this interaction is unclear. It might helpto increase carbohydrate import into infected tissues, in order to

cope with the increased demand related todefence activities, or serve to recover sug-ars from the apoplast (particularly if host-cell permeability is increased) and thusreduce the loss of carbohydrate to thepathogen.

Sugar transporters are also important in

carbon transfer to mycorrhizal fungi22. Col-onization ofMedicago truncatula roots withthe mycorrhizal fungus Glomus versiforme,induces expression of the monosaccharidetransporter gene,MtST1 (MST), in corticalcells of the root that correlates with regionsthat are heavily colonized by the fungus22.The effect is localized to cells within theimmediate vicinity of the fungus, either incells containing an arbuscule, or cells thatare frequently in contact with intercellularhyphae. The nature of the signal for theinduction of plant sugar-carriers duringmicroorganism interactions is not yet clear.

Role in sugar sensing

Sugars can act as regulatory signals thataffect gene expression and hence plantdevelopment. In relation to resource allo-cation, the ability to sense altered sugarconcentrations could have importantadvantages by allowing the plant to tailorits metabolism in source tissues to meet thedemands in sinks. There is great interest indissecting the signalling processes that areinvolved in sugar sensing and responsepathways. There are three possible sugar-sensing systems in plants32: A hexokinase-sensing system. A sucrose-transport-associated sensor. A glucose-transport-associated sensor.Based on sugar signal transduction processesin Saccharomyces, it has been proposed thatmembers of the sugar transporter family inplants might play a role in sugar sensing33. Inyeast, it has been shown that membrane-bound receptors closely related to sugartransporters are used to sense external sugarconcentrations and activate a signal trans-duction pathway leading to the regulation of

transporter gene expression and insertion or degradation of proteinsat the plasma membrane. This allows yeast to respond to a rapidlychanging external environment. The yeast glucose sensors, ScSNF3(senses low glucose levels) and ScRGT2 (senses high glucose lev-els) are homologous to yeast and plant glucose transporters (Fig. 3)but do not mediate significant glucose transport34. The large C-terminal extensions of these proteins are required for the trans-mission of the glucose signal. To date, there is no direct evidence fora role of plant monosaccharide and disaccharide transporters assensors. Nevertheless, the finding that several members of the plantMST and DST families have unusual cytoplasmic extensions, whichare predicted to be cytosolic, has initiated studies in relation to thepossible role of these proteins in sugar sensing33.

Regulation of sugar transporters

As sugar transporters play such a key role in sourcesink interac-tions, it is likely that they are tightly controlled. There are several

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Fig. 5. Localization of the sucrose carrier in a germinating Ricinus seedling. Seeds accu-mulate storage reserves in the endosperm during development. Upon germination, these arehydrolysed and the products, including sugars, are released into the apoplastic space. Seven-day-old dark-grown germinatingRicinus seedlings are shown in (a) with (left) and without

(right) an endosperm. (b) Breakdown of lipids and protein in the endosperm and the release ofsucrose and amino acids into the apoplast for uptake by the cotyledon. (c) Expression patternof the sucrose transporter,RcSUT1 (DST)13,46, in the germinatingRicinus seedling (three-day-old).RcSUT1 transcripts were localized by in situ hybridization using an antisenseRcSUT1cRNA probe. Dark staining, indicating RcSUT1 expression, is seen in both the cotyledonlower epidermal cells (LE) that are situated adjacent to the endosperm (parts iiii) and also inthe phloem (red arrows in iii). No equivalent staining was observed in sections probed withthe sense probe (results not shown). The expression pattern indicates that the epidermal cellsinitially accumulate sucrose from the apoplast and from here sucrose is transferred symplasti-cally to the phloem region. The high level of expression ofRcSUT1 in the phloem indicatesthat sugars are released into the apoplast before active loading by this transporter. Scale bars 100 m in (i) and (ii); 50 m in (iii). (c) reproduced, with permission, from Ref. 13.

Lipids

Proteins

EndospermAminoacids

Sucrose

Cotyl

edon

s

Hypo

cotyl

(a)

(c) (i) (ii)

(iii)

(b)

LE

LE

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levels at which regulation might occur35,36. As for all H-sym-porters, regulation of activity by the proton-motive force is clearlyimportant. Thus, modulations in the activity of the H-ATPasewould immediately affect their sugar transport kinetics.

There are numerous examples for transcriptional regulation ofDSTor MSTgene expression, such as changes in DSTexpressionpattern in leaves undergoing sink-to-source transition19,37 during seed

development (MST and DST)24, or during pollen maturation and ger-mination (MST and DST)27,28. There is also evidence that biotic andabiotic factors (e.g. mechanical treatments, light, water and saltstress, phytohormones, and pathogen attack) have effects on theexpression of certain sugar transporters21,36,38. Post-transcriptionalcontrol mechanisms such as mRNA stability (turnover), mRNAtranslation and post-translational control have also been describedfor sugar transporters. Examples include the diurnal regulation ofDSTs (Refs 12,39), phosphorylationdephosphorylation40, and pos-sible modification of activity by the lipid environment36.

There is evidence that changing sugar levels might have an effecton sugar transporter expression and activity. Evidence has beenprovided that a putative sucrose-sensing pathway could modulatethe expression levels and activity of a protonsucrose transporter

as a function of changing sucrose concentrations in the leaf(hexoses do not elicit the response)41. This would have a directimpact on assimilate partitioning at the level of phloem translo-cation. Changes in transcriptional activity or mRNA turnovermediate this repression by sucrose but additional regulation byalterations in protein turnover or direct modification cannot beruled out. The response is reversible, highlighting the dynamicnature of this signalling pathway.

Evidence for sugar regulation of transporters is variable.AtSUC2 (DST) expression (analysed using a SUC2 promoterGUS construct) appears unaffected by sugars19. However, down-regulation might not be seen in these experiments because of thestability of the GUS protein. In addition, it is still possible thatactivity might be affected by other mechanisms, even if the pro-moter is insensitive to sugars. The expression of the Vicia fabasucrose carrier gene, VfSUT1 (DST), but not the glucose trans-porter, VfSTP1 (MST), decreased in cotyledons following expo-sure to high concentrations of sucrose or glucose (150 mM),whereas lower levels (10 mM) had no effect on transcript levels24.Sucrose-feeding experiments with detached maize leaves led to anincrease in transcript leaves ofZmSUT1 (Ref. 42) (DST). By con-trast, no evidence was found for sugar regulation of three mono-saccharide-transporter genes (CST13) (MSTs) in suspension-cultured cells ofChenopodium rubrum43.

Thus, for sugar transporters, it is now emerging that variouslevels of control are implemented that allow plant cells to regulatethe fluxes of sugars across the plasma membrane during normalgrowth and development, and also when their natural environmentis perturbed.

The future

To comprehend sourcesink regulation fully and to be in a posi-tion to manipulate the complex interactions for agricultural ben-efit, it is vital that the underlying membrane transport processesare thoroughly characterized. This includes determining preciselythe range of sugar transporters that are involved, theirstructurefunction relationships, and defining their cellular andtemporal expression pattern. A particular goal would be the abil-ity to manipulate competition between sinks. For this we need tofind out how sugar carriers are regulated in metabolic and storagesinks and to relate this to the information available on the activity

of the sucrose metabolizing enzymes, invertase and sucrose syn-thase. Extracellular invertase is up-regulated in several situations

affecting sourcesink relations (e.g. following application of phyto-hormones and elicitors, pathogen attack and wounding)44 but fur-ther work is required to investigate the coordination of events. Insink cells, it is important to understand why, in some cases, sucroseis cleaved by a cell-wall invertase and therefore hexose carriers areinvolved, whereas in other cases sucrose is taken up and cleavedinside the cells. In germinating pollen, both monosaccharide and

disaccharide transporters are present2830, although sucrose is thepreferred carbon source for in vitro germination and hexoses areinhibiting. Clearly, work is needed for a full comprehension of therespective role of each carrier type in such cells.

We need to clarify which mechanisms exist for the efflux ofsugars from cells, for example, for efflux from the mesophyll orfrom apoplastically unloading phloem cells. Under nonenergizedconditions, influx carriers might be operating in efflux, allowingsugars to be transported down their concentration gradient; alter-natively, different transporters might be involved. In addition, theidentification of tonoplast sugar transporters is important forunderstanding storage and remobilization from the vacuole. Wemust also consider that entirely different mechanisms might existfor sugar transport, such as those involving ABC transporters.

More evidence is required on the physiological function ofsugar transporters to support the information from expressionstudies. In particular, no antisense studies have been reported forany of the monosaccharide transporters. We eagerly await studieson knockout mutants to dissect the transport processes in greaterdetail. The phenotype of such plants will provide clues concerningthe physiological role and importance of particular transporters. Inaddition, plants with transporter genes under the control of cell-specific promoters will enable us to learn more about sourcesinkinteractions and pathways of sugar movement.

Sensing functions are essential in allowing plants to adapt tochanging environments. One of the major challenges will be toidentify sugar-sensing mechanisms and the signal transductionpathways. It will be important to ascertain whether members ofthe sugar-transporter families are involved in this function.

Acknowlegements

Our work has been supported by a grant from the European Com-mission DG XII Biotechnology programme (ContractBIO4-CT96-0583). L.E.W. is grateful to the Royal Society for support. R.L.swork is supported by the CNRS, the French Ministry for Educationand Research and by the Rgion Poitou Charentes. N.Ss work wassupported by the Deutsche Forschungsgemeinschaft. The help ofVolker Huss with Figure 3 and the help of Cyril Maingourd withFigure 4 is gratefully acknowledged.

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Lorraine Williams* is at the School of Biological Sciences,University of Southampton, Bassett Crescent East, Southampton,UK SO16 7PX; Remi Lemoine is at the Laboratoire de Biochimieet Physiologie Vgtales, ESA CNRS 6161, Btiment Botanique,40 Avenue du Recteur Pineau, F-86022 Poitiers Cedex, France(tel 33 5 49454183; fax33 5 49454186; [email protected]); Norbert Sauer is at theDept of Botany II, Molecular Plant Physiology, University ofErlangen, Staudtstrasse, D-91058 Erlangen, Germany(tel 49 9131 85 28212; fax 49 9131 85 28751;e-mail [email protected]).

*Author for correspondence (tel 44 2380 594278;fax44 2380 594319; e-mail [email protected])

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