the dual function of sugar carriers: transport and sugar ... · apoplasmic transport plants that...

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 andSugar 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. Ward

a

a

Center for Plant Molecular Biology (ZMBP), University of Tübingen, Auf der Morgenstelle 1, D-72076 Tübingen, Germany

b

Institut für Mikrobiologie, Heinrich-Heine-Universität Düsseldorf, Universitätsstrasse 1, Geb. 26.12.01, D-40225Düsseldorf, Germany

c

Department of Biological Sciences, University of Newcastle, New South Wales 2308, Australia

INTRODUCTION

Sucrose and its derivatives represent the major transportforms of photosynthetically assimilated carbon in plants.Sucrose synthesized in green leaves is exported via thephloem, the long-distance distribution network for assimi-lates, to supply nonphotosynthetic organs with energy andcarbon resources. Sucrose not only functions as a transportmetabolite but also contributes to the osmotic driving forcefor phloem translocation (mass flow) and serves as a signalto activate or repress specific genes in a variety of differenttissues.

The long-distance transport of sucrose depends on afamily of proteins that act as sucrose carriers. The analysisof transgenic plants impaired in sucrose transporter expres-sion has demonstrated that sucrose transporter1 (SUT1) isessential for sucrose translocation in potato and tobacco.These results, together with the localization of SUT1 to sieveelements (SEs), indicate that phloem loading occurs in SEsby transmembrane uptake of sucrose directly from the apo-plasm.

The sucrose transporters identified so far arise from a sin-gle gene family. Some of the newly identified members ofthe family are involved in specific functions, such as nutri-tion of developing seeds or pollen. Physiological and molec-ular studies show that sucrose transport is highly regulatedat multiple levels of biological organization and in responseto changing sucrose concentrations. Thus, one of the mostexciting topics in the regulation of sucrose transport is sig-nal perception. By analogy to yeast, in which members ofthe sugar transport family serve as sugar sensors, we pro-pose that members of the plant sugar transporter family playa direct role in the signal transduction responsible for regu-lation of sugar transport and, thus, metabolism in general.

SUGAR TRANSPORT SYSTEMS IN HIGHER PLANTS

Plant Anatomy: Vascular Tissues

Nonphotosynthetic tissues and organs, including the entirebelow-ground portion of the plant, need to be supplied withenergy and fixed carbon. Sugars, synthesized in the meso-phyll cells, serve as the major exported photosyntheticproduct. To accommodate long-distance transport of sug-ars from source (net exporting) to sink (net importing)organs, a vascular network—the phloem—has evolved inland plants. The most abundant compound in the phloemsap of most plant species is the disaccharide sucrose(Zimmermann and Ziegler, 1975). For a minority of plantspecies, the principle translocated sugars fall into twomain groups: the sugar alcohols (mannitol and sorbitol)and the raffinose series (raffinose, stachyose, and verbas-cose) (Zamski and Schnaffer, 1996). In most cases inwhich such sugars predominate, however, sucrose is alsopresent.

With the exception of a few well-studied species, ourknowledge of phloem sap composition is limited to crudeanalyses (Zimmermann and Ziegler, 1975) derived fromstem incision experiments in which sugars present as stor-age compounds in stems may contaminate phloem sapsamples. Therefore, accurate and less invasive techniques,such as in vivo NMR (Köckenberger et al., 1997) or positron-emitting tracer imaging system (Hayashi et al., 1997), will berequired for a more accurate understanding of phloem sapcomposition.

The phloem of angiosperms consists of several types ofcells that are closely associated with the xylem within thevascular bundle. The structure and development of thephloem has been reviewed recently (Sjölund, 1997; Ward etal., 1998; Oparka and Turgeon, 1999, in this issue). The ac-tual conduits in phloem consist of two ontogenetically re-lated cell types: companion cells (CCs) and SEs. These twocells are highly modified and well interconnected by plas-modesmata. SEs, for instance, lose their nuclei, vacuoles,and many other organelles during maturation and form

1

To whom correspondence should be addressed. E-mail [email protected]; fax 49-7071-29-3287.

708 The Plant Cell

tubes of living cells connected by sieve pores. CCs, whichare characterized by dense protoplasm, retain a nucleus andnumerous mitochondria and are thought to provide func-tions essential for the survival of SEs via plasmodesmatallinks (Lucas et al., 1993).

The complete physical pathway of sucrose transport fromsource to sink is not completely elucidated for any plant,and important differences may exist among species. Fromthe point of sucrose synthesis in the mesophyll, the route tothe SE involves several cell types: neighboring mesophyllcells, bundle-sheath cells, phloem parenchyma, and CCs.Cell-to-cell movement of sucrose is considered to occur viaplasmodesmata from the point of synthesis up to the SE/CCcomplex which, in many species, is not well connected tothe surrounding cells (Gamalei, 1989). Two principal routesfor the delivery of sucrose into the SE/CC complex havebeen proposed: (1) transporter-mediated export from meso-phyll cells, apoplasmic diffusion through the cell-wall contin-uum, and subsequent carrier-mediated transport across theSE/CC plasma membrane; and (2) direct symplasmic cell-to-cell diffusion via plasmodesmata. The extent to whichplants utilize either of these pathways and whether plantscan switch between these pathways is a question currentlyunder active investigation.

Apoplasmic Transport

Plants that primarily utilize an apoplasmic phloem loadingmechanism require the transmembrane transport of sucroseand other solutes into the phloem. For such plants, as sche-matized in Figure 1, we can predict a minimum of five su-crose transport activities along the translocation path. Inleaves, the first transport step must be release of sucroseinto the cell wall directly from the mesophyll cell (Figure 1,transporter 1). Mechanistically, this first transporter could bea facilitator or an antiporter. Such sucrose efflux systemshave been described biochemically (see Delrot, 1989; Laloiet al., 1993). Subsequently, at least one transporter is re-quired for uptake into the phloem (Figure 1, transporter 2).These loading processes are required at various stages ofdevelopment, such as during germination for sugar exportfrom leaves or for mobilization of stored carbon, events thatmight require distinct transporters. Reuptake of sucrosealong the translocation pathway is necessary to allow soluteexchange with the phloem, for example, in stems (Figure 1,transporter 3; Minchin and Thorpe, 1987).

In sink tissue, unloading can occur either by transmem-brane export of sucrose (Figure 1, transporter 4) or throughplasmodesmata. Sucrose efflux transporters involved inphloem unloading have been postulated to function as facil-itators or as proton antiporters (Walker et al., 1995). Sucrosein the apoplast of sink tissue can be taken up directly (Figure1, transporter 5) or through the hydrolysis of sucrose intoglucose and fructose by invertase followed by hexose up-take (Figure 1, transporter 6).

Symplasmic Transport

Figure 1 also schematizes the possibility that each transportprocess outlined above could alternatively take place sym-plasmically. Based on the systemic movement of plant virusin phloem, plasmodesmal connections between the SE/CCcomplex and surrounding cells are present even in Solana-ceous species which are classified as type 2a (van Bel and

Figure 1. Long-Distance Sugar Transport by the Phloem.

From its point of synthesis in the mesophyll, sucrose may be loadedinto the SE/CC complex either through plasmodesmata or via theapoplasm. The apoplasmic loading mechanism requires sucrose ex-port (1) from the mesophyll or the vascular parenchyma and re-uptake (2) into the SE/CC complex. Hydrostatic pressure drivesphloem sap movement toward sink tissue. Passive leakage can takeplace along the path (indicated by wavy arrows). Reuptake (3) alsooccurs along the path of the phloem. Apoplasmic phloem or post-phloem unloading necessitates a sucrose exporter at the sink tissue(4). Import of sucrose and other solutes into sink tissue may occurthrough plasmodesmata or sucrose transporters (5). In addition toplasmodesmal and transporter-mediated uptake, cells in the sinkmay take up sucrose, subsequent to its hydrolysis by an apoplasmicinvertase, as hexoses (6). The vacuolar transport system couldconsist of a H1/sucrose antiporter for uptake and a uniporter forrelease.

Sugar Transport and Sugar Sensing 709

Gamalei, 1992). To achieve the pressure difference requiredfor 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 begated open by endogenous plant factors. Symplasmicroutes have been identified in the root by determination ofdye coupling by using small cytoplasmic fluorescent dyes(Wright and Oparka, 1997).

Interestingly, despite the presence of plasmodesmataalong the entire length of the transport path, efflux occursonly in restricted regions, such as the region behind the roottip. It is possible that plants may utilize different mecha-nisms of phloem unloading in different tissues or may evenbe able to switch between apoplasmic and symplasmicmechanisms depending on growth conditions. Besidesthese plasma membrane transporters, uptake and releasesystems are required for subcellular compartments, espe-cially the vacuole, which serves as a transient buffer for sug-ars and other metabolites (Figure 1; Marty, 1999, in thisissue).

The Physics of Mass Flow

Uptake of sucrose into the SEs is believed to increase thehydrostatic pressure difference between the ends of thephloem conduits so as to drive the mass flow movement ofthe phloem sap. The velocity of translocation in the phloemis relatively high, ranging from 0.5 to 3 m hr

2

1

(Köckenbergeret al., 1997). The phloem, then, contains an osmotic pumpwhose efficacy rests primarily on the cooperative functionsof three types of plasma membrane proteins: (1) H

1

/sucrosesymporters that accumulate osmotically active sucrose tomolar concentrations in the phloem; (2) H

1

-ATPases thatprovide the energy necessary for active transport; and (3)water transporters, potentially aquaporins, that take up wa-ter derived from the xylem (for a discussion of aquaporins,see Chrispeels et al., 1999, in this issue; for a discussion ofH

1

-ATPases, see Sze et al., 1999, in this issue). Osmolytesother than sucrose, such as potassium and amino acids,also contribute to the driving force of the sap flow, and thesimultaneous withdrawal of osmolytes and water at sink tis-sues further increases hydrostatic pressure differences. Anessential prerequisite for the resulting osmotic pump is thatthe SE/CC complex be osmotically isolated from neighbor-ing cells. Specifically, if phloem cells are connected toneighboring mesophyll cells, such intercellular connectionsmust be tightly regulated. Differences in the connectivityamong different cell types in leaves are in fact discernableand result in the classification of plants as either apoplasmicor symplasmic loaders (van Bel, 1993). Furthermore, evi-dence for the regulated opening of plasmodesmata hasbeen provided (Oparka and Prior, 1992; Oparka et al.,1994).

Of the numerous components required for long-distancephotoassimilate transport (Figure 1), only proton-coupled

sucrose and monosaccharide uptake transporters havebeen identified at the molecular level. It is unknown whethersucrose release is also proton coupled or if the release carri-ers are related in sequence to the uptake transporters (Wardet al., 1998). The sucrose binding protein, which in manycases colocalizes with the sucrose transporter, might be re-sponsible for facilitated diffusion of sucrose (Overvoorde etal., 1996; Harrington et al., 1997) and may represent a sec-ond sucrose transporter class.

SUGAR TRANSPORTERS

Monosaccharide Transporters

Monosaccharide transport activities have also been identi-fied in a variety of plant species (Maynard and Lucas, 1982;Getz et al., 1987; Gogarten and Bentrup, 1989; Tubbe andBuckhout, 1992). Substrates that are efficiently transportedinclude

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 trans-port (Gogarten and Bentrup, 1989). Plant monosaccharidetransporters were first cloned from

Chlorella kessleri

byexploiting their rapid induction following the addition ofhexoses to the growth medium. Specifically, differentialscreening of cDNAs from autotrophic versus heterotrophiccells enabled the cloning of the first plant hexose trans-porter gene (

HUP1

; Sauer and Tanner, 1989). In contrast tothe yeast hexose transporters (HXTs), which function asuniporters, the

C. kessleri

hexose transporter is a sym-porter (Sauer et al., 1990a; Aoshima et al., 1993). Despitethis difference in the transport mechanism, yeast and

C.kessleri

transporter genes are homologous, encoding pro-teins composed of 12 putative membrane-spanning do-mains. At least three hexose transporters are known toexist in

C. kessleri

(Table 1). The functional proof that thesegenes encode hexose transporters derives from heterolo-gous expression of the plant genes in yeast (Sauer et al.,1990a).

The cloning of higher plant monosaccharide transporterswas accomplished by heterologous hybridization (Sauer etal., 1990b). The monosaccharide transporter family in Arabi-dopsis, 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 protonsymporter (Aoshima et al., 1993; Boorer et al., 1994). Theexpression patterns of various plant monosaccharide trans-porters suggest that these membrane proteins function inhexose uptake in sink tissues (Sauer and Stadler, 1993).Analysis of expression also shows that plant monosaccha-ride transporters are highly regulated, such as in responseto pathogen infection or after wounding (Truernit et al.,

710 The Plant Cell

1996), thus allowing flexible reallocation of fixed carbon. Theexpression of monosaccharide transporters in sink tissuealso supports an apoplasmic mechanism for phloem orpostphloem unloading (Sauer and Stadler, 1993). In thisway, plant sink tissues may acquire hexose in a manner sim-ilar to that employed by yeast that use an extracellular

invertase to hydrolyze external sucrose. One requirementfor this mechanism in plants is the coexpression of plantinvertases and monosaccharide transporters (Ehness andRoitsch, 1997).

The sugar permease family in yeast contains 34 genes(André, 1995; Nelissen et al., 1997; reviewed in Boles andHollenberg, 1997), with 20 members belonging to the HXTsubfamily (

HXT1-17

,

GAL2

,

SNF3

, and

RGT2

). The individualHXTs differ considerably with respect to their kinetic proper-ties, with

K

m

values for glucose uptake ranging from 1 mM forHXT7 to 100 mM for HXT1 (Reifenberger et al., 1997). The ex-pression of

HXT

genes is regulated by glucose concentra-tion, and the transporter homologs SNF3 and RGT2 functionas sensors (see below).

Sucrose Transporters and

SUT

Genes

Sucrose transport activities have been described in a widevariety of systems (Maynard and Lucas, 1982; Giaquinta,1983; reviewed in Bush, 1993; Ward et al., 1998). To cloneplant sucrose transporters, a yeast strain was generatedthat was unable to hydrolyze extracellular sucrose but wascapable of metabolizing internal sucrose due to the pres-ence of a plant-derived sucrose synthase activity (Figure2). The strain was, furthermore, deficient in maltose utili-zation, a safeguard against side activities of the yeast-endogenous maltose transport systems. The resultingyeast cells grow inefficiently on media containing 0.5%sucrose as the sole carbon source and were consequentlyused to clone plant sucrose transporters from spinach andpotato by functional complementation (Riesmeier et al.,1992, 1993).

Detailed transport studies using radioactive tracers havesubsequently allowed determination of kinetic properties,pH optima, inhibitor sensitivity, and substrate specificity ofvarious

SUT

genes. All plant sucrose transporters identifiedso far are energy dependent and sensitive to protono-phores, indicating that they function as proton symporters.The

K

m

for sucrose, in all cases, was found to be in therange of 1 mM (Riesmeier et al., 1993; Lemoine et al., 1996).Similar results were obtained for the Arabidopsis sucrosetransporters SUC1 and SUC2.

The

SUT

genes encode highly hydrophobic proteins. Theyconsist of 12 membrane-spanning domains and are dis-tantly related to the hexose transporter family found in manyorganisms, such as yeast and plants (reviewed in Ward etal., 1997; Rentsch et al., 1998). As for the monosaccharidetransporters, sucrose transporters have been characterizedby the two-electrode voltage clamp method in

X. laevis

oo-cytes (Boorer et al., 1996; Zhou et al., 1997). The stoichiom-etry of H

1

/sucrose cotransport was determined to be 1:1,consistent with stoichiometric estimates obtained earlier inplasma membrane vesicles from sugar beet leaves (Bush,1990; Slone et al., 1991). The

SUT

family thus correspondsto the protonophore-sensitive high-affinity component of

Table 1.

Monosaccharide Transporter Gene Family in Plants

Species Gene NameAccessionNumber

Length(Amino Acids)

Arabidopsis thaliana

AtSTP1 X55350 522AtSTP3 AJ002399 514AtSTP4 X66857 514ERD6 D89051 496AtSUGTRPR Z50752 734ATAP22.19 Z99708 493Fi8E5.100

a

AL022603 508T10M13.6

a

AF001308 513T01O24.7

a

AC002335 521F3O9 AC006341 518T20F21.7 AC006068 522AtFCA6 Z97341 582F1N21.10 AC002130 453T22H22.15 AC005388 483T4B21.9 AF118223 434T4B21.10 AF118223 442T7A14.10 AC005322 623T30D6.1 AC006439 508MKD15.12

a

AB007648 514TACK11J9.5

a

AB012239 515T14N5.7

a

AB012239 525F7G19.20

a

AC000106 454F7G19.23

a

AC000106 490F9D12.9

a

AF077407 507F9D12.17

a

AF077407 526F23E12.140

a

AL022604 729

Beta vulgaris

BvMST1 U64902 549BvMST2 U64902 545BvMST3 U43629 490

Chlorella kessleri

CkHUP1 X55349 534CkHUP2 X66855 540CkHUP3 X75440 534

Lycopersicon esculentum

LeMST1 AJ010942 523

Medicago truncatula

MtST1 U38651 518

Nicotiana tabacum

NtMST1 X66856 523

Picea abies

PaMST1 Z83829 513

Petunia

3

hybrida

PMT1 AF061106 510

Prunus armeniaca

APR MST1 AF000952 475

Saccharum

subsp ScfGLUTRAB L21753 518

Ricinus communis

RcSTC L08196 523RcHEX6 L08188 510RcSTA L08197 522

Vicia faba

VfHext Z93775 516

Vitis vinifera

VvHEXTRAN Y09590 519VvHEXOSET AJ001061 519

a

Amino acid sequences are deduced from genomic sequence.


sucrose-uptake kinetics measured in plants (Maynard andLucas, 1982).

CELLULAR LOCALIZATION OF SUT1 IN THE PHLOEM: CCs AND SEs

Based on the transport mechanism (H

1

symport) of SUT1, itwas expected that the transporter would be involved inphloem loading and thus should be present at the plasmamembrane of SE/CC complexes. In situ hybridization indeeddemonstrates that

SUT1

transcripts are phloem associated(Riesmeier et al., 1993), and the promoters of tomato

SUT1

and Arabidopsis

SUC2

genes direct the expression of re-porter genes in leaf, stem, and root phloem (Truernit andSauer, 1995; A. Weise, B. Hirner, J.M. Ward, and W.B.Frommer, unpublished results). Hence, SUT1 (or SUC2 fromArabidopsis) might play a role not only in phloem loading butalso in retrieval of sucrose leaking from sieve tubes along thetranslocation pathway (Figure 1, transporter 3).

To determine expression at the cellular level, immunolocal-ization studies have been applied to five species. In

Plantagomajor

and Arabidopsis, immunofluorescence with specific

antibodies detects SUC2 in CCs (Stadler et al., 1995; Stadlerand Sauer, 1996). By contrast, immunolocalization using im-munofluorescence and silver-enhanced immunogold stain-ing assign SUT1 to the plasma membranes of enucleate SEsof tobacco, potato, and tomato (Kühn et al., 1997). The dif-ferences in sucrose transporter localization observed in Ara-bidopsis and

P. major

compared with tomato, potato, andtobacco 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 re-main to be identified in those species. This would be consis-tent with a stepwise manner of sucrose loading, wherebydifferent carriers operate in CCs (SUC2) as opposed to SEs(SUT1); such a scenario is suggested by physiological anal-yses (Roeckl, 1949).

In situ hybridization experiments at the electron micro-scope level corroborate the localization of SUT proteins toSEs in a remarkable manner. Specifically, Solanaceous

SUT1

mRNA localizes mainly to SEs, primarily at the orificesof plasmodesmata (Kühn et al., 1997). In addition, antisenseinhibition of

SUT1

expression using a CC-specific promoter(from the

RolC

gene) produces strong phenotypic effectsin transgenic plants due to inhibition of sucrose exportfrom leaves (Kühn et al., 1996). These results indicate that

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 inthe plasma membrane (left). A yeast strain (SUSY7; Riesmeier et al., 1992) was constructed in which the cytosolic and extracellular invertaseswere genetically knocked out (middle). A plant sucrose synthase expressed in the cytosol allows growth on sucrose as the sole carbon sourceonly 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 orglucose is shown. fruc, fructose; gluc, glucose; INV, invertase; suc, sucrose; SUC2, invertase gene; SUSY, sucrose synthase; SUT1, sucrosetransporter 1 gene.

712 The Plant Cell

transcription of the

SUT1

gene occurs in CCs and, in con-junction with high turnover rates of mRNA and protein, pro-vide strong evidence for targeting of plant endogenousmRNA, and potentially SUT1 protein, through the plas-modesmata 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 plasmodesmatain apical meristems (Lucas et al., 1995). Similarly, microin-jection studies in

Cucurbita maxima

suggest that an RNAbinding protein identified in phloem sap of that species iscapable of trafficking a number of mRNAs intercellularly, in-cluding the

SUT1

mRNA (Xoconostle-Càzares et al., 1999).The transport of macromolecules such as mRNAs and pro-teins through the microchannels of plasmodesmata requiresmechanisms of unfolding (Kragler et al., 1998; see alsoLazarowitz and Beachy, 1999, in this issue). The function ofplasmodesmata thus seems, in this respect and many oth-ers, to be highly similar to protein import into organellessuch as plastids (see Keegstra and Cline, 1999, in this is-sue), mitochondria, and the endoplasmic reticulum lumen(Vitale and Denecke, 1999, in this issue).

As schematized in Figure 3, two potential pathways forthe targeting of SUT1 can be postulated: either (1) mRNA isguided as part of a nucleoprotein complex along the cyto-skeleton through the phloem plasmodesmata for subse-quent translation; or (2) translation is effected in the CCs andthe protein is deposited within the SE at the plasmodes-matal orifices via the endomembrane system (Overall andBlackman, 1996).

Other phloem proteins alter the size exclusion limit forplasmodesmata and have been shown to move from cell tocell (Balachandran et al., 1997; Ishiwatari et al., 1998; seeLazarowitz and Beachy,1999, in this issue). Various proteinshave been identified in the phloem sap, some of which werefound to be specific for SEs, namely,

b

-amylase, glutare-doxin, 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 ofmost of these proteins in the phloem is unknown, and theirorigins and biosynthesis are not fully understood. The stabil-ity of proteins in the phloem also is generally unknown. Thepresence of ubiquitin in phloem sap may indicate that pro-tein turnover is occurring. Further research is needed to de-termine both protein turnover rates in the phloem sap andprotein import rates.

Mature SEs are living cells despite the fact that they lacka nucleus and many other organelles (Sjölund, 1997). SEsare thought to be dependent on CCs for many cellularfunctions, but the extent of this dependence cannot bedetermined until the actual metabolic capabilities of SEsare better understood. For example, it is not clear whetherSEs contain plasma membrane proton pumps. In CCs, on

the other hand, the expression of the H

1

-ATPase–encod-ing

AtAHA3

gene has been demonstrated (DeWitt andSussman, 1995; see Sze et al., 1999, in this issue). If SEsdo in fact contain an H

1

-ATPase, then the supply of ATPto SEs through plasmodesmata would be presumably im-portant. Consistent with this, phloem sap has been shownto contain concentrations of ATP in the range of 1 mM(Kluge et al., 1970). Additionally, the biogenesis of anyATPase in SEs may be dependent on a supply of mRNA orprotein from CCs, by analogy to SUT1 biogenesis (Kühn etal., 1997). On the other hand, if SEs do not contain a pro-ton pump or if the proton motive force to drive phloemloading is generated only in CCs, then plasmodesmatalconnections are important for the propagation of this driv-ing force (for both electrical coupling and a pathway forprotons) into SEs (van Bel, 1996). In addition, trafficking ofproteins, nucleic acids, and other molecules through plas-modesmata connecting CCs and SEs is important for

Figure 3. SUT1 Biosynthesis.

In Solanaceous species, SUT1 protein is located in the SE plasmamembrane (PM), while transcription occurs in CCs. There are twopossible pathways: SUT1 mRNA may be delivered through plas-modesmata (pd) by an RNA transport mechanism. Alternatively,SUT1 translation may take place in CCs and delivery to SEs may oc-cur via the plasma membrane or endosomal membranes that arecontinuous through plasmodesmata. These pathways are not exclu-sive and could function in parallel. ER, endoplasmic reticulum; sER,sieve element reticulum.


long-distance signaling and to coordinate development atthe whole-plant level in response to environmental factors,nutrients, and water availability (reviewed in Mezitt andLucas, 1996).

IN VIVO EVIDENCE OF SUT1 TRANSPORTER FUNCTION

If sucrose transport mediated by SUT1 is essential forphloem loading, a reduction in transport activity should af-fect carbon partitioning and photosynthesis. In

SUT1

anti-sense plants (Riesmeier et al., 1994; Kühn et al., 1996), leafsucrose and starch content is five- to 10-fold higher than inthe wild type, and the increase in hexose content is evengreater. In addition,

SUT1

antisense plants grow at markedlyretarded rates, producing crinkled leaves that exhibit chloro-sis and accumulation of anthocyanins. Development of thephenotype depends on the length of the photoperiod andlight intensity (Kühn et al., 1996).

A similar accumulation of soluble carbohydrates occurswhen petioles of potato leaves are cold girdled so as toblock phloem translocation (Krapp et al., 1993). Enhancedpartitioning into insoluble carbohydrates is also found in anumber of studies in which heat girdling is used (Grusak etal., 1990, and references therein). A direct comparison ofantisense repression and cold girdling at the ultrastructurallevel demonstrates that both treatments equally evoke theaccumulation of assimilates in all leaf tissues up to theSE/CC complex. However, microscopy reveals that anti-sense inhibition of loading produces a persistently highsugar level throughout the leaf, whereas cold girdling leadsto localized patches containing high sugar and lipid levels(Schulz et al., 1998).

Efflux measurements of carbohydrates from excisedleaves of antisense plants show strong reduction in phloemtransport (Riesmeier et al., 1994). With less carbohydratetransport to sinks, the plants have reduced root growth andtuber yield, phenotypic qualities also observed in transgenicpotato plants in which apoplasmic loading is prevented bythe 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 growthretardation and accumulation of carbohydrates in leaves(Bürkle et al., 1998). The export of recently fixed

14

CO

2

isblocked to almost nondetectable levels even in plants inhib-ited to an intermediate degree, and stronger inhibition wasfound to be lethal. Thus, proton-coupled carriers seem to beindispensable for phloem loading at least in Solanaceousspecies.

Comparable effects were observed in potato plants inwhich

SUT1

was expressed in antisense orientation undercontrol of the CC-specific

RolC

promoter (Kühn et al., 1996).It was, however, not possible to estimate the control coeffi-cient of

SUT1

because the actual amount of SUT1 protein

and sucrose transport activity in the phloem was masked bylow levels of

SUT1

expression presumably in mesophyllcells (Lemoine et al., 1996). The effects observed are there-fore in agreement with expected results that

SUT1

transcrip-tion in CCs is essential for phloem loading.

It remains unclear whether antisense repression also af-fects other members of the

SUT

gene family. A completeanalysis of the role of individual members of the gene familywill require approaches such as the use of “knockout” mu-tants in Arabidopsis. The potential of this approach forstudying transport has been elegantly demonstrated in thecase of potassium channels (Krysan et al., 1996; Gaymardet al., 1998; Hirsch et al., 1998; see also Chrispeels et al.,1999, in this issue). Identification of “knockout” mutants insugar transport is in progress in several research laborato-ries.

SUCROSE TRANSPORTERS IN PHLOEM ANDPOST-PHLOEM UNLOADING

As detailed above, sucrose and hexoses have to be im-ported into sink tissues in roots, pollen, seeds, and else-where. SUT1/SUC2 expression has indeed been found inthese tissues (Riesmeier et al., 1993; Truernit and Sauer,1995). However, the direct function of such phloem-associ-ated H1/sucrose symporters in sink tissues remains un-clear. In several plant species, such as tomato, tobacco,potato, Arabidopsis, P. major, Ricinus communis, Viciafaba, carrot, rice, and pea, additional sucrose transportergenes have been identified, as listed in Table 2 (Gahrtz etal., 1994, 1996; Sauer and Stolz, 1994; Harrington et al.,1997; Hirose et al., 1997; Bürkle et al., 1998; Shakya andSturm, 1998; Tegeder et al., 1999). Several of these genes/proteins show highly specific expression patterns. For ex-ample, in Plantago, SUC1 is expressed in young ovules(Gahrtz et al., 1996), and sucrose transporter transcriptscan be detected in the transfer cells of cotyledons from Vi-cia seeds and pea (Table 2; Harrington et al., 1997; Weberet al., 1997; Tegeder et al., 1999). Interestingly, these carri-ers are also expressed in source leaves, indicating a dualfunction in both phloem loading in leaves and in seed im-port.

Other members of the SUT family are required in unload-ing zones, such as pollen, ovules, and roots. A pollen-specific 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 indirect transport into sink cells or in sucrose retrieval. Thislatter function could control sink strength. Osmotic regula-tion, especially that involved in regulation of phloem or post-phloem unloading, has been discussed in detail by Patrick(1997). Carriers in source tissue for efflux from mesophyll,

714 The Plant Cell

carriers in sink tissues for efflux from phloem and post-phloem, and carriers involved in transient storage in vacu-oles have yet to be identified (Figure 1).

SENSING MECHANISMS IN SUGAR TRANSPORT

A common misconception is that transport processes, es-pecially sugar transport in higher plants, are constitutive andthat biosynthetic activities in the source and catabolic activ-ities in the sink are the key factors controlling allocation ofcarbohydrates. Carbohydrate export rate is increased 10-foldin plants overexpressing pyruvate decarboxylase (Tadege etal., 1998), indicating a large potential for upregulation.Transporters, however, are located in strategic positionsalong metabolic pathways, and thus an effective regulatorymechanism would be to control uptake and efflux directly.

Indeed, there is strong evidence that sugar transport regu-lates the distribution of assimilates within the plant throughvarious macromolecular signaling events.

In the simplest sensing scenario, cells would contain onlyan intracellular receptor for a sugar metabolite. Such cells,whether located in source or sink tissues, could modulatemetabolic processes, such as photosynthesis or carriergene expression. However, due to intracellular metabolism,the effector cells involved in these processes must be ableto differentiate between biosynthesis and transport, andtherefore both intra- and extracellular concentrations of sug-ars need to be sensed. Furthermore, provided that the cellhas a spectrum of carriers of varying affinity and capacity forsugar, extracellular sensors, as shown in Figure 4, can ad-just sugar uptake to match requirements, for example, byinducing high-affinity uptake systems at low external con-centration.

In principle, multiple sensors could be utilized, some for

Table 2. Sucrose Transporter Gene Family in Plants

Species Gene Name Accession Number Length (Amino Acids) Localizationa

Arabidopsis thaliana AtSUC1 X75365 513 SoL, SiL, Ro, Flb, phloemc

AtSUC2 X75382 512 SoL, SiL, Flb, CCsAtSUT2 AC004138 594AtSUT4 AC000132 511AtSUT5 AB016875 492AtSUT8 AC005398 493

Beta vulgaris BvSUT1 X83850 523Daucus carota DcSUT1a Y16766 501 SoL, Stb

DcSUT1b Y16767 501DcSUT2 Y16768 515 St, TP, Fl, Stb

Lycopersiconesculentum

LeSUT1 X82275 510 CCs,b SEb,d, phloemc

Nicotiana tabacum NtSUT1 X82276 507 SoL, Ro, St, SiL, Flb

Oryza sativa OsSUT1 D87819 537 Pa, LS, LBb

Sp, E, Rab

Pisum sativum PsSUT1 AF009922 524 Fl, SoL, Ro, St, Sb

TC, Sp, SCb, TCe, Spe

Plantago major PmSUC1 X84379 503 Fl, V, Fl, St, SiL, SoL, Rob

Young ovulese, CCd

PmSUC2 X75764 510 SoL, St, Ro, Fl, SiL, Frb, CCd

Solanum tuberosum StSUT1 X69165 516 SoL, Ro, Flb

Phloemc, abaxial phloeme

Spinacea oleracea SoLSUT1 X67125 525 SoLb

Ricinus communis RcRSC1 Z31561 533 C, Ro, Hb, E, SiL, SoLb

Vicia faba VfSUT1 Z93774 523 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, ra-chis; 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.


high-affinity responses and others for adaptation to high-flux requirements. Because the plasma membrane has alimited capacity for protein content, this signal may at thesame time lead to an increase in the turnover of low-affinitysystems. Increased turnover of transporters can also becontrolled via an internal sensor, thus decreasing import ifintracellular concentrations exceed the requirements.

Although such regulatory networks could also be effectivein unicellular organisms like yeast or algae, intercellulartransport in higher plants is more complicated. This is be-cause at least two cellular activities—export from one celland import into the adjacent cell—have to be integrated. Lit-tle is known about the molecular mechanisms involved insugar sensing in relation to transport in higher plants. Yeastcould thus serve as a model to help uncover the regulatorynetworks in higher plants.

YEAST AS A MODEL OF SUGAR SIGNALING

The yeast Saccharomyces cerevisiae contains a large spec-trum of .200 integral membrane proteins, many of which

are clearly involved in transmembrane solute transport. Forexample, yeast contains .20 permeases for amino acidtransport (André, 1995; Nelissen et al., 1997) and .20 per-meases for sugar transport (André, 1995; Boles andHollenberg, 1997). The redundancy of transport systemssuggests that complex regulatory networks are absolutelynecessary to control the uptake of nutrients in response to arapidly changing external environment. As shown in Figure5, yeast has developed a two-pronged regulatory system toensure coordination between the supply of sugars from theenvironment and the enzymatic machinery of the cells: (1)the extracellular concentration of sugars is sensed andsugar transport activity is regulated accordingly; (2) sugartransport activity determines the flux of sugars into the cell,

Figure 4. Model for Metabolite Sensing by a Combination of Inter-nal and Membrane-Bound Receptors.

In addition to an internal receptor (see text), membrane-bound re-ceptors are used to sense external sugar concentrations. Such sen-sors trigger a signaling cascade regulating transporter biogenesisand insertion or degradation of proteins at the plasma membrane. Inthis scenario, low sugar concentrations activate a sensor to inducesugar transporter genes (preferentially high affinity). This enablesmore efficient sugar uptake. If, on the other hand, internal sugarconcentration becomes too high, the intracellular sensor may eitherrepress transporter transcription or trigger inactivation via endocyto-sis and degradation of the transporter, thus reducing the influx. In-duction of low-affinity/high-capacity transporters could increaseuptake at higher external concentrations.

Figure 5. Sugar Signal Transduction in Saccharomyces cerevisiae.

HXT-type transporters mediate glucose uptake. Hexokinase PII(HXK2) functions in cytosolic sugar signaling, resulting in transcrip-tional regulation of enzymes and transporters necessary for sugarutilization. The SNF3 (high affinity) and RGT2 (low affinity) glucosereceptors sense the external glucose concentration. These are ho-mologous to HXT-type transporters but contain a C-terminal exten-sion that functions in signaling. The SNF3 and RGT2 signalingpathways affect transcriptional regulation of high-affinity and low-affinity/high-capacity hexose transporter genes, respectively. Seetext for details.

716 The Plant Cell

subsequently generating intracellular signals for furtherregulatory processes.

In S. cerevisiae, multiple transport systems for glucose areregulated at the transcriptional level in response to the ex-ternal concentration of glucose. For example, HXT2 andHXT7 serve as high-affinity glucose transporters and are in-duced only by low levels of glucose but repressed at highlevels, whereas HXT1 functions as a low-affinity transporterand is induced only by high concentrations of glucose(Özcan and Johnston, 1995; Boles and Hollenberg, 1997).Consequently, sensors of extracellular glucose that respondnot only to the kind of carbon source in the medium but alsoto its concentration are required. Once inside the cell, glucoseis phosphorylated by three different kinases: HXK1, HXK2,and GLK1. Finally, it is converted through the glycolyticpathway mainly into ethanol. By contrast to the uptake ofglucose, the regulation of the intracellular glucose concen-tration, phosphorylation, and subsequently, the regulation offlux through glycolysis must be controlled by intracellularsignals (Boles et al., 1997). Furthermore, the expression ofgenes for the utilization of alternative carbon sources like su-crose or galactose, and genes involved in gluconeogenesis,must be shut off in the presence of sufficient amounts of thepreferred carbon source, glucose. This is achieved througha mechanism known as glucose (or carbon) catabolite re-pression (Ronne, 1995; Gancedo, 1998).

The glucose signal that triggers induction of hexose trans-porter genes is generated by the hexose sensors SNF3 andRGT2. On the other hand, the signal that triggers glucose re-pression is somehow connected to the kinase activity ofHXK2 (Ma et al., 1989; Rose et al., 1991). In principle, thereare two possibilities for sensory proteins to detect signalingmolecules. First, sensors might act as receptors, binding thetriggering molecule (e.g., glucose) and transducing the sig-nal via other proteins. Second, sensors might behave likeenzymes or transporters and undergo structural changes soas to monitor the presence or absence of the triggeringcompound directly. Flux measurements by such a sensorprotein would involve the recognition of the velocity of theenzymatic reaction as the ratio of active to free enzyme.

SUGAR SENSORS: A NEW PERSPECTIVEOF TRANSPORTERS

Cell Surface Sugar Sensors

In Escherichia coli, it has long been known that glucosesensing is mediated through glucose phosphorylation dur-ing transport by the phosphotransferase system (Postma etal., 1993). However, no related proteins have yet been de-tected at the plasma membrane of eukaryotic cells. Glucosesensing in yeast seems to involve plasma membrane pro-teins that resemble glucose transporters but additionally

possess large cytoplasmic signaling domains (Özcan et al.,1996a). A similar mechanism has been discovered recentlyfor amino acid sensing (Didion et al., 1998; Iraqui et al.,1999) and might be a general phenomenon not restricted toyeast.

In yeast, SNF3 appears to be a sensor of low levels of glu-cose and mainly regulates expression of high-affinity glu-cose transporters, whereas RGT2 appears to be a sensor ofhigh glucose concentrations that regulates expression oflow-affinity glucose transporters. Additionally, SNF3 is re-quired at high levels of glucose for repression of thehigh-affinity transporters HXT2, HXT6, and HXT7 (Liang andGaber, 1996; Vagnoli et al., 1998). Dominant mutations inboth RGT2 and SNF3 that lead to the generation of signalsin the absence of glucose have been identified (Özcan et al.,1996a). Despite the homology of SNF3 and RGT2 to glucosepermeases, these transmembrane proteins do not seem tobe able to mediate significant glucose transport (Liang andGaber, 1996; Özcan et al., 1998). The large C-terminal ex-tension of SNF3 (303 amino acids) contains two nearly iden-tical repeats of 25 amino acids. One of these repeats is alsopresent in the 218–amino acid C-terminal extension of RGT2and in RAG4 (GenBank accession number Y14849) fromKluyveromyces lactis, which contains a 250–amino acidC-terminal extension and controls the expression of the low-affinity glucose transporter RAG1 (Chen et al., 1992). InNeurospora crassa, the glucose sensor RCO3 contains a119–amino acid C-terminal extension that is dissimilar tothat of SNF3, RGT2, and RAG4 (Madi et al., 1997).

From mutational analyses, yeast glucose sensors appearto function as two interacting domains (Özcan et al., 1998;Vagnoli et al., 1998): the C-terminal extensions that are re-quired for the transmission of the glucose signal, and themembrane-spanning domain necessary for glucose recogni-tion. Because the glucose transporters HXT1 and HXT2 canbe converted into glucose sensors by fusion to the SNF3 Cterminus, it is tempting to speculate that the glucose sen-sors act as glucose transporters with a very low glucosetransport capacity (i.e., too low to support growth of mu-tants that lack glucose transporters), which transduce theglucose signal by a conformational shift during glucosetransport.

Another protein (SSY1) that appears to function as anamino acid sensor has recently been identified in yeast.SSY1 shows the features typical of the SNF3/RGT2 pair: atransmembrane domain related to amino acid permeases, along cytoplasmic extension (in this case located at the N ter-minus of the protein), a low transcription rate, and a lowcoding probability (André, 1995; Didion et al., 1998; Iraqui etal., 1999). SSY1, rather than being a transporter, controlsthe transcription of genes encoding amino acid permeasesand seems to respond to changes in the extracellular con-centration of various amino acids (Didion et al., 1998; Iraquiet al., 1999). The amino acid sequence of the cytoplasmicextension of SSY1 shows no significant similarities to thoseof SNF3 and RGT2.


The only intermediate components so far known to be in-volved in glucose-induced signal transduction in yeast arethe transcription factor RGT1 (Özcan et al., 1996a) andSCFGrr1, a ubiquitin protein ligase complex including theF-box protein GRR1, SKP1, and CDC53 (Li and Johnston,1997; Skowyra et al., 1997). RGT1 is a zinc cluster proteinthat binds directly to promoters of the HXT genes (Özcan etal., 1996b). It acts as a repressor of HXT genes in cellsgrowing without glucose and as a transcriptional activator ofHXT1 in cells growing on high levels of glucose. Repressionof transcription by RGT1 is mediated by the SSN6-TUP1complex, whereas RGT1-mediated induction is independentof these proteins (Figure 5).

The SCFGrr1 protein complex is required for regulation ofRGT1 activity (Özcan and Johnston, 1995) mediating thesignal generated by SNF3 to inhibit the RGT1 repressorfunction in response to low levels of glucose. It is also re-quired for conversion of RGT1 into an activator triggered byRGT2 in the presence of high levels of glucose. Ubiquitina-tion of RGT1 or its regulator may target it for protein degra-dation by the proteasome or directly affect its function.SCFGrr1 complex may be directly stimulated by glucose (Liand Johnston, 1997) or may depend on glucose-activatedkinase because target proteins must be phosphorylated tointeract with GRR1 (Skowyra et al., 1997).

A third sensor protein, MEP2, was recently found in S.cerevisiae to be required for pseudohyphal differentiation inresponse to ammonium limitation (Lorenz and Heitman,1998). Under such conditions, diploid yeast cells differenti-ate into a filamentous, pseudohyphal growth form. MEP2belongs to a family of three closely related ammonium per-meases (Marini et al., 1997). However, unlike the other twomembers of this transporter family, MEP2 serves as both anammonium transporter and a component of an ammoniumsensor. mep2 mutant strains have no defects in growthrates or ammonium uptake, but no longer form pseudohy-phal filaments on media containing limiting amounts of am-monium. Unlike the glucose sensor proteins, however,MEP2 is able to transport its substrate; and as comparedwith the other members of the ammonium permease family,MEP2 contains no significant amino acid extensions on ei-ther its N or C terminus.

Intracellular Sugar Sensing: Enzymes as Sensors

In the triggering reaction of glucose repression in yeast,HXK2 seems to play an important and probably more directrole. Mutations in HXK2 abolish glucose repression of inver-tase and other glucose-repressed genes (Entian, 1980). Thecatalytic and regulatory functions of HXK2 are inseparablefrom glucose repression and inversely correlated to itssugar-phosphorylating activity (Ma et al., 1989; Rose et al.,1991). HXK2 exists in a dimeric–monomeric equilibrium thatis affected by phosphorylation (Randez-Gil et al., 1998). Invivo, dephosphorylation of HXK2 is promoted upon addition

of glucose and is dependent on protein phosphatase 1(CID1/GLC7). A protein kinase involved in phosphorylationof HXK2 has not been found, and it is possible that phos-phorylation of HXK2 could result from substrate-inducedautophosphorylation (Fernández et al., 1988). It has been re-ported that HXK2 has a weak protein kinase activity (Herreroet al., 1989; see above). Moreover, a hxk2 mutant that is notable to undergo phosphorylation can no longer transducethe glucose repression signal (Randez-Gil et al., 1998).These properties might classify HXK2 as an enzyme that ad-ditionally, through its enzymatic function, can act as a sen-sor protein. However, the actual mechanism representingthe on–off switch of the glucose signal is not understood.The glucose repression signal finally inhibits the protein ki-nase SNF1/CAT1, a central element in the regulatory pro-cess (Figure 5) and highly conserved in eukaryotes. Glucoseinhibition of SNF1 depends on protein phosphatase 1(GLC7) and its targeting subunit REG1 (Ludin et al., 1998). Inthe absence of glucose, SNF1 relieves repression by theMIG-SSN6-TUP1 complexes (De Vit et al., 1997) but is alsorequired for the operation of other transcription factors(Gancedo, 1998).

In accordance with HXK2 being a sensor for glucose, thetriggering of glucose repression in yeast is dependent onglucose uptake. However, the repression is not dependenton a specific hexose transporter protein; the glucose repres-sion signal rather correlates with the extent of glucose influxinto cells (Reifenberger et al., 1997). These observations fitvery well with the two-pronged regulatory model describedabove: first, glucose transport activity is adjusted to theextracellular glucose concentration via SNF3 and RGT2;second, glucose transport activity limits provision of intra-cellular glucose, which then might act as a substrate forHXK2 as well as a global glucose signal (Figure 5). In addi-tion, cross-talk between the two different processes mightensure feedback coordination. Such a function has recentlybeen assigned to HXK2 which, in addition to carbon catabo-lite repression, seems also to be involved in glucose induc-tion of HXT gene expression (Randez-Gil et al., 1998).

SUGAR-MEDIATED REGULATION OF SINK AND SOURCE GENES

A large spectrum of genes is regulated by sucrose andmonosaccharides (reviewed in Thomas and Rodriguez, 1994;Koch, 1996). The interplay of regulatory processes intercon-nected with sugar regulation provides the plant with valu-able mechanisms to adjust to environmental conditions andalso to control developmental and physiological processes(e.g., photosynthesis and flowering) (Bernier et al., 1993;Jang and Sheen, 1994; Corbesier et al., 1998). Carbohy-drate-responsive genes can be classified as initiating “feastor famine” responses. Genes for photosynthesis and re-source mobilization are induced by carbohydrate depletion

718 The Plant Cell

(the famine response), whereas increasing sugar concentra-tions stimulate gene expression for utilization and storage(the feast response) independently of location (i.e., in sourceor 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, canspecifically control the expression of a number of genes.Examples of sucrose-regulated genes include an Arabidop-sis leucine zipper gene, ATB2, and the RolC promoter fromAgrobacterium (Smeekens and Rook, 1997; Yokohama etal., 1997). Externally supplied sucrose exceeding concentra-tions of 25 mM lead to a repression of ATB2 transcription(Rook et al., 1998). In sugar beet, high sugar concentrationslead to a repression of sucrose transport activity, correlatingwith a reduction in steady state mRNA levels of BvSUT1(Chiou and Bush, 1998); glucose and fructose affect trans-port activity to a lesser extent. Sucrose can repress tran-scription of photosynthetic genes encoding, for example,chlorophyll a/b binding protein (CAB), ribulose-1,5-bisphos-phate carboxylase/oxygenase (Rubisco), and plastocyanin.Sucrose-uncoupled (sun) mutants have been identified, inwhich sucrose concentration is uncoupled from the repres-sion of such genes (Dijkwel et al., 1996, 1997). Taken to-gether, these studies indicate the presence of sucrose-specific signal perception and transduction processes inwhich both internal and external sensors might be involved.Glucose-specific responses have also been described(Thomas and Rodriguez, 1994; Koch, 1996). Moreover, glu-cose and sucrose seem to control different pathways.Whereas glucose favors cell division, sucrose relates tostorage compound accumulation in seeds (Weber et al.,1998).

A specific hexose-sensing system in which hexokinaseplays 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 andSheen, 1994). Specifically, nonmetabolizable glucose ana-logs (e.g., 6-deoxyglucose or 3-O-methylglucose) that aretaken up into cells but are not metabolized by hexokinasedo not repress gene induction in photosynthetic or glyox-ylate cycles. Only substrates of hexokinase that are takenup and phosphorylated mimic glucose-specific repression(Graham et al., 1994; Jang and Sheen, 1994). Additionally,phosphorylated hexoses do not alter gene expression, butinhibition of hexokinase blocks the 2-deoxyglucose– andmannose-dependent repression.

Thus, hexokinase activity per se is involved in sensing, afinding that is further strengthened by studies of transgenicArabidopsis plants in which the expression of the hexo-kinase-encoding genes AtHXK1 and AtHXK2 had beenprevented (Jang et al., 1997). In antisense plants, the glu-cose-dependent repression of typical famine genes, such asRubisco and CAB, is impaired, thereby leading to reducedsensitivity to high external glucose concentrations. Interest-ingly, Arabidopsis plants overexpressing a yeast HXK gene,

thus bypassing sugar flux through the plant’s endogenoushexokinases, behave similarly to the AtHXK antisense plants(Jang et al., 1997).

These data support a direct role for hexokinase itself insignaling in addition to its kinase activity. However, the situ-ation seems to be more complex. Transgenic tobaccoplants overexpressing a yeast invertase in the cytosol, apo-plasm, or vacuole all accumulate elevated levels of hexoses.However, only in plants with apoplasmic or vacuolar inver-tase expression was gene expression repressed by the ele-vated sugar content (Herbers et al., 1996). Furthermore,because the introduction of sugar phosphates into cells byelectroporation does not modify the expression of carbohy-drate-responsive genes (Jang and Sheen, 1994), it seems tobe the flux of sugars undergoing phosphorylation that issensed rather than the mere internal concentration of sugarphosphates.

A more recently identified hexokinase-independent glu-cose-signaling system, schematized in Figure 6, seems tobe preferentially responsible for controlling “feast” andpathogen-related gene expression. In photoautotrophicChenopodium rubrum cell suspensions, the expression ofinvertase and sucrose synthase genes is induced upontreatment with 6-deoxyglucose (Godt et al., 1995; Roitsch etal., 1995). In transgenic Arabidopsis, 3-O-methylglucose ac-tivates a patatin class I promoter fused to b-glucuronidase,which suggests that the sensing mechanism for this non-phosphorylatable analog occurs before hexokinase in thesignaling pathway.

Martin et al. (1997) have identified several Arabidopsismutants with reduced sugar response (rsr) that harbor apatatin promoter–b-glucuronidase construct. These mu-tants, in which the patatin promoter does not respond tosugars, offer a good model for studying hexokinase-inde-pendent sugar sensing. Specifically, despite high intracellu-lar concentrations of hexoses caused by specific enzymeinhibitors, patatin expression was downregulated strongly,thereby supporting a model in which extracellular concentra-tions or fluxes are sensed at the cell exterior (Müller-Röberet al., 1990; Zrenner et al., 1995). As in the case of the hexo-kinase-dependent sensing mechanism, fluxes are more im-portant than steady state levels of carbohydrate to initiate aresponse. Studies on sugar-induced pathogen-related genes,moreover, provide strong evidence for the existence ofsensing mechanisms, located at the plasma membrane,which might correspond to the RGT2/SNF3-type sensingsystem present in yeast.

Despite the central importance of sugars as key regula-tors of gene expression, very little is known about the signaltransduction mechanisms in which they take part. Severalstudies have provided evidence that mechanisms similar toyeast phosphorylation events are involved in sugar-specificsignal transduction cascades. Several kinase genes havebeen found in plants with homology to SNF1 of which somecomplement the snf1 yeast mutant. In vivo function hasbeen demonstrated in transgenic potato plants expressing


an SNF1-related protein kinase gene in antisense orientationsuch that a decrease in sucrose synthase expression is ob-served in tubers (Halford and Hardie, 1998). Rubisco generepression and invertase gene induction by sugars involvethe action of both kinases and phosphatases (Ehness et al.,1997). Also, in the case of the regulation of sporamin andb-amylase gene expression, the involvement of proteinphosphorylation is likely inasmuch as treatment with specificinhibitors 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 transportcan be adapted to the changing needs of the plant. Indeed,

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-methyl-glucose can be transported but are not substrates for hexokinase; therefore, signal pathways requiring hexokinase activity are not triggered bythese 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-dependentpathway. Sucrose can be metabolized and hexoses used in the hexokinase-dependent pathway.

720 The Plant Cell

comparison of the transport activities in developing versusmature leaves has shown that H1/sucrose cotransport is differ-entially active and develops during leaf maturation (Lemoineet al., 1992). Hormones such as auxin and cytokinin havelong 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). Inbroad bean, the direct promotion of assimilate export by theapplication of gibberellin was reported (Aloni et al., 1986).Phloem loading in isolated bundles of celery seems to be di-rectly affected by gibberellin and auxin (Daie et al., 1986).However, a principle problem of such studies is the difficultyto differentiate between effects operating within the net-work.

Proton-coupled sugar transporters can be regulated intwo major ways: (1) indirectly by regulating H1-ATPase ac-tivity, or (2) more specifically by controlling the expression ofsugar transporters at the transcriptional and post-transcrip-tional levels. Several factors are known to regulate ATPaseactivity and/or transcription: fusicoccin (Oecking et al.,1997; Baunsgaard et al., 1998), salicylic acid (Bourboulouxet al., 1998), and anaerobiosis, which probably acts at thelevel of ATP supply for the H1-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 twoplasma membrane ATPases, LHA4 and LHA2 (Mito et al.,1996). This induction is dependent on sugar uptake and me-tabolism, inasmuch as mannitol and 3-O-methylglucosehave no effect. These results suggest that the induction ofexpression of H1-ATPase genes by metabolizable sugarsmay be part of a generalized cellular response to promotecell growth in the presence of abundant carbon sources(Mito et al., 1996).

Potato SUT1 and Arabidopsis AtSUC2 are expressed insource and sink tissues (Riesmeier et al., 1993; Truernit andSauer, 1995). The expression of the sucrose transporterSUT1 is diurnally regulated at both the mRNA and proteinlevel (Kühn et al., 1997), in accordance with diurnal regula-tion of export rates from leaves (Heinecke et al., 1994).SUT1 mRNA and protein levels can, furthermore, be in-duced by the addition of auxin and cytokinin to detachedleaves (C. Kühn and W.B. Frommer, unpublished results),whereas no such effect was observed for either of the twomajor H1-ATPase genes expressed in potato leaves (Harmset al., 1994). Sucrose itself was shown to be involved in reg-ulating sucrose transporter activity, potentially at the tran-scriptional level (Chiou and Bush, 1998).

Inhibitor experiments indicate that SUT1 activity is alsoregulated at the post-translational level by phosphorylation(Roblin et al., 1998). Protein kinase activities, which might beresponsible for phosphorylation of sucrose transporters inthe SEs, have been detected in the phloem sap (Nakamuraet al., 1993). As described in yeast, sugars may also regulatethe stability of transporters (Jiang et al., 1997). Inhibition

studies using cycloheximide show that the half-life of SUT1is in the range of a few hours (Kühn et al., 1997). This highturnover rate may indicate specific mechanisms controllingthe number of active carriers in the plasma membrane andmay suggest involvement of endocytosis, as in the case ofmammalian glucose transporters and yeast amino acid per-meases (Hein et al., 1995; Thorens, 1996).

Concerning monosaccharide transport, no clear functionhas been demonstrated using antisense or “knockout” strat-egies. Very little is also known about its regulation. Coordi-nated regulation of mRNAs for extracellular invertase and amonosaccharide transporter in C. rubrum has been de-scribed (Ehness and Roitsch, 1997). Because sucrose syn-thase and invertase gene expression is regulated by sugars,one may expect a complex network coordinating uptake ofboth monosaccharides and sucrose with the metabolicevents involving both extracellular and intracellular sensorsas sketched in Figure 6.

PLANT TRANSPORTER FAMILIES IN SUGAR SENSING

Are there known members of the plant transporter familiesthat could be sensors? Indications, as presented above,suggest that transporters might be involved in sensing hex-oses (Figure 6; Martin et al., 1997). As described above,such sensors in yeast often contain additional cytosolic do-mains that are thought to play a role in transmitting the sig-nal. Analysis of the plant monosaccharide transporter MSTfamily (Table 1) indicates that the Arabidopsis genome con-tains at least 26 MST genes. Although none of the predictedAtMST proteins share obvious similarities with the C-termi-nal extensions found in the yeast RGT2 and SNF3, two Ara-bidopsis genes (AtSUGTRPR and F23E12.140; Table 1) thatare closely related to each other contain extended centralloops. Additionally, one member of the tomato and Arabi-dopsis SUT family is characterized by the presence of a longcentral loop predicted to be cytosolic (L. Barker, C. Kühn, B.Hirner, E. Boles, H. Hellmann, A. Weise, J.M. Ward, andW.B. Frommer, unpublished results). The availability of thefull sequence from Arabidopsis will provide access for moredetailed analysis. Because the putative tomato sucrose sen-sor colocalizes with SUT1 and because no sucrose trans-port activity is detectable, one might speculate that it isinvolved in controlling the expression and turnover of SUT1in SEs (Figure 7).

Because transporter-like sensors have also been identi-fied for amino acids and ammonium, one may speculate thatthe transporter families also contain respective sensors.Within the large amino acid transporter families, no ho-mologs containing large cytosolic domains similar to SSY1have been found to date (Fischer et al., 1998). Because inthe putative yeast ammonium sensor MEP2 no extendedloops or other features that specify it as a sensor have beenidentified and because it represents a functional transport


protein, sequence comparisons seem inappropriate to iden-tify plant homologs. None of the plant ammonium transport-ers that are highly related to the yeast MEP genes containextended cytosolic loops (N. von Wirén and W.B. Frommer,unpublished results). In all cases, experimental proof will berequired to identify and characterize putative plant metabo-lite sensors. One approach could be to determine if, in“knockout” mutants, the transcriptional and post-transcrip-tional regulation of other transporters of the same family isaffected.

CONCLUSIONS

In summary, sensors have probably evolved from transport-ers due to their suitability to recognize their substrates. Thiscould have occurred by the addition of a signaling domain toan existing transporter. Plants have to adapt to changingenvironments, and sensing functions are thus essential. Ascompared with yeast, the identification of sensors in plantswill be more difficult, but as in the case of functional expres-sion to identify plant transporters, knowledge from yeastmay serve as a tool to identify plant, and potentially animal,sensors as well.

Yeast complementation has indeed allowed the identifica-tion and characterization of both monosaccharide and su-crose transporters from plants. Both classes of carrier areencoded by large gene families. SUT1, localized in SEs, is

an essential component responsible for phloem loading, aswas shown by antisense inhibition in transgenic potato andtobacco. Physiological studies have shown that plant sugartransport and metabolism are highly regulated by sugars atthe transcriptional and post-transcriptional levels. In yeast,sugar regulation of transporters is controlled by sensors atthe plasma membrane. The availability of genes for mem-bers of the plant MST and SUT family and other phloemsap-specific proteins provides the tools to further exploreand understand the mechanism and regulation of long-dis-tance transport and its role in sugar sensing and regulationin plants.

ACKNOWLEDGMENTS

We are grateful to Bruno André (Université Libre de Bruxelles, Bel-gium) for critical reading of the manuscript and helpful discussion.This work was supported by grants from Deutsche Forschungsge-meinschaft (Grant No. SFB446) and the European Union Biotech-nology Program (Grant Nos. BIO4 CT96-0583 and BIO4 CT96-0311)and by an Alexander von Humboldt fellowship to S.L.

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DOI 10.1105/tpc.11.4.707 1999;11;707-726Plant Cell

and John M. WardSylvie Lalonde, Eckhard Boles, Hanjo Hellmann, Laurence Barker, John W. Patrick, Wolf B. Frommer

The Dual Function of Sugar Carriers: Transport and Sugar Sensing

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