MEMBRANE STRUCTURE AND FUNCTION

The Dual Function of Sugar Carriers: Transport and Sugar Sensing

Correspondence to: Wolf B. Frommer, frommer{at}uni-tuebingen.de (E-mail), 49-7071-29-3287 (fax)

	INTRODUCTION

TOP INTRODUCTION SUGAR TRANSPORT SYSTEMS IN... SUGAR TRANSPORTERS CELLULAR LOCALIZATION OF SUT1... IN VIVO EVIDENCE OF... SUCROSE TRANSPORTERS IN PHLOEM... SENSING MECHANISMS IN SUGAR... YEAST AS A MODEL... SUGAR SENSORS: A NEW... SUGAR-MEDIATED REGULATION OF... HORMONAL REGULATION OF SUGAR... PLANT TRANSPORTER FAMILIES IN... CONCLUSIONS REFERENCES

Sucrose and its derivatives represent the major transport forms of photosynthetically assimilated carbon in plants. Sucrose synthesized in green leaves is exported via the phloem, the long-distance distribution network for assimilates, to supply nonphotosynthetic organs with energy and carbon resources. Sucrose not only functions as a transport metabolite but also contributes to the osmotic driving force for phloem translocation (mass flow) and serves as a signal to activate or repress specific genes in a variety of different tissues.

The long-distance transport of sucrose depends on a family of proteins that act as sucrose carriers. The analysis of transgenic plants impaired in sucrose transporter expression has demonstrated that sucrose transporter1 (SUT1) is essential for sucrose translocation in potato and tobacco. These results, together with the localization of SUT1 to sieve elements (SEs), indicate that phloem loading occurs in SEs by transmembrane uptake of sucrose directly from the apoplasm.

The sucrose transporters identified so far arise from a single gene family. Some of the newly identified members of the family are involved in specific functions, such as nutrition of developing seeds or pollen. Physiological and molecular studies show that sucrose transport is highly regulated at multiple levels of biological organization and in response to changing sucrose concentrations. Thus, one of the most exciting topics in the regulation of sucrose transport is signal perception. By analogy to yeast, in which members of the sugar transport family serve as sugar sensors, we propose that members of the plant sugar transporter family play a direct role in the signal transduction responsible for regulation of sugar transport and, thus, metabolism in general.

	SUGAR TRANSPORT SYSTEMS IN HIGHER PLANTS

TOP INTRODUCTION SUGAR TRANSPORT SYSTEMS IN... SUGAR TRANSPORTERS CELLULAR LOCALIZATION OF SUT1... IN VIVO EVIDENCE OF... SUCROSE TRANSPORTERS IN PHLOEM... SENSING MECHANISMS IN SUGAR... YEAST AS A MODEL... SUGAR SENSORS: A NEW... SUGAR-MEDIATED REGULATION OF... HORMONAL REGULATION OF SUGAR... PLANT TRANSPORTER FAMILIES IN... CONCLUSIONS REFERENCES

Plant Anatomy: Vascular Tissues
Nonphotosynthetic tissues and organs, including the entire below-ground portion of the plant, need to be supplied with energy and fixed carbon. Sugars, synthesized in the mesophyll cells, serve as the major exported photosynthetic product. To accommodate long-distance transport of sugars from source (net exporting) to sink (net importing) organs, a vascular network—the phloem—has evolved in land plants. The most abundant compound in the phloem sap of most plant species is the disaccharide sucrose (Zimmermann and Ziegler 1975 ). For a minority of plant species, the principle translocated sugars fall into two main groups: the sugar alcohols (mannitol and sorbitol) and the raffinose series (raffinose, stachyose, and verbascose) (Zamski and Schnaffer 1996 ). In most cases in which such sugars predominate, however, sucrose is also present.

With the exception of a few well-studied species, our knowledge of phloem sap composition is limited to crude analyses (Zimmermann and Ziegler 1975 ) derived from stem incision experiments in which sugars present as storage compounds in stems may contaminate phloem sap samples. Therefore, accurate and less invasive techniques, such as in vivo NMR (Kockenberger et al. 1997 ) or positron-emitting tracer imaging system (Hayashi et al. 1997 ), will be required for a more accurate understanding of phloem sap composition.

The phloem of angiosperms consists of several types of cells that are closely associated with the xylem within the vascular bundle. The structure and development of the phloem has been reviewed recently (Sjolund 1997 ; Ward et al. 1998 ; Oparka and Turgeon 1999 , in this issue). The actual conduits in phloem consist of two ontogenetically related cell types: companion cells (CCs) and SEs. These two cells are highly modified and well interconnected by plasmodesmata. SEs, for instance, lose their nuclei, vacuoles, and many other organelles during maturation and form tubes of living cells connected by sieve pores. CCs, which are characterized by dense protoplasm, retain a nucleus and numerous mitochondria and are thought to provide functions essential for the survival of SEs via plasmodesmatal links (Lucas et al. 1993 ).

The complete physical pathway of sucrose transport from source to sink is not completely elucidated for any plant, and important differences may exist among species. From the point of sucrose synthesis in the mesophyll, the route to the SE involves several cell types: neighboring mesophyll cells, bundle-sheath cells, phloem parenchyma, and CCs. Cell-to-cell movement of sucrose is considered to occur via plasmodesmata from the point of synthesis up to the SE/CC complex which, in many species, is not well connected to the surrounding cells (Gamalei 1989 ). Two principal routes for the delivery of sucrose into the SE/CC complex have been proposed: (1) transporter-mediated export from mesophyll cells, apoplasmic diffusion through the cell-wall continuum, and subsequent carrier-mediated transport across the SE/CC plasma membrane; and (2) direct symplasmic cell-to-cell diffusion via plasmodesmata. The extent to which plants utilize either of these pathways and whether plants can switch between these pathways is a question currently under active investigation.

Apoplasmic Transport
Plants that primarily utilize an apoplasmic phloem loading mechanism require the transmembrane transport of sucrose and other solutes into the phloem. For such plants, as schematized in Figure 1, we can predict a minimum of five sucrose transport activities along the translocation path. In leaves, the first transport step must be release of sucrose into the cell wall directly from the mesophyll cell (Figure 1, transporter 1). Mechanistically, this first transporter could be a facilitator or an antiporter. Such sucrose efflux systems have been described biochemically (see Delrot 1989 ; Laloi et al. 1993 ). Subsequently, at least one transporter is required for uptake into the phloem (Figure 1, transporter 2). These loading processes are required at various stages of development, such as during germination for sugar export from leaves or for mobilization of stored carbon, events that might require distinct transporters. Reuptake of sucrose along the translocation pathway is necessary to allow solute exchange with the phloem, for example, in stems (Figure 1, transporter 3; Minchin and Thorpe 1987 ).

View larger version (32K): [in this window] [in a new window]   Figure 1. Long-Distance Sugar Transport by the Phloem. From its point of synthesis in the mesophyll, sucrose may be loaded into the SE/CC complex either through plasmodesmata or via the apoplasm. The apoplasmic loading mechanism requires sucrose export (1) from the mesophyll or the vascular parenchyma and reuptake (2) into the SE/CC complex. Hydrostatic pressure drives phloem sap movement toward sink tissue. Passive leakage can take place along the path (indicated by wavy arrows). Reuptake (3) also occurs along the path of the phloem. Apoplasmic phloem or post-phloem unloading necessitates a sucrose exporter at the sink tissue (4). Import of sucrose and other solutes into sink tissue may occur through plasmodesmata or sucrose transporters (5). In addition to plasmodesmal and transporter-mediated uptake, cells in the sink may take up sucrose, subsequent to its hydrolysis by an apoplasmic invertase, as hexoses (6). The vacuolar transport system could consist of a H+/sucrose antiporter for uptake and a uniporter for release.

In sink tissue, unloading can occur either by transmembrane export of sucrose (Figure 1, transporter 4) or through plasmodesmata. Sucrose efflux transporters involved in phloem unloading have been postulated to function as facilitators or as proton antiporters (Walker et al. 1995 ). Sucrose in the apoplast of sink tissue can be taken up directly (Figure 1, transporter 5) or through the hydrolysis of sucrose into glucose and fructose by invertase followed by hexose uptake (Figure 1, transporter 6).

Symplasmic Transport
Figure 1 also schematizes the possibility that each transport process outlined above could alternatively take place symplasmically. Based on the systemic movement of plant virus in phloem, plasmodesmal connections between the SE/CC complex and surrounding cells are present even in Solanaceous species which are classified as type 2a (van Bel and Gamalei 1992 ). To achieve the pressure difference required for mass flow, the plasmodesmata must normally be closed. The systemic spread of silencing signals via the phloem (Voinnet et al. 1998 ) indicates that plasmodesmata can be gated open by endogenous plant factors. Symplasmic routes have been identified in the root by determination of dye coupling by using small cytoplasmic fluorescent dyes (Wright and Oparka 1997 ).

Interestingly, despite the presence of plasmodesmata along the entire length of the transport path, efflux occurs only in restricted regions, such as the region behind the root tip. It is possible that plants may utilize different mechanisms of phloem unloading in different tissues or may even be able to switch between apoplasmic and symplasmic mechanisms depending on growth conditions. Besides these plasma membrane transporters, uptake and release systems are required for subcellular compartments, especially the vacuole, which serves as a transient buffer for sugars and other metabolites (Figure 1; Marty 1999 , in this issue).

The Physics of Mass Flow
Uptake of sucrose into the SEs is believed to increase the hydrostatic pressure difference between the ends of the phloem conduits so as to drive the mass flow movement of the phloem sap. The velocity of translocation in the phloem is relatively high, ranging from 0.5 to 3 m hr^-1 (Kockenberger et al. 1997 ). The phloem, then, contains an osmotic pump whose efficacy rests primarily on the cooperative functions of three types of plasma membrane proteins: (1) H⁺/sucrose symporters that accumulate osmotically active sucrose to molar concentrations in the phloem; (2) H⁺-ATPases that provide the energy necessary for active transport; and (3) water transporters, potentially aquaporins, that take up water derived from the xylem (for a discussion of aquaporins, see Chrispeels et al. 1999 , in this issue; for a discussion of H⁺-ATPases, see Sze et al. 1999 , in this issue). Osmolytes other than sucrose, such as potassium and amino acids, also contribute to the driving force of the sap flow, and the simultaneous withdrawal of osmolytes and water at sink tissues further increases hydrostatic pressure differences. An essential prerequisite for the resulting osmotic pump is that the SE/CC complex be osmotically isolated from neighboring cells. Specifically, if phloem cells are connected to neighboring mesophyll cells, such intercellular connections must be tightly regulated. Differences in the connectivity among different cell types in leaves are in fact discernable and result in the classification of plants as either apoplasmic or symplasmic loaders (van Bel 1993 ). Furthermore, evidence for the regulated opening of plasmodesmata has been provided (Oparka and Prior 1992 ; Oparka et al. 1994 ).

Of the numerous components required for long-distance photoassimilate transport (Figure 1), only proton-coupled sucrose and monosaccharide uptake transporters have been identified at the molecular level. It is unknown whether sucrose release is also proton coupled or if the release carriers are related in sequence to the uptake transporters (Ward et al. 1998 ). The sucrose binding protein, which in many cases colocalizes with the sucrose transporter, might be responsible for facilitated diffusion of sucrose (Overvoorde et al. 1996 ; Harrington et al. 1997 ) and may represent a second sucrose transporter class.

	SUGAR TRANSPORTERS

TOP INTRODUCTION SUGAR TRANSPORT SYSTEMS IN... SUGAR TRANSPORTERS CELLULAR LOCALIZATION OF SUT1... IN VIVO EVIDENCE OF... SUCROSE TRANSPORTERS IN PHLOEM... SENSING MECHANISMS IN SUGAR... YEAST AS A MODEL... SUGAR SENSORS: A NEW... SUGAR-MEDIATED REGULATION OF... HORMONAL REGULATION OF SUGAR... PLANT TRANSPORTER FAMILIES IN... CONCLUSIONS REFERENCES

Monosaccharide Transporters
Monosaccharide transport activities have also been identified in a variety of plant species (Maynard and Lucas 1982 ; Getz et al. 1987 ; Gogarten and Bentrup 1989 ; Tubbe and Buckhout 1992 ). Substrates that are efficiently transported include ß-D-glucose, 3-O-methyl ß-D-glucose, 2-deoxy ß-D-glucose, -D-mannose, and ß-D-fructose, whereas ß-L-glucose and ß-D-ribose are poor substrates for transport (Gogarten and Bentrup 1989 ). Plant monosaccharide transporters were first cloned from Chlorella kessleri by exploiting their rapid induction following the addition of hexoses to the growth medium. Specifically, differential screening of cDNAs from autotrophic versus heterotrophic cells enabled the cloning of the first plant hexose transporter gene (HUP1; Sauer and Tanner 1989 ). In contrast to the yeast hexose transporters (HXTs), which function as uniporters, the C. kessleri hexose transporter is a symporter (Sauer et al. 1990a ; Aoshima et al. 1993 ). Despite this difference in the transport mechanism, yeast and C. kessleri transporter genes are homologous, encoding proteins composed of 12 putative membrane-spanning domains. At least three hexose transporters are known to exist in C. kessleri (Table 1). The functional proof that these genes encode hexose transporters derives from heterologous expression of the plant genes in yeast (Sauer et al. 1990a ).

The cloning of higher plant monosaccharide transporters was accomplished by heterologous hybridization (Sauer et al. 1990b ). The monosaccharide transporter family in Arabidopsis, as shown in Table 1, contains in excess of 26 genes, and multiple genes have been isolated from other species. STP1 was characterized by heterologous expression in Xenopus laevis oocytes and shown to function as a proton symporter (Aoshima et al. 1993 ; Boorer et al. 1994 ). The expression patterns of various plant monosaccharide transporters suggest that these membrane proteins function in hexose uptake in sink tissues (Sauer and Stadler 1993 ). Analysis of expression also shows that plant monosaccharide transporters are highly regulated, such as in response to pathogen infection or after wounding (Truernit et al. 1996 ), thus allowing flexible reallocation of fixed carbon. The expression of monosaccharide transporters in sink tissue also supports an apoplasmic mechanism for phloem or postphloem unloading (Sauer and Stadler 1993 ). In this way, plant sink tissues may acquire hexose in a manner similar to that employed by yeast that use an extracellular invertase to hydrolyze external sucrose. One requirement for this mechanism in plants is the coexpression of plant invertases and monosaccharide transporters (Ehness and Roitsch 1997 ).

The sugar permease family in yeast contains 34 genes (Andre 1995 ; Nelissen et al. 1997 ; reviewed in Boles and Hollenberg 1997 ), with 20 members belonging to the HXT subfamily (HXT1-17, GAL2, SNF3, and RGT2). The individual HXTs differ considerably with respect to their kinetic properties, with K_m values for glucose uptake ranging from 1 mM for HXT7 to 100 mM for HXT1 (Reifenberger et al. 1997 ). The expression of HXT genes is regulated by glucose concentration, and the transporter homologs SNF3 and RGT2 function as sensors (see below).

Sucrose Transporters and SUT Genes
Sucrose transport activities have been described in a wide variety of systems (Maynard and Lucas 1982 ; Giaquinta 1983 ; reviewed in Bush 1993 ; Ward et al. 1998 ). To clone plant sucrose transporters, a yeast strain was generated that was unable to hydrolyze extracellular sucrose but was capable of metabolizing internal sucrose due to the presence of a plant-derived sucrose synthase activity (Figure 2). The strain was, furthermore, deficient in maltose utilization, a safeguard against side activities of the yeast-endogenous maltose transport systems. The resulting yeast cells grow inefficiently on media containing 0.5% sucrose as the sole carbon source and were consequently used to clone plant sucrose transporters from spinach and potato by functional complementation (Riesmeier et al. 1992 , Riesmeier et al. 1993 ).

View larger version (21K): [in this window] [in a new window]   Figure 2. A Yeast System for Functional Cloning of Sucrose Transporters. Wild-type yeast (Saccharomyces cerevisiae) utilizes sucrose primarily through activities of an extracellular invertase and hexose transporters in the plasma membrane (left). A yeast strain (SUSY7; Riesmeier et al. 1992 ) was constructed in which the cytosolic and extracellular invertases were genetically knocked out (middle). A plant sucrose synthase expressed in the cytosol allows growth on sucrose as the sole carbon source only if a sucrose transporter is expressed in the plasma membrane (right). The ability (+) or inability (-) of the yeast strains to grow on sucrose or glucose is shown. fruc, fructose; gluc, glucose; INV, invertase; suc, sucrose; SUC2, invertase gene; SUSY, sucrose synthase; SUT1, sucrose transporter 1 gene.

Detailed transport studies using radioactive tracers have subsequently allowed determination of kinetic properties, pH optima, inhibitor sensitivity, and substrate specificity of various SUT genes. All plant sucrose transporters identified so far are energy dependent and sensitive to protonophores, indicating that they function as proton symporters. The K_m for sucrose, in all cases, was found to be in the range of 1 mM (Riesmeier et al. 1993 ; Lemoine et al. 1996 ). Similar results were obtained for the Arabidopsis sucrose transporters SUC1 and SUC2.

The SUT genes encode highly hydrophobic proteins. They consist of 12 membrane-spanning domains and are distantly related to the hexose transporter family found in many organisms, such as yeast and plants (reviewed in Ward et al., 1997; Rentsch et al. 1998 ). As for the monosaccharide transporters, sucrose transporters have been characterized by the two-electrode voltage clamp method in X. laevis oocytes (Boorer et al. 1996 ; Zhou et al. 1997 ). The stoichiometry of H⁺/sucrose cotransport was determined to be 1:1, consistent with stoichiometric estimates obtained earlier in plasma membrane vesicles from sugar beet leaves (Bush 1990 ; Slone et al. 1991 ). The SUT family thus corresponds to the protonophore-sensitive high-affinity component of sucrose-uptake kinetics measured in plants (Maynard and Lucas 1982 ).

	CELLULAR LOCALIZATION OF SUT1 IN THE PHLOEM: CCs AND SEs

TOP INTRODUCTION SUGAR TRANSPORT SYSTEMS IN... SUGAR TRANSPORTERS CELLULAR LOCALIZATION OF SUT1... IN VIVO EVIDENCE OF... SUCROSE TRANSPORTERS IN PHLOEM... SENSING MECHANISMS IN SUGAR... YEAST AS A MODEL... SUGAR SENSORS: A NEW... SUGAR-MEDIATED REGULATION OF... HORMONAL REGULATION OF SUGAR... PLANT TRANSPORTER FAMILIES IN... CONCLUSIONS REFERENCES

Based on the transport mechanism (H⁺ symport) of SUT1, it was expected that the transporter would be involved in phloem loading and thus should be present at the plasma membrane of SE/CC complexes. In situ hybridization indeed demonstrates that SUT1 transcripts are phloem associated (Riesmeier et al. 1993 ), and the promoters of tomato SUT1 and Arabidopsis SUC2 genes direct the expression of reporter genes in leaf, stem, and root phloem (Truernit and Sauer 1995 ; A. Weise, B. Hirner, J.M. Ward, and W.B. Frommer, unpublished results). Hence, SUT1 (or SUC2 from Arabidopsis) might play a role not only in phloem loading but also in retrieval of sucrose leaking from sieve tubes along the translocation pathway (Figure 1, transporter 3).

To determine expression at the cellular level, immunolocalization studies have been applied to five species. In Plantago major and Arabidopsis, immunofluorescence with specific antibodies detects SUC2 in CCs (Stadler et al. 1995 ; Stadler and Sauer 1996 ). By contrast, immunolocalization using immunofluorescence and silver-enhanced immunogold staining assign SUT1 to the plasma membranes of enucleate SEs of tobacco, potato, and tomato (Kuhn et al. 1997 ). The differences in sucrose transporter localization observed in Arabidopsis and P. major compared with tomato, potato, and tobacco may be due to differences in loading mechanisms. However, the transporters studied in Arabidopsis and P. major do not appear to be orthologs of SUT1, which may remain to be identified in those species. This would be consistent with a stepwise manner of sucrose loading, whereby different carriers operate in CCs (SUC2) as opposed to SEs (SUT1); such a scenario is suggested by physiological analyses (Roeckl 1949 ).

In situ hybridization experiments at the electron microscope level corroborate the localization of SUT proteins to SEs in a remarkable manner. Specifically, Solanaceous SUT1 mRNA localizes mainly to SEs, primarily at the orifices of plasmodesmata (Kuhn et al. 1997 ). In addition, antisense inhibition of SUT1 expression using a CC-specific promoter (from the RolC gene) produces strong phenotypic effects in transgenic plants due to inhibition of sucrose export from leaves (Kuhn et al. 1996 ). These results indicate that transcription of the SUT1 gene occurs in CCs and, in conjunction with high turnover rates of mRNA and protein, provide strong evidence for targeting of plant endogenous mRNA, and potentially SUT1 protein, through the plasmodesmata that interconnect CCs and SEs.

These data may seem surprising at first sight; however, trafficking of RNA is known to occur in Drosophila and X. laevis during oogenesis and in neurons (St. Johnston 1995 ). In maize, moreover, mRNA and protein produced from the KNOTTED-1 gene are transported through plasmodesmata in apical meristems (Lucas et al. 1995 ). Similarly, microinjection studies in Cucurbita maxima suggest that an RNA binding protein identified in phloem sap of that species is capable of trafficking a number of mRNAs intercellularly, including the SUT1 mRNA (Xoconostle-Cazares et al. 1999 ). The transport of macromolecules such as mRNAs and proteins through the microchannels of plasmodesmata requires mechanisms of unfolding (Kragler et al. 1998 ; see also Lazarowitz and Beachy 1999 , in this issue). The function of plasmodesmata thus seems, in this respect and many others, to be highly similar to protein import into organelles such as plastids (see Keegstra and Cline 1999 , in this issue), mitochondria, and the endoplasmic reticulum lumen (Vitale and Denecke 1999 , in this issue).

As schematized in Figure 3, two potential pathways for the targeting of SUT1 can be postulated: either (1) mRNA is guided as part of a nucleoprotein complex along the cytoskeleton through the phloem plasmodesmata for subsequent translation; or (2) translation is effected in the CCs and the protein is deposited within the SE at the plasmodesmatal orifices via the endomembrane system (Overall and Blackman 1996 ).

View larger version (151K): [in this window] [in a new window]   Figure 3. SUT1 Biosynthesis. In Solanaceous species, SUT1 protein is located in the SE plasma membrane (PM), while transcription occurs in CCs. There are two possible pathways: SUT1 mRNA may be delivered through plasmodesmata (pd) by an RNA transport mechanism. Alternatively, SUT1 translation may take place in CCs and delivery to SEs may occur via the plasma membrane or endosomal membranes that are continuous through plasmodesmata. These pathways are not exclusive and could function in parallel. ER, endoplasmic reticulum; sER, sieve element reticulum.

Other phloem proteins alter the size exclusion limit for plasmodesmata and have been shown to move from cell to cell (Balachandran et al. 1997 ; Ishiwatari et al. 1998 ; see Lazarowitz and Beachy 1999 , in this issue). Various proteins have been identified in the phloem sap, some of which were found to be specific for SEs, namely, ß-amylase, glutaredoxin, thioredoxin, cyclophilin, protein kinases, ubiquitin, and P-protein PP2a (Schobert et al. 1995 ; Wang et al. 1995 ; Sjolund 1997 ; Szederkenyi et al. 1997 ). The role of most of these proteins in the phloem is unknown, and their origins and biosynthesis are not fully understood. The stability of proteins in the phloem also is generally unknown. The presence of ubiquitin in phloem sap may indicate that protein turnover is occurring. Further research is needed to determine both protein turnover rates in the phloem sap and protein import rates.

Mature SEs are living cells despite the fact that they lack a nucleus and many other organelles (Sjolund 1997 ). SEs are thought to be dependent on CCs for many cellular functions, but the extent of this dependence cannot be determined until the actual metabolic capabilities of SEs are better understood. For example, it is not clear whether SEs contain plasma membrane proton pumps. In CCs, on the other hand, the expression of the H⁺-ATPase–encoding AtAHA3 gene has been demonstrated (DeWitt and Sussman 1995 ; see Sze et al. 1999 , in this issue). If SEs do in fact contain an H⁺-ATPase, then the supply of ATP to SEs through plasmodesmata would be presumably important. Consistent with this, phloem sap has been shown to contain concentrations of ATP in the range of 1 mM (Kluge et al. 1970 ). Additionally, the biogenesis of any ATPase in SEs may be dependent on a supply of mRNA or protein from CCs, by analogy to SUT1 biogenesis (Kuhn et al. 1997 ). On the other hand, if SEs do not contain a proton pump or if the proton motive force to drive phloem loading is generated only in CCs, then plasmodesmatal connections are important for the propagation of this driving force (for both electrical coupling and a pathway for protons) into SEs (van Bel 1996 ). In addition, trafficking of proteins, nucleic acids, and other molecules through plasmodesmata connecting CCs and SEs is important for long-distance signaling and to coordinate development at the whole-plant level in response to environmental factors, nutrients, and water availability (reviewed in Mezitt and Lucas 1996 ).

	IN VIVO EVIDENCE OF SUT1 TRANSPORTER FUNCTION

TOP INTRODUCTION SUGAR TRANSPORT SYSTEMS IN... SUGAR TRANSPORTERS CELLULAR LOCALIZATION OF SUT1... IN VIVO EVIDENCE OF... SUCROSE TRANSPORTERS IN PHLOEM... SENSING MECHANISMS IN SUGAR... YEAST AS A MODEL... SUGAR SENSORS: A NEW... SUGAR-MEDIATED REGULATION OF... HORMONAL REGULATION OF SUGAR... PLANT TRANSPORTER FAMILIES IN... CONCLUSIONS REFERENCES

If sucrose transport mediated by SUT1 is essential for phloem loading, a reduction in transport activity should affect carbon partitioning and photosynthesis. In SUT1 antisense plants (Riesmeier et al. 1994 ; Kuhn et al. 1996 ), leaf sucrose and starch content is five- to 10-fold higher than in the wild type, and the increase in hexose content is even greater. In addition, SUT1 antisense plants grow at markedly retarded rates, producing crinkled leaves that exhibit chlorosis and accumulation of anthocyanins. Development of the phenotype depends on the length of the photoperiod and light intensity (Kuhn et al. 1996 ).

A similar accumulation of soluble carbohydrates occurs when petioles of potato leaves are cold girdled so as to block phloem translocation (Krapp et al. 1993 ). Enhanced partitioning into insoluble carbohydrates is also found in a number of studies in which heat girdling is used (Grusak et al. 1990 , and references therein). A direct comparison of antisense repression and cold girdling at the ultrastructural level demonstrates that both treatments equally evoke the accumulation of assimilates in all leaf tissues up to the SE/CC complex. However, microscopy reveals that antisense inhibition of loading produces a persistently high sugar level throughout the leaf, whereas cold girdling leads to localized patches containing high sugar and lipid levels (Schulz et al. 1998 ).

Efflux measurements of carbohydrates from excised leaves of antisense plants show strong reduction in phloem transport (Riesmeier et al. 1994 ). With less carbohydrate transport to sinks, the plants have reduced root growth and tuber yield, phenotypic qualities also observed in transgenic potato plants in which apoplasmic loading is prevented by the overexpression of a yeast invertase in cell walls of leaves (Heinecke et al. 1992 ; Riesmeier et al. 1994 ). In tobacco, antisense repression of SUT1 also leads to dramatic growth retardation and accumulation of carbohydrates in leaves (Burkle et al. 1998 ). The export of recently fixed ¹⁴CO₂ is blocked to almost nondetectable levels even in plants inhibited to an intermediate degree, and stronger inhibition was found to be lethal. Thus, proton-coupled carriers seem to be indispensable for phloem loading at least in Solanaceous species.

Comparable effects were observed in potato plants in which SUT1 was expressed in antisense orientation under control of the CC-specific RolC promoter (Kuhn et al. 1996 ). It was, however, not possible to estimate the control coefficient of SUT1 because the actual amount of SUT1 protein and sucrose transport activity in the phloem was masked by low levels of SUT1 expression presumably in mesophyll cells (Lemoine et al. 1996 ). The effects observed are therefore in agreement with expected results that SUT1 transcription in CCs is essential for phloem loading.

It remains unclear whether antisense repression also affects other members of the SUT gene family. A complete analysis of the role of individual members of the gene family will require approaches such as the use of "knockout" mutants in Arabidopsis. The potential of this approach for studying transport has been elegantly demonstrated in the case of potassium channels (Krysan et al. 1996 ; Gaymard et al. 1998 ; Hirsch et al. 1998 ; see also Chrispeels et al. 1999 , in this issue). Identification of "knockout" mutants in sugar transport is in progress in several research laboratories.

	SUCROSE TRANSPORTERS IN PHLOEM AND POST-PHLOEM UNLOADING

TOP INTRODUCTION SUGAR TRANSPORT SYSTEMS IN... SUGAR TRANSPORTERS CELLULAR LOCALIZATION OF SUT1... IN VIVO EVIDENCE OF... SUCROSE TRANSPORTERS IN PHLOEM... SENSING MECHANISMS IN SUGAR... YEAST AS A MODEL... SUGAR SENSORS: A NEW... SUGAR-MEDIATED REGULATION OF... HORMONAL REGULATION OF SUGAR... PLANT TRANSPORTER FAMILIES IN... CONCLUSIONS REFERENCES

As detailed above, sucrose and hexoses have to be imported into sink tissues in roots, pollen, seeds, and elsewhere. SUT1/SUC2 expression has indeed been found in these tissues (Riesmeier et al. 1993 ; Truernit and Sauer 1995 ). However, the direct function of such phloem-associated H⁺/sucrose symporters in sink tissues remains unclear. In several plant species, such as tomato, tobacco, potato, Arabidopsis, P. major, Ricinus communis, Vicia faba, carrot, rice, and pea, additional sucrose transporter genes have been identified, as listed in Table 2 (Gahrtz et al. 1994 , Gahrtz et al. 1996 ; Sauer and Stolz 1994 ; Harrington et al. 1997 ; Hirose et al. 1997 ; Burkle et al. 1998 ; Shakya and Sturm 1998 ; Tegeder et al. 1999 ). Several of these genes/proteins show highly specific expression patterns. For example, in Plantago, SUC1 is expressed in young ovules (Gahrtz et al. 1996 ), and sucrose transporter transcripts can be detected in the transfer cells of cotyledons from Vicia seeds and pea (Table 2; Harrington et al. 1997 ; Weber et al. 1997 ; Tegeder et al. 1999 ). Interestingly, these carriers are also expressed in source leaves, indicating a dual function in both phloem loading in leaves and in seed import.

Other members of the SUT family are required in unloading zones, such as pollen, ovules, and roots. A 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 in direct transport into sink cells or in sucrose retrieval. This latter function could control sink strength. Osmotic regulation, especially that involved in regulation of phloem or postphloem unloading, has been discussed in detail by Patrick 1997 . Carriers in source tissue for efflux from mesophyll, carriers in sink tissues for efflux from phloem and postphloem, and carriers involved in transient storage in vacuoles have yet to be identified (Figure 1).

	SENSING MECHANISMS IN SUGAR TRANSPORT

TOP INTRODUCTION SUGAR TRANSPORT SYSTEMS IN... SUGAR TRANSPORTERS CELLULAR LOCALIZATION OF SUT1... IN VIVO EVIDENCE OF... SUCROSE TRANSPORTERS IN PHLOEM... SENSING MECHANISMS IN SUGAR... YEAST AS A MODEL... SUGAR SENSORS: A NEW... SUGAR-MEDIATED REGULATION OF... HORMONAL REGULATION OF SUGAR... PLANT TRANSPORTER FAMILIES IN... CONCLUSIONS REFERENCES

A common misconception is that transport processes, especially sugar transport in higher plants, are constitutive and that biosynthetic activities in the source and catabolic activities in the sink are the key factors controlling allocation of carbohydrates. Carbohydrate export rate is increased 10-fold in plants overexpressing pyruvate decarboxylase (Tadege et al. 1998 ), indicating a large potential for upregulation. Transporters, however, are located in strategic positions along metabolic pathways, and thus an effective regulatory mechanism would be to control uptake and efflux directly. Indeed, there is strong evidence that sugar transport regulates the distribution of assimilates within the plant through various macromolecular signaling events.

In the simplest sensing scenario, cells would contain only an intracellular receptor for a sugar metabolite. Such cells, whether located in source or sink tissues, could modulate metabolic processes, such as photosynthesis or carrier gene expression. However, due to intracellular metabolism, the effector cells involved in these processes must be able to differentiate between biosynthesis and transport, and therefore both intra- and extracellular concentrations of sugars need to be sensed. Furthermore, provided that the cell has a spectrum of carriers of varying affinity and capacity for sugar, extracellular sensors, as shown in Figure 4, can adjust sugar uptake to match requirements, for example, by inducing high-affinity uptake systems at low external concentration.

View larger version (26K): [in this window] [in a new window]   Figure 4. Model for Metabolite Sensing by a Combination of Internal and Membrane-Bound Receptors. In addition to an internal receptor (see text), membrane-bound receptors are used to sense external sugar concentrations. Such sensors trigger a signaling cascade regulating transporter biogenesis and insertion or degradation of proteins at the plasma membrane. In this scenario, low sugar concentrations activate a sensor to induce sugar transporter genes (preferentially high affinity). This enables more efficient sugar uptake. If, on the other hand, internal sugar concentration becomes too high, the intracellular sensor may either repress transporter transcription or trigger inactivation via endocytosis and degradation of the transporter, thus reducing the influx. Induction of low-affinity/high-capacity transporters could increase uptake at higher external concentrations.

In principle, multiple sensors could be utilized, some for high-affinity responses and others for adaptation to high-flux requirements. Because the plasma membrane has a limited capacity for protein content, this signal may at the same time lead to an increase in the turnover of low-affinity systems. Increased turnover of transporters can also be controlled via an internal sensor, thus decreasing import if intracellular concentrations exceed the requirements.

Although such regulatory networks could also be effective in unicellular organisms like yeast or algae, intercellular transport in higher plants is more complicated. This is because at least two cellular activities—export from one cell and import into the adjacent cell—have to be integrated. Little is known about the molecular mechanisms involved in sugar sensing in relation to transport in higher plants. Yeast could thus serve as a model to help uncover the regulatory networks in higher plants.

	YEAST AS A MODEL OF SUGAR SIGNALING

TOP INTRODUCTION SUGAR TRANSPORT SYSTEMS IN... SUGAR TRANSPORTERS CELLULAR LOCALIZATION OF SUT1... IN VIVO EVIDENCE OF... SUCROSE TRANSPORTERS IN PHLOEM... SENSING MECHANISMS IN SUGAR... YEAST AS A MODEL... SUGAR SENSORS: A NEW... SUGAR-MEDIATED REGULATION OF... HORMONAL REGULATION OF SUGAR... PLANT TRANSPORTER FAMILIES IN... CONCLUSIONS REFERENCES

The yeast Saccharomyces cerevisiae contains a large spectrum of >200 integral membrane proteins, many of which are clearly involved in transmembrane solute transport. For example, yeast contains >20 permeases for amino acid transport (Andre 1995 ; Nelissen et al. 1997 ) and >20 permeases for sugar transport (Andre 1995 ; Boles and Hollenberg 1997 ). The redundancy of transport systems suggests that complex regulatory networks are absolutely necessary to control the uptake of nutrients in response to a rapidly changing external environment. As shown in Figure 5, yeast has developed a two-pronged regulatory system to ensure coordination between the supply of sugars from the environment and the enzymatic machinery of the cells: (1) the extracellular concentration of sugars is sensed and sugar transport activity is regulated accordingly; (2) sugar transport activity determines the flux of sugars into the cell, subsequently generating intracellular signals for further regulatory processes.

View larger version (39K): [in this window] [in a new window]   Figure 5. Sugar Signal Transduction in Saccharomyces cerevisiae. HXT-type transporters mediate glucose uptake. Hexokinase PII (HXK2) functions in cytosolic sugar signaling, resulting in transcriptional regulation of enzymes and transporters necessary for sugar utilization. The SNF3 (high affinity) and RGT2 (low affinity) glucose receptors sense the external glucose concentration. These are homologous to HXT-type transporters but contain a C-terminal extension that functions in signaling. The SNF3 and RGT2 signaling pathways affect transcriptional regulation of high-affinity and low-affinity/high-capacity hexose transporter genes, respectively. See text for details.

In S. cerevisiae, multiple transport systems for glucose are regulated at the transcriptional level in response to the external concentration of glucose. For example, HXT2 and HXT7 serve as high-affinity glucose transporters and are induced only by low levels of glucose but repressed at high levels, whereas HXT1 functions as a low-affinity transporter and is induced only by high concentrations of glucose (Ozcan and Johnston 1995 ; Boles and Hollenberg 1997 ). Consequently, sensors of extracellular glucose that respond not only to the kind of carbon source in the medium but also to its concentration are required. Once inside the cell, glucose is phosphorylated by three different kinases: HXK1, HXK2, and GLK1. Finally, it is converted through the glycolytic pathway mainly into ethanol. By contrast to the uptake of glucose, the regulation of the intracellular glucose concentration, phosphorylation, and subsequently, the regulation of flux through glycolysis must be controlled by intracellular signals (Boles et al. 1997 ). Furthermore, the expression of genes for the utilization of alternative carbon sources like sucrose or galactose, and genes involved in gluconeogenesis, must be shut off in the presence of sufficient amounts of the preferred carbon source, glucose. This is achieved through a mechanism known as glucose (or carbon) catabolite repression (Ronne 1995 ; Gancedo 1998 ).

The glucose signal that triggers induction of hexose transporter genes is generated by the hexose sensors SNF3 and RGT2. On the other hand, the signal that triggers glucose repression is somehow connected to the kinase activity of HXK2 (Ma et al. 1989 ; Rose et al. 1991 ). In principle, there are two possibilities for sensory proteins to detect signaling molecules. First, sensors might act as receptors, binding the triggering molecule (e.g., glucose) and transducing the signal via other proteins. Second, sensors might behave like enzymes or transporters and undergo structural changes so as to monitor the presence or absence of the triggering compound directly. Flux measurements by such a sensor protein would involve the recognition of the velocity of the enzymatic reaction as the ratio of active to free enzyme.

	SUGAR SENSORS: A NEW PERSPECTIVE OF TRANSPORTERS

TOP INTRODUCTION SUGAR TRANSPORT SYSTEMS IN... SUGAR TRANSPORTERS CELLULAR LOCALIZATION OF SUT1... IN VIVO EVIDENCE OF... SUCROSE TRANSPORTERS IN PHLOEM... SENSING MECHANISMS IN SUGAR... YEAST AS A MODEL... SUGAR SENSORS: A NEW... SUGAR-MEDIATED REGULATION OF... HORMONAL REGULATION OF SUGAR... PLANT TRANSPORTER FAMILIES IN... CONCLUSIONS REFERENCES

Cell Surface Sugar Sensors
In Escherichia coli, it has long been known that glucose sensing is mediated through glucose phosphorylation during transport by the phosphotransferase system (Postma et al. 1993 ). However, no related proteins have yet been detected at the plasma membrane of eukaryotic cells. Glucose sensing in yeast seems to involve plasma membrane proteins that resemble glucose transporters but additionally possess large cytoplasmic signaling domains (Ozcan et al. 1996a ). A similar mechanism has been discovered recently for amino acid sensing (Didion et al. 1998 ; Iraqui et al. 1999 ) and might be a general phenomenon not restricted to yeast.

In yeast, SNF3 appears to be a sensor of low levels of glucose and mainly regulates expression of high-affinity glucose transporters, whereas RGT2 appears to be a sensor of high glucose concentrations that regulates expression of low-affinity glucose transporters. Additionally, SNF3 is required at high levels of glucose for repression of the high-affinity transporters HXT2, HXT6, and HXT7 (Liang and Gaber 1996 ; Vagnoli et al. 1998 ). Dominant mutations in both RGT2 and SNF3 that lead to the generation of signals in the absence of glucose have been identified (Ozcan et al. 1996a ). Despite the homology of SNF3 and RGT2 to glucose permeases, these transmembrane proteins do not seem to be able to mediate significant glucose transport (Liang and Gaber 1996 ; Ozcan et al. 1998 ). The large C-terminal extension of SNF3 (303 amino acids) contains two nearly identical repeats of 25 amino acids. One of these repeats is also present in the 218–amino acid C-terminal extension of RGT2 and in RAG4 (GenBank accession number Y14849) from Kluyveromyces lactis, which contains a 250–amino acid C-terminal extension and controls the expression of the low-affinity glucose transporter RAG1 (Chen et al. 1992 ). In Neurospora crassa, the glucose sensor RCO3 contains a 119–amino acid C-terminal extension that is dissimilar to that of SNF3, RGT2, and RAG4 (Madi et al. 1997 ).

From mutational analyses, yeast glucose sensors appear to function as two interacting domains (Ozcan et al. 1998 ; Vagnoli et al. 1998 ): the C-terminal extensions that are required for the transmission of the glucose signal, and the membrane-spanning domain necessary for glucose recognition. Because the glucose transporters HXT1 and HXT2 can be converted into glucose sensors by fusion to the SNF3 C terminus, it is tempting to speculate that the glucose sensors act as glucose transporters with a very low glucose transport capacity (i.e., too low to support growth of mutants that lack glucose transporters), which transduce the glucose signal by a conformational shift during glucose transport.

Another protein (SSY1) that appears to function as an amino acid sensor has recently been identified in yeast. SSY1 shows the features typical of the SNF3/RGT2 pair: a transmembrane domain related to amino acid permeases, a long cytoplasmic extension (in this case located at the N terminus of the protein), a low transcription rate, and a low coding probability (Andre 1995 ; Didion et al. 1998 ; Iraqui et al. 1999 ). SSY1, rather than being a transporter, controls the transcription of genes encoding amino acid permeases and seems to respond to changes in the extracellular concentration of various amino acids (Didion et al. 1998 ; Iraqui et al. 1999 ). The amino acid sequence of the cytoplasmic extension of SSY1 shows no significant similarities to those of SNF3 and RGT2.

The only intermediate components so far known to be involved in glucose-induced signal transduction in yeast are the transcription factor RGT1 (Ozcan et al. 1996a ) and SCF^Grr1, a ubiquitin protein ligase complex including the F-box protein GRR1, SKP1, and CDC53 (Li and Johnston 1997 ; Skowyra et al. 1997 ). RGT1 is a zinc cluster protein that binds directly to promoters of the HXT genes (Ozcan et al. 1996b ). It acts as a repressor of HXT genes in cells growing without glucose and as a transcriptional activator of HXT1 in cells growing on high levels of glucose. Repression of transcription by RGT1 is mediated by the SSN6-TUP1 complex, whereas RGT1-mediated induction is independent of these proteins (Figure 5).

The SCF^Grr1 protein complex is required for regulation of RGT1 activity (Ozcan and Johnston 1995 ) mediating the signal generated by SNF3 to inhibit the RGT1 repressor function in response to low levels of glucose. It is also required for conversion of RGT1 into an activator triggered by RGT2 in the presence of high levels of glucose. Ubiquitination of RGT1 or its regulator may target it for protein degradation by the proteasome or directly affect its function. SCF^Grr1 complex may be directly stimulated by glucose (Li and Johnston 1997 ) or may depend on glucose-activated kinase because target proteins must be phosphorylated to interact with GRR1 (Skowyra et al. 1997 ).

A third sensor protein, MEP2, was recently found in S. cerevisiae to be required for pseudohyphal differentiation in response to ammonium limitation (Lorenz and Heitman 1998 ). Under such conditions, diploid yeast cells differentiate into a filamentous, pseudohyphal growth form. MEP2 belongs to a family of three closely related ammonium permeases (Marini et al. 1997 ). However, unlike the other two members of this transporter family, MEP2 serves as both an ammonium transporter and a component of an ammonium sensor. mep2 mutant strains have no defects in growth rates or ammonium uptake, but no longer form pseudohyphal filaments on media containing limiting amounts of ammonium. Unlike the glucose sensor proteins, however, MEP2 is able to transport its substrate; and as compared with the other members of the ammonium permease family, MEP2 contains no significant amino acid extensions on either its N or C terminus.

Intracellular Sugar Sensing: Enzymes as Sensors
In the triggering reaction of glucose repression in yeast, HXK2 seems to play an important and probably more direct role. Mutations in HXK2 abolish glucose repression of invertase and other glucose-repressed genes (Entian 1980 ). The catalytic and regulatory functions of HXK2 are inseparable from glucose repression and inversely correlated to its sugar-phosphorylating activity (Ma et al. 1989 ; Rose et al. 1991 ). HXK2 exists in a dimeric–monomeric equilibrium that is affected by phosphorylation (Randez-Gil et al. 1998 ). In vivo, dephosphorylation of HXK2 is promoted upon addition of glucose and is dependent on protein phosphatase 1 (CID1/GLC7). A protein kinase involved in phosphorylation of HXK2 has not been found, and it is possible that phosphorylation of HXK2 could result from substrate-induced autophosphorylation (Fernandez et al. 1988 ). It has been reported that HXK2 has a weak protein kinase activity (Herrero et al. 1989 ; see above). Moreover, a hxk2 mutant that is not able to undergo phosphorylation can no longer transduce the glucose repression signal (Randez-Gil et al. 1998 ). These properties might classify HXK2 as an enzyme that additionally, through its enzymatic function, can act as a sensor protein. However, the actual mechanism representing the on–off switch of the glucose signal is not understood. The glucose repression signal finally inhibits the protein kinase SNF1/CAT1, a central element in the regulatory process (Figure 5) and highly conserved in eukaryotes. Glucose inhibition of SNF1 depends on protein phosphatase 1 (GLC7) and its targeting subunit REG1 (Ludin et al. 1998 ). In the absence of glucose, SNF1 relieves repression by the MIG-SSN6-TUP1 complexes (De Vit et al. 1997 ) but is also required for the operation of other transcription factors (Gancedo 1998 ).

In accordance with HXK2 being a sensor for glucose, the triggering of glucose repression in yeast is dependent on glucose uptake. However, the repression is not dependent on a specific hexose transporter protein; the glucose repression signal rather correlates with the extent of glucose influx into cells (Reifenberger et al. 1997 ). These observations fit very well with the two-pronged regulatory model described above: first, glucose transport activity is adjusted to the extracellular glucose concentration via SNF3 and RGT2; second, glucose transport activity limits provision of intracellular glucose, which then might act as a substrate for HXK2 as well as a global glucose signal (Figure 5). In addition, cross-talk between the two different processes might ensure feedback coordination. Such a function has recently been assigned to HXK2 which, in addition to carbon catabolite repression, seems also to be involved in glucose induction of HXT gene expression (Randez-Gil et al. 1998 ).

	SUGAR-MEDIATED REGULATION OF SINK AND SOURCE GENES

TOP INTRODUCTION SUGAR TRANSPORT SYSTEMS IN... SUGAR TRANSPORTERS CELLULAR LOCALIZATION OF SUT1... IN VIVO EVIDENCE OF... SUCROSE TRANSPORTERS IN PHLOEM... SENSING MECHANISMS IN SUGAR... YEAST AS A MODEL... SUGAR SENSORS: A NEW... SUGAR-MEDIATED REGULATION OF... HORMONAL REGULATION OF SUGAR... PLANT TRANSPORTER FAMILIES IN... CONCLUSIONS REFERENCES

A large spectrum of genes is regulated by sucrose and monosaccharides (reviewed in Thomas and Rodriguez 1994 ; Koch 1996 ). The interplay of regulatory processes interconnected with sugar regulation provides the plant with valuable mechanisms to adjust to environmental conditions and also to control developmental and physiological processes (e.g., photosynthesis and flowering) (Bernier et al. 1993 ; Jang and Sheen 1994 ; Corbesier et al. 1998 ). Carbohydrate-responsive genes can be classified as initiating "feast or famine" responses. Genes for photosynthesis and resource mobilization are induced by carbohydrate depletion (the famine response), whereas increasing sugar concentrations stimulate gene expression for utilization and storage (the feast response) independently of location (i.e., in source or sink tissues) (Rocha-Sosa et al. 1989 ; Muller-Rober et al. 1990 ; Sheen 1990 ; Graham et al. 1994 ; Jang and Sheen 1994 ; Thomas and Rodriguez 1994 ; Koch 1996 ).

Sucrose, as the principal transport form of sugars, can specifically control the expression of a number of genes. Examples of sucrose-regulated genes include an Arabidopsis leucine zipper gene, ATB2, and the RolC promoter from Agrobacterium (Smeekens and Rook 1997 ; Yokohama et al. 1997 ). Externally supplied sucrose exceeding concentrations of 25 mM lead to a repression of ATB2 transcription (Rook et al. 1998 ). In sugar beet, high sugar concentrations lead to a repression of sucrose transport activity, correlating with a reduction in steady state mRNA levels of BvSUT1 (Chiou and Bush 1998 ); glucose and fructose affect transport activity to a lesser extent. Sucrose can repress transcription of photosynthetic genes encoding, for example, chlorophyll a/b binding protein (CAB), ribulose-1,5-bisphosphate carboxylase/oxygenase (Rubisco), and plastocyanin. Sucrose-uncoupled (sun) mutants have been identified, in which sucrose concentration is uncoupled from the repression of such genes (Dijkwel et al. 1996 , Dijkwel et al. 1997 ). Taken together, these studies indicate the presence of sucrose-specific signal perception and transduction processes in which both internal and external sensors might be involved. Glucose-specific responses have also been described (Thomas and Rodriguez 1994 ; Koch 1996 ). Moreover, glucose and sucrose seem to control different pathways. Whereas glucose favors cell division, sucrose relates to storage compound accumulation in seeds (Weber et al. 1998 ).

A specific hexose-sensing system in which hexokinase plays a central role, potentially as an intracellular sensor, has been identified in the repression of typical "famine" genes (Figure 6; Sheen 1990 ; Graham et al. 1994 ; Jang and Sheen 1994 ). Specifically, nonmetabolizable glucose analogs (e.g., 6-deoxyglucose or 3-O-methylglucose) that are taken up into cells but are not metabolized by hexokinase do not repress gene induction in photosynthetic or glyoxylate cycles. Only substrates of hexokinase that are taken up and phosphorylated mimic glucose-specific repression (Graham et al. 1994 ; Jang and Sheen 1994 ). Additionally, phosphorylated hexoses do not alter gene expression, but inhibition of hexokinase blocks the 2-deoxyglucose– and mannose-dependent repression.

View larger version (31K): [in this window] [in a new window]   Figure 6. Current Representation of Sugar Sensing in Plants. Monosaccharide transporters allow the uptake of hexose analogs useful for probing the sugar signaling pathway. 6-Deoxyglucose and 3-O-methylglucose can be transported but are not substrates for hexokinase; therefore, signal pathways requiring hexokinase activity are not triggered by these analogs, whereas genes like patatin class I, invertase, or sucrose synthase genes are induced via a hexokinase-independent pathway. Mannose and 2-deoxyglucose serve as substrates for hexokinase and can thus repress photosynthetic genes via the hexokinase-dependent pathway. Sucrose can be metabolized and hexoses used in the hexokinase-dependent pathway.

Thus, hexokinase activity per se is involved in sensing, a finding that is further strengthened by studies of transgenic Arabidopsis plants in which the expression of the hexokinase-encoding genes AtHXK1 and AtHXK2 had been prevented (Jang et al. 1997 ). In antisense plants, the glucose-dependent repression of typical famine genes, such as Rubisco and CAB, is impaired, thereby leading to reduced sensitivity to high external glucose concentrations. Interestingly, Arabidopsis plants overexpressing a yeast HXK gene, thus bypassing sugar flux through the plant's endogenous hexokinases, behave similarly to the AtHXK antisense plants (Jang et al. 1997 ).

These data support a direct role for hexokinase itself in signaling in addition to its kinase activity. However, the situation seems to be more complex. Transgenic tobacco plants overexpressing a yeast invertase in the cytosol, apoplasm, or vacuole all accumulate elevated levels of hexoses. However, only in plants with apoplasmic or vacuolar invertase expression was gene expression repressed by the elevated sugar content (Herbers et al. 1996 ). Furthermore, because the introduction of sugar phosphates into cells by electroporation does not modify the expression of carbohydrate-responsive genes (Jang and Sheen 1994 ), it seems to be the flux of sugars undergoing phosphorylation that is sensed rather than the mere internal concentration of sugar phosphates.

A more recently identified hexokinase-independent glucose-signaling system, schematized in Figure 6, seems to be preferentially responsible for controlling "feast" and pathogen-related gene expression. In photoautotrophic Chenopodium rubrum cell suspensions, the expression of invertase and sucrose synthase genes is induced upon treatment with 6-deoxyglucose (Godt et al. 1995 ; Roitsch et al. 1995 ). In transgenic Arabidopsis, 3-O-methylglucose activates a patatin class I promoter fused to ß-glucuronidase, which suggests that the sensing mechanism for this nonphosphorylatable analog occurs before hexokinase in the signaling pathway.

Martin et al. 1997 have identified several Arabidopsis mutants with reduced sugar response (rsr) that harbor a patatin promoter–ß-glucuronidase construct. These mutants, in which the patatin promoter does not respond to sugars, offer a good model for studying hexokinase-independent sugar sensing. Specifically, despite high intracellular concentrations of hexoses caused by specific enzyme inhibitors, patatin expression was downregulated strongly, thereby supporting a model in which extracellular concentrations or fluxes are sensed at the cell exterior (Muller-Rober et al. 1990 ; Zrenner et al. 1995 ). As in the case of the hexokinase-dependent sensing mechanism, fluxes are more important than steady state levels of carbohydrate to initiate a response. Studies on sugar-induced pathogen-related genes, moreover, provide strong evidence for the existence of sensing mechanisms, located at the plasma membrane, which might correspond to the RGT2/SNF3-type sensing system present in yeast.

Despite the central importance of sugars as key regulators of gene expression, very little is known about the signal transduction mechanisms in which they take part. Several studies have provided evidence that mechanisms similar to yeast phosphorylation events are involved in sugar-specific signal transduction cascades. Several kinase genes have been found in plants with homology to SNF1 of which some complement the snf1 yeast mutant. In vivo function has been demonstrated in transgenic potato plants expressing an SNF1-related protein kinase gene in antisense orientation such that a decrease in sucrose synthase expression is observed in tubers (Halford and Hardie 1998 ). Rubisco gene repression and invertase gene induction by sugars involve the action of both kinases and phosphatases (Ehness et al. 1997 ). Also, in the case of the regulation of sporamin and ß-amylase gene expression, the involvement of protein phosphorylation is likely inasmuch as treatment with specific inhibitors of kinases and phosphatases reduces sugar-specific induction (Ohto and Nakamura 1995 ; Takeda et al. 1994 ).

	HORMONAL REGULATION OF SUGAR TRANSPORT

TOP INTRODUCTION SUGAR TRANSPORT SYSTEMS IN... SUGAR TRANSPORTERS CELLULAR LOCALIZATION OF SUT1... IN VIVO EVIDENCE OF... SUCROSE TRANSPORTERS IN PHLOEM... SENSING MECHANISMS IN SUGAR... YEAST AS A MODEL... SUGAR SENSORS: A NEW... SUGAR-MEDIATED REGULATION OF... HORMONAL REGULATION OF SUGAR... PLANT TRANSPORTER FAMILIES IN... CONCLUSIONS REFERENCES

Many studies have provided evidence that sugar transport can be adapted to the changing needs of the plant. Indeed, comparison of the transport activities in developing versus mature leaves has shown that H⁺/sucrose cotransport is differentially active and develops during leaf maturation (Lemoine et al. 1992 ). Hormones such as auxin and cytokinin have long been known to increase the rate of phloem transport. Fusicoccin and auxin can rapidly promote sucrose uptake, whereas abscisic acid acts as an inhibitor (Malek and Baker 1978 ; Sturgis and Rubery 1982 ; Vreugdenhil 1983 ). In broad bean, the direct promotion of assimilate export by the application of gibberellin was reported (Aloni et al. 1986 ). Phloem loading in isolated bundles of celery seems to be directly affected by gibberellin and auxin (Daie et al. 1986 ). However, a principle problem of such studies is the difficulty to differentiate between effects operating within the network.

Proton-coupled sugar transporters can be regulated in two major ways: (1) indirectly by regulating H⁺-ATPase activity, or (2) more specifically by controlling the expression of sugar transporters at the transcriptional and post-transcriptional levels. Several factors are known to regulate ATPase activity and/or transcription: fusicoccin (Oecking et al. 1997 ; Baunsgaard et al. 1998 ), salicylic acid (Bourbouloux et al. 1998 ), and anaerobiosis, which probably acts at the level of ATP supply for the H⁺-ATPase (Sowonick et al. 1974 ; Giaquinta 1977 ; Servaites et al. 1979 ; Thorpe et al. 1979 ; Maynard and Lucas 1982 ; see also Sze et al. 1999 , in this issue). Sucrose can also induce accumulation of two plasma membrane ATPases, LHA4 and LHA2 (Mito et al. 1996 ). This induction is dependent on sugar uptake and metabolism, inasmuch as mannitol and 3-O-methylglucose have no effect. These results suggest that the induction of expression of H⁺-ATPase genes by metabolizable sugars may be part of a generalized cellular response to promote cell growth in the presence of abundant carbon sources (Mito et al. 1996 ).

Potato SUT1 and Arabidopsis AtSUC2 are expressed in source and sink tissues (Riesmeier et al. 1993 ; Truernit and Sauer 1995 ). The expression of the sucrose transporter SUT1 is diurnally regulated at both the mRNA and protein level (Kuhn et al. 1997 ), in accordance with diurnal regulation of export rates from leaves (Heinecke et al. 1994 ). SUT1 mRNA and protein levels can, furthermore, be induced by the addition of auxin and cytokinin to detached leaves (C. Kühn and W.B. Frommer, unpublished results), whereas no such effect was observed for either of the two major H⁺-ATPase genes expressed in potato leaves (Harms et al. 1994 ). Sucrose itself was shown to be involved in regulating sucrose transporter activity, potentially at the transcriptional level (Chiou and Bush 1998 ).

Inhibitor experiments indicate that SUT1 activity is also regulated at the post-translational level by phosphorylation (Roblin et al. 1998 ). Protein kinase activities, which might be responsible for phosphorylation of sucrose transporters in the SEs, have been detected in the phloem sap (Nakamura et al. 1993 ). As described in yeast, sugars may also regulate the stability of transporters (Jiang et al. 1997 ). Inhibition studies using cycloheximide show that the half-life of SUT1 is in the range of a few hours (Kuhn et al. 1997 ). This high turnover rate may indicate specific mechanisms controlling the number of active carriers in the plasma membrane and may suggest involvement of endocytosis, as in the case of mammalian glucose transporters and yeast amino acid permeases (Hein et al. 1995 ; Thorens 1996 ).

Concerning monosaccharide transport, no clear function has been demonstrated using antisense or "knockout" strategies. Very little is also known about its regulation. Coordinated regulation of mRNAs for extracellular invertase and a monosaccharide transporter in C. rubrum has been described (Ehness and Roitsch 1997 ). Because sucrose synthase and invertase gene expression is regulated by sugars, one may expect a complex network coordinating uptake of both monosaccharides and sucrose with the metabolic events involving both extracellular and intracellular sensors as sketched in Figure 6.

	PLANT TRANSPORTER FAMILIES IN SUGAR SENSING

TOP INTRODUCTION SUGAR TRANSPORT SYSTEMS IN... SUGAR TRANSPORTERS CELLULAR LOCALIZATION OF SUT1... IN VIVO EVIDENCE OF... SUCROSE TRANSPORTERS IN PHLOEM... SENSING MECHANISMS IN SUGAR... YEAST AS A MODEL... SUGAR SENSORS: A NEW... SUGAR-MEDIATED REGULATION OF... HORMONAL REGULATION OF SUGAR... PLANT TRANSPORTER FAMILIES IN... CONCLUSIONS REFERENCES

Are there known members of the plant transporter families that could be sensors? Indications, as presented above, suggest that transporters might be involved in sensing hexoses (Figure 6; Martin et al. 1997 ). As described above, such sensors in yeast often contain additional cytosolic domains that are thought to play a role in transmitting the signal. Analysis of the plant monosaccharide transporter MST family (Table 1) indicates that the Arabidopsis genome contains at least 26 MST genes. Although none of the predicted AtMST proteins share obvious similarities with the C-terminal extensions found in the yeast RGT2 and SNF3, two Arabidopsis genes (AtSUGTRPR and F23E12.140; Table 1) that are closely related to each other contain extended central loops. Additionally, one member of the tomato and Arabidopsis SUT family is characterized by the presence of a long central loop predicted to be cytosolic (L. Barker, C. Kühn, B. Hirner, E. Boles, H. Hellmann, A. Weise, J.M. Ward, and W.B. Frommer, unpublished results). The availability of the full sequence from Arabidopsis will provide access for more detailed analysis. Because the putative tomato sucrose sensor colocalizes with SUT1 and because no sucrose transport activity is detectable, one might speculate that it is involved in controlling the expression and turnover of SUT1 in SEs (Figure 7).

View larger version (18K): [in this window] [in a new window]   Figure 7. A Potential Sucrose-Sensing Mechanism in SEs. Solanaceous SUT1 and a sucrose sensor colocalize in SEs (by analogy with yeast SNF3 and RGT2 proteins). The putative sensor regulates SUT1 either directly or via an indirect signaling mechanism such as phosphorylation. The high turnover rates of SUT1 may indicate that regulation occurs at the level of protein inactivation and degradation; however, because SUT1 is transcribed in companion cells, a regulatory mechanism involving transcriptional control is more complicated but still possible.

Because transporter-like sensors have also been identified for amino acids and ammonium, one may speculate that the transporter families also contain respective sensors. Within the large amino acid transporter families, no homologs containing large cytosolic domains similar to SSY1 have been found to date (Fischer et al. 1998 ). Because in the putative yeast ammonium sensor MEP2 no extended loops or other features that specify it as a sensor have been identified and because it represents a functional transport protein, sequence comparisons seem inappropriate to identify plant homologs. None of the plant ammonium transporters that are highly related to the yeast MEP genes contain extended cytosolic loops (N. von Wirén and W.B. Frommer, unpublished results). In all cases, experimental proof will be required to identify and characterize putative plant metabolite sensors. One approach could be to determine if, in "knockout" mutants, the transcriptional and post-transcriptional regulation of other transporters of the same family is affected.

	CONCLUSIONS

TOP INTRODUCTION SUGAR TRANSPORT SYSTEMS IN... SUGAR TRANSPORTERS CELLULAR LOCALIZATION OF SUT1... IN VIVO EVIDENCE OF... SUCROSE TRANSPORTERS IN PHLOEM... SENSING MECHANISMS IN SUGAR... YEAST AS A MODEL... SUGAR SENSORS: A NEW... SUGAR-MEDIATED REGULATION OF... HORMONAL REGULATION OF SUGAR... PLANT TRANSPORTER FAMILIES IN... CONCLUSIONS REFERENCES

In summary, sensors have probably evolved from transporters due to their suitability to recognize their substrates. This could have occurred by the addition of a signaling domain to an existing transporter. Plants have to adapt to changing environments, and sensing functions are thus essential. As compared with yeast, the identification of sensors in plants will be more difficult, but as in the case of functional expression to identify plant transporters, knowledge from yeast may serve as a tool to identify plant, and potentially animal, sensors as well.

Yeast complementation has indeed allowed the identification and characterization of both monosaccharide and sucrose transporters from plants. Both classes of carrier are encoded by large gene families. SUT1, localized in SEs, is an essential component responsible for phloem loading, as was shown by antisense inhibition in transgenic potato and tobacco. Physiological studies have shown that plant sugar transport and metabolism are highly regulated by sugars at the transcriptional and post-transcriptional levels. In yeast, sugar regulation of transporters is controlled by sensors at the plasma membrane. The availability of genes for members of the plant MST and SUT family and other phloem sap-specific proteins provides the tools to further explore and understand the mechanism and regulation of long-distance transport and its role in sugar sensing and regulation in plants.

	ACKNOWLEDGMENTS

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

	REFERENCES

TOP INTRODUCTION SUGAR TRANSPORT SYSTEMS IN... SUGAR TRANSPORTERS CELLULAR LOCALIZATION OF SUT1... IN VIVO EVIDENCE OF... SUCROSE TRANSPORTERS IN PHLOEM... SENSING MECHANISMS IN SUGAR... YEAST AS A MODEL... SUGAR SENSORS: A NEW... SUGAR-MEDIATED REGULATION OF... HORMONAL REGULATION OF SUGAR... PLANT TRANSPORTER FAMILIES IN... CONCLUSIONS REFERENCES

Aloni, B., Daie, J., and Wyse, R.E. (1986) Enhancement of [¹⁴C] sucrose export from source leaves of Vicia faba by gibberellic acid. Plant Physiol. 82:962-967[Abstract/Free Full Text].

André, B. (1995) An overview of membrane transport proteins in Saccharomyces cerevisiae.. Yeast 11:1575-1611[CrossRef][Web of Science][Medline].

Aoshima, H., Yamada, M., Sauer, N., Komor, E., and Schobert, C. (1993) Heterologous expression the proton/hexose cotransporter from Chlorella in Xenopus oocytes and its characterization with respect to sugar specificity, pH and membrane potential. J. Plant Physiol. 141:293-297[Web of Science].

Balachandran, S., Xiang, Y., Schobert, C., Thompson, G.A., and Lucas, W.J. (1997) Phloem sap proteins from Cucurbita maxima and Ricinus communis have the capacity to traffic cell to cell through plasmodesmata. Proc. Natl. Acad. Sci. USA 94:14150-14155[Abstract/Free Full Text].

Baunsgaard, L., Fuglsang, A.T., Jahn, T., Korthout, H.A.A.J., de Boer, A.H., and Palmgren, M.G. (1998) The 14-3-3 proteins associate with the plasma membrane H⁺-ATPase to generate a fusicoccin binding complex and a fusicoccin responsive system. Plant J. 13:661-671[CrossRef][Web of Science][Medline].

Bernier, G., Havelange, A., Houssa, C., Petitjean, A., and Lejeune, P. (1993) Physiological signals that induce flowering. Plant Cell 5:1147-1155[Free Full Text].

Boles, E., and Hollenberg, C.P. (1997) The molecular genetics of hexose transport in yeasts. FEMS Microbiol. Rev. 21:85-111[CrossRef][Web of Science][Medline].

Boles, E., Zimmermann, F.K., and Thevelein, J.M. (1997). Metabolic signals. In Yeast Sugar Metabolism: Biochemistry, Genetics, Biotechnology and Applications, F.K. Zimmermann and K.-D. Entian, eds (Lancaster, PA: Technomic), pp. 379–407.

Boorer, K.J., Loo, D.D.F., and Wright, E.M. (1994) Steady-state and presteady-state kinetics of the H⁺/hexose cotransporter (STP1) from Arabidopsis thaliana expressed in Xenopus oocytes. J. Biol. Chem. 269:20417-20424[Abstract/Free Full Text].

Boorer, K.J., Loo, D.D.F., Frommer, W.B., and Wright, E.M. (1996) Transport mechanism of the cloned potato H⁺/sucrose transporter StSUT1. J. Biol. Chem. 271:25139-25144[Abstract/Free Full Text].

Bourbouloux, A., Raymond, P., and Delrot, S. (1998) Effects of salicylic acid on sugar and amino acid uptake. J. Exp. Bot. 49:239-247[Abstract/Free Full Text].

Bürkle, L., Hibberd, J.M., Quick, W.P., Kühn, C., Hirner, B., and Frommer, W.B. (1998) The H⁺-sucrose co-transporter NtSUT1 is essential for sugar export from tobacco leaves. Plant Physiol. 118:59-68[Abstract/Free Full Text].

Bush, D.R. (1990) Electrogenicity, pH-dependence, and stoichiometry of the proton–sucrose symport. Plant Physiol. 93:1590-1596[Abstract/Free Full Text].

Bush, D.R. (1993) Proton-coupled sugar and amino acid transporters in plants. Annu. Rev. Plant Physiol. Plant Mol. Biol. 44:513-542.

Chen, X.J., Wesolowski-Louvel, M., and Fukuhara, H. (1992) Glucose transport in the yeast Kluyveromyces lactis. II. Transcriptional regulation of the glucose transporter gene RAG1. Mol. Gen. Genet. 233:97-105[CrossRef][Medline].

Chiou, T.J., and Bush, D.R. (1998) Sucrose is a signal molecule in assimilate partitioning. Proc. Natl. Acad. Sci. USA 95:4784-4788[Abstract/Free Full Text].

Chrispeels, M.J., Crawford, N.M., and Schroeder, J.I. (1999) Proteins for transport of water and mineral nutrients across the membranes of plant cells. Plant Cell 11:661-675[Free Full Text].

Corbesier, L., Lejeune, P., and Bernier, G. (1998) The role of carbohydrates in the induction of flowering in Arabidopsis thaliana: Comparison between the wild type and a starchless mutant. Planta 206:131-137[CrossRef][Web of Science][Medline].

Daie, J., Watts, M., Aloni, B., and Wyse, R.E. (1986) In vitro and in vivo modification of sugar transport and translocation in celery by phytohormones. Plant Sci. 46:35-41.

Delrot, S. (1989). Phloem loading. In Transport of Photoassimilates, D.A. Baker and J.A. Milburn, eds (London: Longman Scientific), pp. 167–205.

De Vit, M.J., Waddle, J.A., and Johnston, M. (1997) Regulated nuclear translocation of the Mig1 glucose repressor. Mol. Biol. Cell 8:1603-1618[Abstract].

DeWitt, N.D., and Sussman, M.R. (1995) Immunocytological localization of an epitope-tagged plasma membrane proton pump (H⁺-ATPase) in phloem companion cells. Plant Cell 7:2053-2067[Abstract].

Didion, T., Regenberg, B., Jorgensen, M.U., Kielland-Brandt, M.C., and Andersen, H.A. (1998) The permease homologue Ssy1p controls the expression of amino acid and peptide transporter genes in Saccharomyces cerevisiae.. Mol. Microbiol. 27:643-650[CrossRef][Web of Science][Medline].

Dijkwel, P.P., Kock, P., Bezemer, R., Weisbeek, P., and Smeekens, S. (1996) Sucrose represses the developmentally controlled transient activation of the plastocyanin gene in Arabidopsis thaliana seedlings. Plant Physiol. 110:455-463[Abstract].

Dijkwel, P.P., Huijser, C., Weisbeeek, P.J., Chua, N.-H., and Smeekens, S.C.M. (1997) Sucrose control of phytochrome A signaling in Arabidopsis. Plant Cell 9:583-595[Abstract].

Ehness, R., and Roitsch, T. (1997) Co-ordinated induction of mRNAs for extracellular invertase and a glucose transporter in Chenopodium rubrum by cytokinins. Plant J. 11:539-548[CrossRef][Web of Science][Medline].

Ehness, R., Ecker, M., Godt, D.E., and Roitsch, T. (1997) Glucose and stress independently regulate source and sink metabolism and defense mechanisms via signal transduction pathways involving protein phosphorylation. Plant Cell 9:1825-1841[Abstract].

Entian, K.D. (1980) Genetic and biochemical evidence for hexokinase PII as a key enzyme involved in carbon catabolite repression in yeast. Mol. Gen. Genet. 178:633-637[CrossRef][Web of Science][Medline].

Fernández, R., Herrero, P., Fernández, E., Fernández, M.T., López-Boado, Y.S., and Moreno, F. (1988) Autophosphorylation of yeast hexokinase PII. J. Gen. Microbiol. 134:2493-2498[Medline].

Fischer, W.N., André, B., Rentsch, D., Krolkiewicz, S., Tegeder, M., Breitkreuz, K., and Frommer, W.B. (1998) Amino acid transport in plants. Trends Plant Sci. 3:188-195[CrossRef][Web of Science].

Gahrtz, M., Stolz, J., and Sauer, N. (1994) A phloem-specific sucrose H⁺ symporter from Plantago major L. supports the model of apoplastic phloem loading. Plant J. 6:697-706[CrossRef][Web of Science][Medline].

Gahrtz, M., Schmelzer, E., Stolz, J., and Sauer, N. (1996) Expression of the PmSUC1 sucrose carrier gene from Plantago major L. is induced during seed development. Plant J. 9:93-100[CrossRef][Web of Science][Medline].

Gamalei, Y. (1989) Structure and function of leaf minor veins in trees and herbs. Trees 3:96-110[CrossRef].

Gancedo, J.M. (1998) Yeast carbon catabolite repression. Microbiol. Mol. Biol. Rev. 62:334-361[Abstract/Free Full Text].

Gaymard, F., Pilot, G., Lacombe, B., Bouchez, D., Bruneau, D., Boucherez, J., Michaux-Ferrière, N., Thibaud, J.P., and Sentenac, H. (1998) Identification and disruption of a plant Shaker-like outward channel involved in K⁺ release into the xylem sap. Cell 94:647-655[CrossRef][Web of Science][Medline].

Getz, H.P., Knauer, D., and Willenbrink, J. (1987) Transport of sugars across the plasma membrane of beetroot protoplasts. Planta 171:185-196[CrossRef].

Giaquinta, R.T. (1977) Possible role of pH gradient and membrane ATPase in the loading of sucrose into the sieve tubes. Nature 267:369-370[CrossRef].

Giaquinta, R.T. (1983) Phloem loading of sucrose. Annu. Rev. Plant Physiol. 34:347-387[Web of Science].

Godt, D.E., Riegel, A., and Roitsch, T. (1995) Regulation of sucrose synthase expression in Chenopodium rubrum: Characterization of sugar induced expression in photoautotrophic suspension cultures and sink tissue specific expression in plants. J. Plant Physiol. 146:231-236.

Gogarten, J.P., and Bentrup, F.W. (1989) Substrate specificity of the hexose carrier in the plasma membrane of Chenopodium suspension cells probes by transmembrane exchange diffusion. Planta 178:52-60[CrossRef].

Graham, I.A., Denby, K.J., and Leaver, C.J. (1994) Carbon catabolite repression regulates glyoxylate cycle gene expression in cucumber. Plant Cell 6:761-772[Abstract/Free Full Text].

Grusak, M.A., Delrot, S., and Ntsika, G. (1990) Short-term effects of heat-girdles on source leaves of Vicia faba: Analysis of phloem loading and carbon partitioning parameters. J. Exp. Bot. 41:1371-1377[Abstract/Free Full Text].

Halford, N.G., and Hardie, D.G. (1998) SNF1-related protein kinases: Global regulators of carbon metabolism in plants? Plant Mol. Biol. 37:735-748[CrossRef][Web of Science][Medline].

Harms, K., Wöhner, R.V., Schulz, B., and Frommer, W.B. (1994) Regulation of two p-type H⁺-ATPase genes from potato. Plant Mol. Biol. 26:979-988[Medline].

Harrington, G.N., Franceschi, V.R., Offler, C.E., Patrick, J.W., Harper, J.F., Frommer, W.B., Tegeder, M., and Hitz, W.D. (1997) Cell specific expression of three genes involved in plasma membrane sucrose transport in developing Vicia faba seed. Protoplasma 197:160-173[CrossRef][Web of Science].

Hayashi, H., Okada, Y., Mano, H., Kume, T., Matsuhashi, S., S.-Ishioka, N., Uchida, H., and Chino, M. (1997) Detection and characterization of nitrogen circulation through sieve tubes and xylem vessels of rice plants. Plant Soil 196:233-237[CrossRef].

Hein, C., Springael, J.Y., Volland, C., Haguenauer-Tsapis, R., and André, B. (1995) NPII, an essential yeast gene involved in induced degradation of Gap1 and Fur4 permeases, encodes the Rsp5 ubiquitin–protein ligase. Mol. Microbiol. 18:77-87[CrossRef][Web of Science][Medline].

Heinecke, D., Sonnewald, U., Büssis, D., Günter, G., Leidreiter, K., Wilke, I., Raschke, K., Willmitzer, L., and Heldt, H.W. (1992) Apoplastic expression of yeast-derived invertase in potato. Effects on photosynthesis, leaf soluble composition, water relations, and tuber composition. Plant Physiol. 100:301-308[Abstract/Free Full Text].

Heinecke, D., Kruse, A., Flügge, U.-I., Frommer, W.B., Riesmer, J.W., Willmitzer, L., and Heldt, H.W. (1994) Effect of antisense repression of the chloroplast triose-phosphate translocator on photosynthetic metabolism in transgenic potato plants. Planta 193:174-180[Web of Science].

Herbers, K., Meuwly, P., Frommer, W.B., Métraux, J.P., and Sonnewald, U. (1996) Systemic acquired resistance mediated by the ectopic expression of invertase: Possible hexose sensing in the secretory pathway. Plant Cell 8:793-803[Abstract].

Herrero, P., Fernández, R., and Moreno, F. (1989) The hexokinase isoenzyme PII of Saccharomyces cerevisiae is a protein kinase. J. Gen. Microbiol. 135:1209-1216[Abstract/Free Full Text].

Hirose, T., Imaizumi, N., Scofield, G.N., Furbank, R.T., and Ohsugi, R. (1997) cDNA cloning and tissue-specific expression of a gene for sucrose transporter from rice (Oryza sativa L.). Plant Cell Physiol. 38:1389-1396[Abstract/Free Full Text].

Hirsch, R.E., Lewis, B.D., Spalding, E.P., and Sussman, M.R. (1998) A role for the AKT1 potassium channel in plant nutrition. Science 280:918-921[Abstract/Free Full Text].

Iraqui, I., Vissers, S., Bernard, F., De Craene, J.-O., Boles, E., Urrestarazu, A., and André, B. (1999) Amino acid signaling in Saccharomyces cerevisiae: A permease-like sensor of external amino acids and the F-box protein Grr1p are required for transcriptional induction of the AGP1 gene encoding a broad-specificity amino acid permease. Mol. Cell. Biol. 19:989-1001[Abstract/Free Full Text].

Ishiwatari, Y., Fujiwara, T., McFarland, K.C., Nemoto, K., Hayashi, H., Chino, M., and Lucas, W.J. (1998) Rice phloem thioredoxin h has the capacity to mediate its own cell-to-cell transport through plasmodesmata. Planta 205:12-22[CrossRef][Web of Science][Medline].

Jang, J.C., and Sheen, J. (1994) Sugar sensing in higher plants. Plant Cell 6:1665-1679[Abstract].

Jang, J.C., León, P., Zhou, L., and Sheen, J. (1997) Hexokinase as a sugar sensor in higher plants. Plant Cell 9:5-19[Abstract].

Jiang, H., Medintz, I., and Michaels, C.A. (1997) Two glucose sensing/signaling pathways stimulate glucose-induced inactivation of maltose permease in Saccharomyces.. Mol. Biol. Cell 8:1293-1304[Abstract].

Keegstra, K., and Cline, K. (1999) Protein import and routing systems of chloroplasts. Plant Cell 11:557-570[Free Full Text].

Kluge, M., Becker, D., and Ziegler, H. (1970) Untersuchungen über ATP und andere organische Phosphoverbindungen im Siebrohrensaft von Yucca flaccida und Salix triandra. Planta 91:68-79.

Koch, K.E. (1996) Carbohydrate modulated gene expression in plants. Annu. Rev. Plant Physiol. Plant Mol. Biol. 47:509-540[CrossRef][Web of Science].

Köckenberger, W., Pope, J.M., Xia, Y., Jeffrey, K.R., Komor, E., and Callaghan, P.T. (1997) A non-invasive measurement of phloem and xylem water flow in castor bean seedlings by nuclear magnetic resonance microimaging. Planta 201:53-63[CrossRef][Web of Science].

Kragler, F., Monzer, J.K., Xoconostle-Cázares, B., and Lucas, W.J. (1998) Cell-to-cell transport of proteins: Requirement for unfolding and characterization of binding to a putative plasmodesmal receptor. Plant J. 15:367-381[CrossRef][Web of Science].

Krapp, A., Hofmann, B., Schäfer, C., and Stitt, M. (1993) Regulation of the expression of rbcS and other photosynthetic genes by carbohydrates: A mechanism for the sink regulation of photosynthesis. Plant J. 3:817-828.

Krysan, P.J., Young, J.C., Tax, F., and Sussman, M.R. (1996) Identification of transferred DNA insertions within Arabidopsis genes involved in signal transduction and ion transport. Proc. Natl. Acad. Sci. USA 93:8145-8150[Abstract/Free Full Text].

Kühn, C., Quick, W.P., Schulz, A., Sonnewald, U., and Frommer, W.B. (1996) Companion cell–specific inhibition of the potato sucrose transporter SUT1. Plant Cell Environ. 19:1115-1123[CrossRef].

Kühn, C., Franceschi, V.R., Schulz, A., Lemoine, R., and Frommer, W.B. (1997) Localization and turnover of sucrose transporters in enucleate sieve elements indicate macromolecular trafficking. Science 275:1298-1300[Abstract/Free Full Text].

Laloi, M., Delrot, S., and M'Batchi, B. (1993) Characterization of sugar efflux from sugar beet leaf plasma membrane vesicles. Plant Physiol. Biochem. 31:731-741.

Lazarowitz, S.R., and Beachy, R.N. (1999) Viral movement proteins as probes for intracellular and intercellular trafficking in plants. Plant Cell 11:535-548[Free Full Text].

Lemoine, R., Gallet, O., Gaillard, C., Frommer, W.B., and Delrot, S. (1992) Plasma membrane vesicles from source and sink leaves. Plant Physiol. 100:1150-1156[Abstract/Free Full Text].

Lemoine, R., Kühn, C., Thiele, N., Delrot, S., and Frommer, W.B. (1996) Antisense inhibition of the sucrose transporter: Effects on amount of carrier and sucrose transport activity. Plant Cell Environ. 19:1124-1131[CrossRef].

Li, F.N., and Johnston, M. (1997) Grr1 of Saccharomyces cerevisiae is connected to the ubiquitin proteolysis machinery through Skp1: Coupling glucose sensing to gene expression and the cell cycle. EMBO J. 16:5629-5638[CrossRef][Web of Science][Medline].

Liang, H., and Gaber, R.F. (1996) A novel signal transduction pathway in Saccharomyces cerevisiae defined by SNF3-regulated expression of HXT6. Mol. Biol. Cell 7:1953-1966[Abstract].

Lorenz, M.C., and Heitman, J. (1998) The MEP2 ammonium permease regulates pseudohyphal differentiation in Saccharomyces cerevisiae.. EMBO J. 17:1236-1247[CrossRef][Web of Science][Medline].

Lucas, W.J., Ding, B., and van der Schoot, C. (1993) Plasmodesmata and the supracellular nature of plants. New Phytol. 125:435-476[CrossRef][Web of Science].

Lucas, W.J., Bouché-Pillon, S., Jackson, D.P., Nguyen, L., Baker, L., Ding, B., and Hake, S. (1995) Selective trafficking of KNOTTED-1 homeodomain protein and its RNA through plasmodesmata. Science 270:1980-1983[Abstract/Free Full Text].

Ludin, K., Jiang, R., and Carlson, M. (1998) Glucose-regulated interaction of a regulatory subunit of protein phosphatase 1 with the Snf1 protein kinase in Saccharomyces cerevisiae.. Proc. Natl. Acad. Sci. USA 95:6245-6250[Abstract/Free Full Text].

Ma, H., Bloom, L.M., Zhu, Z., Walsh, C.T., and Botstein, D. (1989) The residual enzymatic phosphorylation activity of hexokinase II mutants is correlated with glucose repression in Saccharomyces cerevisiae.. Mol. Cell. Biol. 9:5643-5649[Abstract/Free Full Text].

Madi, L., McBride, S.K., Bailey, L.A., and Ebbole, D.J. (1997) rco-3, a gene involved in glucose transport and conidiation in Neurospora crassa.. Genetics 146:499-506[Abstract].

Malek, F., and Baker, D.A. (1978) Effect of fusicoccin on proton co-transport of sugars in the phloem loading of Ricinus communis L. Plant Sci. Lett. 11:233-239.

Marini, A.M., Soussi-Boudekou, S., Vissers, S., and André, B. (1997) A family of ammonium transporters in Saccharomyces cerevisiae.. Mol. Cell. Biol. 17:4282-4293[Abstract].

Martin, T., Hellman, H., Schmidt, R., Willmitzer, L., and Frommer, W.B. (1997) Identification of mutants in metabolically regulated gene expression. Plant J. 11:53-62[CrossRef][Web of Science][Medline].

Marty, F. (1999) Plant vacuoles. Plant Cell 11:587-599[Free Full Text].

Maynard, J.W., and Lucas, W.J. (1982) Sucrose and glucose uptake in Beta vulgaris leaf tissue. A case for a general (apoplastic) retrieval system. Plant Physiol. 70:1436-1443[Abstract/Free Full Text].

Mezitt, L.A., and Lucas, W.J. (1996) Plasmodesmal cell-to-cell transport of proteins and nucleic acids. Plant Mol. Biol. 32:251-273[CrossRef][Web of Science][Medline].

Minchin, P.E.H., and Thorpe, M.R. (1987) Measurement of unloading and reloading of photoassimilates within the stem of bean. J. Exp. Bot. 38:211-220[Abstract/Free Full Text].

Mito, N., Wimmers, L.E., and Bennett, A.B. (1996) Sugar regulates mRNA abundance of H⁺-ATPase gene family members in tomato. Plant Physiol. 112:1229-1236[Abstract].

Müller-Röber, B., Kossmann, J., Hannah, L.C., Willmitzer, L., and Sonnewald, U. (1990) One of two different ADP-glucose pyrophosphorylase genes from potato responds strongly to elevated levels of sucrose. Mol. Gen. Genet. 224:136-146[Web of Science][Medline].

Nakamura, S., Hayashi, H., Mori, S., and Chino, M. (1993) Protein phosphorylation in the sieve tubes of rice plants. Plant Cell Physiol. 34:927-933[Abstract/Free Full Text].

Nelissen, B., de Wachter, R., and Goffeau, A. (1997) Classification of all putative permeases and other membrane plurispanners of the major facilitator superfamily encoded by the complete genome of Saccharomyces cerevisiae.. FEMS Microbiol. Rev. 21:113-134[CrossRef][Web of Science][Medline].

Oecking, C., Piotrowski, M., Hagemeier, J., and Hagemann, K. (1997) Topology and target interaction of the fusicoccin-binding 14-3-3 homologs of Commelina communis.. Plant J. 12:441-453[CrossRef][Web of Science].

Ohto, M.A., and Nakamura, K. (1995) Sugar-induced increase of calcium-dependent protein kinases associated with the plasma membrane in leaf tissues of tobacco. Plant Physiol. 109:973-981[Abstract].

Oparka, K., and Prior, D.A.M. (1992) Direct evidence for pressure-generated closure of plasmodesmata. Plant J. 2:741-750[Web of Science].

Oparka, K.J., and Turgeon, R. (1999) Sieve elements and companion cells—Traffic control centers of the phloem. Plant Cell 11:739-750[Free Full Text].

Oparka, K.J., Duckett, C.M., Prior, D.A.M., and Fisher, D.B. (1994) Real-time imaging of phloem unloading in the root tip of Arabidopsis.. Plant J. 6:759-766[CrossRef][Web of Science].

Overall, R.L., and Blackman, L.M. (1996) A model for macromolecular structure of plasmodesmata. Trends Plant Sci. 1:207-211.

Overvoorde, P.J., Frommer, W.B., and Grimes, H.D. (1996) A soybean sucrose binding protein independently mediates nonsaturable sucrose uptake in yeast. Plant Cell 8:271-280[Abstract].

Özcan, S., and Johnston, M. (1995) Three different regulatory mechanisms enable yeast hexose transporter (HXT) genes to be induced by different levels of glucose. Mol. Cell. Biol. 15:1564-1572[Abstract].

Özcan, S., Dover, J., Rosenwald, A.G., Woelfl, S., and Johnston, M. (1996a) Two glucose transporters in S. cerevisiae are glucose sensors that generate a signal for induction of gene expression. Proc. Natl. Acad. Sci. USA 93:12428-12432[Abstract/Free Full Text].

Özcan, S., Leong, T., and Johnston, M. (1996b) Rgt1p of Saccharomyces cerevisiae, a key regulator of glucose-induced genes, is both an activator and a repressor of transcription. Mol. Cell. Biol. 16:6419-6426[Abstract].

Özcan, S., Dover, J., and Johnston, M. (1998) Glucose sensing and signaling by two glucose receptors in the yeast Saccharomyces cerevisiae.. EMBO J. 17:2566-2573[CrossRef][Web of Science][Medline].

Patrick, J.W. (1997) Phloem unloading: Sieve element unloading and post-sieve element transport. Annu. Rev. Plant Physiol. Plant Mol. Biol. 48:191-222[CrossRef][Web of Science].

Postma, P.W., Lengeler, J.W., and Jacobson, G.R. (1993) Phosphoenolpyruvate:carbohydrate phosphotransferase systems of bacteria. Microbiol. Rev. 57:543-594[Abstract/Free Full Text].

Randez-Gil, F., Sanz, P., Entian, K.-D., and Prieto, J.A. (1998) Carbon source–dependent phosphorylation of hexokinase PII and its role in the glucose-signaling response in yeast. Mol. Cell. Biol. 18:2940-2948[Abstract/Free Full Text].

Reifenberger, E., Boles, E., and Ciriacy, M. (1997) Kinetic characterization of individual hexose transporters of Saccharomyces cerevisiae and their relation to the triggering mechanisms of glucose repression. Eur. J. Biochem. 245:324-333[Web of Science][Medline].

Rentsch, D., Boorer, K., and Frommer, W.B. (1998) Molecular biology of sucrose, amino acid and oligopeptide transporters at the plasma membrane of plant cells. J. Membr. Biol. 162:177-190[CrossRef][Web of Science][Medline].

Riesmeier, J.W., Willmitzer, L., and Frommer, W.B. (1992) Isolation and characterization of a sucrose carrier cDNA from spinach by functional expression in yeast. EMBO J. 11:4705-4713[Web of Science][Medline].

Riesmeier, J.W., Hirner, B., and Frommer, W.B. (1993) Expression of the sucrose transporter from potato correlates with the sink-to-source transition in leaves. Plant Cell 5:1591-1598[Abstract].

Riesmeier, J.W., Willmitzer, L., and Frommer, W.B. (1994) Evidence for an essential role of the sucrose transporter in phloem loading and assimilate partitioning. EMBO J. 13:1-7[Web of Science][Medline].

Roblin, G., Sakr, S., Bonmort, J., and Delrot, S. (1998) Regulation of a plant plasma membrane sucrose transporter by phosphorylation. FEBS Lett. 424:165-168[CrossRef][Web of Science][Medline].

Rocha-Sosa, M., Sonnewald, U., Frommer, W., Stratmann, M., Schell, J., and Willmitzer, L. (1989) Both developmental and metabolic signals activate the promoter of a patatin class I gene. EMBO J. 8:23-29[Web of Science][Medline].

Roeckl, B. (1949) Nachweis eines Konzentrationshubs zwischen Palisadenzellen und Siebröhren. Planta 36:530-550.

Roitsch, T., Bittner, M., and Godt, D.E. (1995) Induction of apoplastic invertase of Chenopodium rubrum by D-glucose and a glucose analog and tissue-specific expression suggest a role in sink-regulation. Plant Physiol. 108:285-294[Abstract].

Ronne, H. (1995) Glucose repression in fungi. Trends Genet. 11:12-17[CrossRef][Web of Science][Medline].

Rook, F., Grrits, N., Kortstee, A., van Kampen, M., Borrias, M., Wiesbeek, P., and Smeekens, S. (1998) Sucrose-specific signaling represses translation of the Arabidopsis ATB2 bZIP transcription factor gene. Plant J. 15:253-263[CrossRef][Web of Science][Medline].

Rose, M., Albig, W., and Entian, K.-D. (1991) Glucose repression in Saccharomyces cerevisiae is directly associated with hexose phosphorylation by hexokinases PI and PII. Eur. J. Biochem. 199:511-518[Medline].

Sauer, N., and Stadler, R. (1993) A sink-specific H⁺/monosaccharide co-transporter from Nicotiana tabacum: Cloning and heterologous expression in baker's yeast. Plant J. 4:601-610[CrossRef][Web of Science][Medline].

Sauer, N., and Stolz, J. (1994) SUC1 and SUC2: Two sucrose transporters from Arabidopsis thaliana: Expression and characterization in baker's yeast and identification of the histidine-tagged protein. Plant J. 6:67-77[CrossRef][Web of Science][Medline].

Sauer, N., and Tanner, W. (1989) The hexose carrier from Chlorella. cDNA cloning of a eucaryotic H⁺-cotransporter. FEBS Lett. 259:43-46[CrossRef][Web of Science][Medline].

Sauer, N., Caspari, T., Klebl, F., and Tanner, W. (1990a) Functional expression of the Chlorella hexose transporter in S. pombe.. Proc. Natl. Acad. Sci. USA 87:7949-7950[Abstract/Free Full Text].

Sauer, N., Friedländer, K., and Gräml-Wicke, U. (1990b) Primary structure, genomic organization and heterologous expression of a glucose transporter from A. thaliana.. EMBO J. 9:3045-3050[Web of Science][Medline].

Schobert, C., Grossmann, P., Gottschalk, M., Komor, E., Pecsvaradi, A., and Nieden, U.Z. (1995) Sieve-tube exudate from Ricinus communis L. seedlings contains ubiquitin and chaperones. Planta 196:205-210[Web of Science].

Schulz, A., Kühn, C., Riesmeier, J.W., and Frommer, W.B. (1998) Ultrastructural effects in potato leaves due to antisense-inhibition of the sucrose transporter indicate a symplasmic pre-phloem transport of assimilates and an apoplasmic mode of phloem loading. Planta 206:533-543[CrossRef][Web of Science].

Servaites, J.C., Schrader, L.E., and Jung, D.M. (1979) Energy-dependent loading of amino acids and sucrose into the phloem of soybean. Plant Physiol. 64:546-550[Abstract/Free Full Text].

Shakya, R., and Sturm, A. (1998) Characterization of source- and sink-specific sucrose/H⁺ symporters from carrot. Plant Physiol. 118:1473-1480[Abstract/Free Full Text].

Sheen, J. (1990) Metabolic repression of transcription in higher plants. Plant Cell 2:1027-1038[Abstract/Free Full Text].

Sjölund, R.D. (1997) The phloem sieve element: A river runs through it. Plant Cell 9:1137-1146[CrossRef][Web of Science][Medline].

Skowyra, D., Craig, K.L., Tyers, M., Elledge, S.J., and Harper, J.W. (1997) F-box proteins are receptors that recruit phosphorylated substrates to the SCF ubiquitin–ligase complex. Cell 91:209-219[CrossRef][Web of Science][Medline].

Slone, J.H., Buckhout, T.J., and Vanderwoude, W.J. (1991) Symport of proton and sucrose in plasma membrane vesicles isolated from spinach leaves. Plant Physiol. 96:615-618[Abstract/Free Full Text].

Smeekens, S., and Rook, F. (1997) Sugar sensing and sugar-mediated signal transduction in plants. Plant Physiol. 115:7-13[Web of Science][Medline].

Sowonick, S.A., Geiger, D.R., and Fellows, R.J. (1974) Evidence for active phloem loading in the minor veins of sugar beet. Plant Physiol. 54:886-891[Abstract/Free Full Text].

Stadler, R., and Sauer, N. (1996) The Arabidopsis thaliana AtSUC2 gene is specifically expressed in companion cells. Bot. Acta 109:299-308[Web of Science].

Stadler, R., Brandner, J., Schulz, A., Gahrtz, M., and Sauer, N. (1995) Phloem loading by the PmSUC2 sucrose carrier from Plantago major occurs into companion cells. Plant Cell 7:1545-1554[Abstract].

St. Johnston, D. (1995) The intracellular localization of messenger RNAs. Cell 81:161-170[CrossRef][Web of Science][Medline].

Sturgis, J.N., and Rubery, P.H. (1982) The effects of indol 3-indolyl-acetic acid and fusicoccin on the kinetic parameters of sucrose uptake by disc from expanded primary leaves of Phaseolus vulgaris.. Plant Sci. Lett. 24:319-326[CrossRef].

Sze, H., Li, X., and Palmgren, M.G. (1999) Energization of plant cell membranes by H⁺-pumping ATPases: Regulation and biosynthesis. Plant Cell 11:677-689[Free Full Text].

Szederkényi, J., Komor, E., and Schobert, C. (1997) Cloning of the cDNA for glutaredoxin, an abundant sieve-tube exudate protein from Ricinus communis L. and characterisation of the glutathione-dependent thiol-reduction system in sieve tubes. Planta 202:349-356[CrossRef][Web of Science][Medline].

Tadege, M., Bucher, M., Stähli, W., Suter, M., Dupuis, I., and Kuhlemeier, C. (1998) Activation of plant defense responses and sugar efflux by expression of pyruvate decarboxylase in potato leaves. Plant J. 16:661-671[CrossRef][Web of Science].

Takeda, S., Mano, S., Ohto, M., and Nakamura, N. (1994) Inhibitors of protein phosphatases 1 and 2A block the sugar-inducible gene expression in plants. Plant Physiol. 106:567-574[Abstract].

Tegeder, M., Wang, X.D., Frommer, W.B., Offler, C.E., and Patrick, J.W. (1999) Sucrose transport into developing seeds of Pisum sativum L. Plant J. in press.

Thomas, B.R., and Rodriguez, R.L. (1994) Metabolite signals regulate gene expression and source/sink relations in cereal seedlings. Plant Physiol. 106:1235-1239[Web of Science][Medline].

Thorens, B. (1996) Glucose transporters in the regulation of intestinal, renal, and liver glucose fluxes. Am. J. Physiol. 270:541-553.

Thorpe, M.R., Minchin, P.E.H., and Dye, E.A. (1979) Oxygen effects on phloem loading. Plant Sci. Lett. 15:345-350.

Truernit, E., and Sauer, N. (1995) The promoter of the Arabidopsis thaliana SUC2 sucrose-H⁺ symporter gene directs expression of ß-glucuronidase to the phloem: Evidence for phloem loading and unloading by SUC2. Planta 196:564-570[Web of Science][Medline].

Truernit, E., Schmid, J., Epple, P., Illig, J., and Sauer, N. (1996) The sink-specific and stress-regulated Arabidopsis STP4 gene: Enhanced expression of a gene encoding a monosaccharide transporter by wounding, elicitors, and pathogen challenge. Plant Cell 8:2169-2182[Abstract].

Tubbe, A., and Buckhout, T.J. (1992) In vitro analysis of the H⁺-hexose symporter on the plasma membrane of sugarbeets (Beta vulgaris L.). Plant Physiol. 99:945-951[Abstract/Free Full Text].

Vagnoli, P., Coons, D.M., and Bisson, L.F. (1998) The C-terminal domain of Snf3p mediates glucose-responsive signal transduction in Saccharomyces cerevisiae.. FEMS Microbiol. Lett. 160:31-36[CrossRef][Medline].

van Bel, A.J.E. (1993) Strategies of phloem loading. Annu. Rev. Plant Physiol. Plant Mol. Biol. 44:253-281[CrossRef][Web of Science].

van Bel, A.J.E. (1996) Interaction between sieve element and companion cell and the consequences for photoassimilate distribution. Two structural hardware frames with associated physiological software packages? J. Exp. Bot. 47:1129-1140.

van Bel, A.J.E., and Gamalei, Y.V. (1992) Ecophysiology of phloem loading in source leaves. Plant Cell Environ. 15:265-270[CrossRef].

Vitale, A., and Denecke, J. (1999) The endoplasmic reticulum—Gateway of the secretory pathway. Plant Cell 11:615-628[Free Full Text].

Voinnet, O., Vain, P., Angell, S., and Baulcombe, D.C. (1998) Systemic spread of sequence-specific transgene RNA degradation in plants is initiated by localized introduction of ectopic promoterless DNA. Cell 95:177-187[CrossRef][Web of Science][Medline].

Vreugdenhil, D. (1983) Abscisic acid inhibits phloem loading of sucrose. Physiol. Plant. 57:463-467[CrossRef].

Walker, N.A., Patrick, J.W., Zhang, W., and Fieuw, S. (1995) Mechanism of photosynthate efflux from seed coats of Phaseolus vulgaris: A chemiosmotic analysis. J. Exp. Bot. 46:539-549[Abstract/Free Full Text].

Wang, Q., Monroe, J., and Sjölund, R.D. (1995) Identification and characterization of a phloem-specific ß-amylase. Plant Physiol. 109:743-750[Abstract].

Ward, J., Kühn, C., Tegeder, M., and Frommer, W.B. (1998) Sucrose transport in plants. Int. Rev. Cytol. 178:41-71[Web of Science][Medline].

Weber, H., Borisjuk, L., Heim, U., Sauer, N., and Wobus, U. (1997) A role for sugar transporters during seed development: Molecular characterization of a hexose and a sucrose carrier in fava bean seeds. Plant Cell 9:895-908[Abstract/Free Full Text].

Weber, H., Heim, U., Golombek, S., Borisjuk, L., Manteuffel, R., and Wobus, U. (1998) Expression of a yeast-derived invertase in developing cotyledons of Vicia narboensis alters the carbohydrate state and affects storage functions. Plant J. 16:163-172[CrossRef][Web of Science][Medline].

Wright, K.M., and Oparka, K.J. (1997) Metabolic inhibitors induce symplastic movement of solutes from the transport phloem of Arabidopsis roots. J. Exp. Bot. 48:1807-1814.

Xoconostle-Càzares, B., Xiang, Y., Ruiz-Medrano, R., Wang, H.L., Monzer, J., Yoo, B.C., McFarland, K.C., Franceschi, V.R., and Lucas, W.L. (1999) Plant paralog to viral movement protein that potentiates transport of mRNA into the phloem. Science 283:94-98[Abstract/Free Full Text].

Yokohama, R., Hirose, T., Fujii, N., Aspuria, E.T., Kato, A., and Uchimiya, H. (1997) The rolC promoter of Agrobacterium rhizogenes Ri plasmid is activated by sucrose in transgenic tobacco plants. Mol. Gen. Genet. 244:15-22.

Zamski, E., and Schnaffer, A.A. (1996). Photoassimilates, Distribution Plants and Crops. (New York: Decker).

Zhou, J.J., Theodolou, F., Sauer, N., Sanders, D., and Miller, A.J. (1997) A kinetic model with ordered cytoplasmic dissociation for SUC1, an Arabidopsis H⁺/sucrose cotransporter expressed in Xenopus oocytes. J. Membr. Biol. 159:113-125[CrossRef][Web of Science][Medline].

Zimmermann, M.H., and Ziegler, H. (1975). List of sugars and sugar alcohols in sieve-tube exudates. In Transport in Plants, Encyclopedia of Plant Physiology, New Series Vol. 1. I. Phloem Transport, M.H. Zimmermann and J.A. Milburn, eds (New York: Springer-Verlag), pp. 245–271.

Zrenner, R., Salanoubat, M., Willmitzer, L., and Sonnewald, U. (1995) Evidence of the crucial role of sucrose synthase for sink strength using transgenic potato plants (Solanum tuberosum L.). Plant J. 7:97-107[CrossRef][Web of Science][Medline].

This article has been cited by other articles:

				A. J. McCormick, D. A. Watt, and M. D. Cramer Supply and demand: sink regulation of sugar accumulation in sugarcane J. Exp. Bot., February 1, 2009; 60(2): 357 - 364. [Abstract] [Full Text] [PDF]

				D. Pozueta-Romero, P. Gonzalez, E. Etxeberria, and J. Pozueta-Romero The Hyperbolic and Linear Phases of the Sucrose Accumulation Curve in Turnip Storage Cells Denote Carrier-mediated and Fluid Phase Endocytic Transport, Respectively J. Amer. Soc. Hort. Sci., July 1, 2008; 133(4): 612 - 618. [Abstract] [Full Text] [PDF]

				L. Lejay, J. Wirth, M. Pervent, J. M.-F. Cross, P. Tillard, and A. Gojon Oxidative Pentose Phosphate Pathway-Dependent Sugar Sensing as a Mechanism for Regulation of Root Ion Transporters by Photosynthesis Plant Physiology, April 1, 2008; 146(4): 2036 - 2053. [Abstract] [Full Text] [PDF]

				H. Zhang, H. Rong, and D. Pilbeam Signalling mechanisms underlying the morphological responses of the root system to nitrogen in Arabidopsis thaliana J. Exp. Bot., July 1, 2007; 58(9): 2329 - 2338. [Abstract] [Full Text] [PDF]

				D. Gagneul, A. Ainouche, C. Duhaze, R. Lugan, F. R. Larher, and A. Bouchereau A Reassessment of the Function of the So-Called Compatible Solutes in the Halophytic Plumbaginaceae Limonium latifolium Plant Physiology, July 1, 2007; 144(3): 1598 - 1611. [Abstract] [Full Text] [PDF]

				Q.-S. Qiu, S. C. Hardin, J. Mace, T. P. Brutnell, and S. C. Huber Light and Metabolic Signals Control the Selective Degradation of Sucrose Synthase in Maize Leaves during Deetiolation Plant Physiology, May 1, 2007; 144(1): 468 - 478. [Abstract] [Full Text] [PDF]

				G. N. Scofield, N. Aoki, T. Hirose, M. Takano, C. L. D. Jenkins, and R. T. Furbank The role of the sucrose transporter, OsSUT1, in germination and early seedling growth and development of rice plants J. Exp. Bot., February 1, 2007; 58(3): 483 - 495. [Abstract] [Full Text] [PDF]

				T. Remans, P. Nacry, M. Pervent, S. Filleur, E. Diatloff, E. Mounier, P. Tillard, B. G. Forde, and A. Gojon The Arabidopsis NRT1.1 transporter participates in the signaling pathway triggering root colonization of nitrate-rich patches PNAS, December 12, 2006; 103(50): 19206 - 19211. [Abstract] [Full Text] [PDF]

				C. Conde, A. Agasse, D. Glissant, R. Tavares, H. Geros, and S. Delrot Pathways of Glucose Regulation of Monosaccharide Transport in Grape Cells Plant Physiology, August 1, 2006; 141(4): 1563 - 1577. [Abstract] [Full Text] [PDF]

				E. Baroja-Fernandez, E. Etxeberria, F. J. Munoz, M. T. Moran-Zorzano, N. Alonso-Casajus, P. Gonzalez, and J. Pozueta-Romero An Important Pool of Sucrose Linked to Starch Biosynthesis is Taken up by Endocytosis in Heterotrophic Cells Plant Cell Physiol., April 1, 2006; 47(4): 447 - 456. [Abstract] [Full Text] [PDF]

				I. Couee, C. Sulmon, G. Gouesbet, and A. El Amrani Involvement of soluble sugars in reactive oxygen species balance and responses to oxidative stress in plants J. Exp. Bot., February 1, 2006; 57(3): 449 - 459. [Abstract] [Full Text] [PDF]

				B. H. Junker, R. Wuttke, A. Nunes-Nesi, D. Steinhauser, N. Schauer, D. Bussis, L. Willmitzer, and A. R. Fernie Enhancing Vacuolar Sucrose Cleavage Within the Developing Potato Tuber has only Minor Effects on Metabolism Plant Cell Physiol., February 1, 2006; 47(2): 277 - 289. [Abstract] [Full Text] [PDF]

				H. Azevedo, C. Conde, H. Geros, and R. M. Tavares The Non-host Pathogen Botrytis cinerea Enhances Glucose Transport in Pinus pinaster Suspension-cultured Cells Plant Cell Physiol., February 1, 2006; 47(2): 290 - 298. [Abstract] [Full Text] [PDF]

				C. Solfanelli, A. Poggi, E. Loreti, A. Alpi, and P. Perata Sucrose-Specific Induction of the Anthocyanin Biosynthetic Pathway in Arabidopsis Plant Physiology, February 1, 2006; 140(2): 637 - 646. [Abstract] [Full Text] [PDF]

				D. Y. Little, H. Rao, S. Oliva, F. Daniel-Vedele, A. Krapp, and J. E. Malamy The putative high-affinity nitrate transporter NRT2.1 represses lateral root initiation in response to nutritional cues PNAS, September 20, 2005; 102(38): 13693 - 13698. [Abstract] [Full Text] [PDF]

				E. Etxeberria, P. Gonzalez, P. Tomlinson, and J. Pozueta-Romero Existence of two parallel mechanisms for glucose uptake in heterotrophic plant cells J. Exp. Bot., July 1, 2005; 56(417): 1905 - 1912. [Abstract] [Full Text] [PDF]

				E. Etxeberria, E. Baroja-Fernandez, F. J. Munoz, and J. Pozueta-Romero Sucrose-inducible Endocytosis as a Mechanism for Nutrient Uptake in Heterotrophic Plant Cells Plant Cell Physiol., March 1, 2005; 46(3): 474 - 481. [Abstract] [Full Text] [PDF]

				G.-L. Wu, X.-Y. Zhang, L.-Y. Zhang, Q.-H. Pan, Y.-Y. Shen, and D.-P. Zhang Phloem Unloading in Developing Walnut Fruit is Symplasmic in the Seed Pericarp and Apoplasmic in the Fleshy Pericarp Plant Cell Physiol., October 15, 2004; 45(10): 1461 - 1470. [Abstract] [Full Text] [PDF]

				G. Tallman Are diurnal patterns of stomatal movement the result of alternating metabolism of endogenous guard cell ABA and accumulation of ABA delivered to the apoplast around guard cells by transpiration? J. Exp. Bot., September 1, 2004; 55(405): 1963 - 1976. [Abstract] [Full Text] [PDF]

				S. Munos, C. Cazettes, C. Fizames, F. Gaymard, P. Tillard, M. Lepetit, L. Lejay, and A. Gojon Transcript Profiling in the chl1-5 Mutant of Arabidopsis Reveals a Role of the Nitrate Transporter NRT1.1 in the Regulation of Another Nitrate Transporter, NRT2.1 PLANT CELL, September 1, 2004; 16(9): 2433 - 2447. [Abstract] [Full Text] [PDF]

				J. Watari, Y. Kobae, S. Yamaki, K. Yamada, K. Toyofuku, T. Tabuchi, and K. Shiratake Identification of Sorbitol Transporters Expressed in the Phloem of Apple Source Leaves Plant Cell Physiol., August 15, 2004; 45(8): 1032 - 1041. [Abstract] [Full Text] [PDF]

				J. Price, A. Laxmi, S. K. St. Martin, and J.-C. Jang Global Transcription Profiling Reveals Multiple Sugar Signal Transduction Mechanisms in Arabidopsis PLANT CELL, August 1, 2004; 16(8): 2128 - 2150. [Abstract] [Full Text] [PDF]

				A. Wiese, N. Elzinga, B. Wobbes, and S. Smeekens A Conserved Upstream Open Reading Frame Mediates Sucrose-Induced Repression of Translation PLANT CELL, July 1, 2004; 16(7): 1717 - 1729. [Abstract] [Full Text] [PDF]

				J. C. Lloyd and O. V. Zakhleniuk Responses of primary and secondary metabolism to sugar accumulation revealed by microarray expression analysis of the Arabidopsis mutant, pho3 J. Exp. Bot., June 1, 2004; 55(400): 1221 - 1230. [Abstract] [Full Text] [PDF]

				S. Meyer, C. Lauterbach, M. Niedermeier, I. Barth, R. D. Sjolund, and N. Sauer Wounding Enhances Expression of AtSUC3, a Sucrose Transporter from Arabidopsis Sieve Elements and Sink Tissues Plant Physiology, February 1, 2004; 134(2): 684 - 693. [Abstract] [Full Text] [PDF]

				E. Urbanczyk-Wochniak, A. Leisse, U. Roessner-Tunali, A. Lytovchenko, J. Reismeier, L. Willmitzer, and A. R. Fernie Expression of a Bacterial Xylose Isomerase in Potato Tubers Results in an Altered Hexose Composition and a Consequent Induction of Metabolism Plant Cell Physiol., December 15, 2003; 44(12): 1359 - 1367. [Abstract] [Full Text] [PDF]

				L. A. S. Contim, A. J. Waclawovsky, N. Delu-Filho, C. P. Pirovani, W. R. Clarindo, M. E. Loureiro, C. R. Carvalho, and E. P. B. Fontes The soybean sucrose binding protein gene family: genomic organization, gene copy number and tissue-specific expression of the SBP2 promoter J. Exp. Bot., December 1, 2003; 54(393): 2643 - 2653. [Abstract] [Full Text] [PDF]

				D. Chandran, A. Reinders, and J. M. Ward Substrate Specificity of the Arabidopsis thaliana Sucrose Transporter AtSUC2 J. Biol. Chem., November 7, 2003; 278(45): 44320 - 44325. [Abstract] [Full Text] [PDF]

				R. Wachter, M. Langhans, R. Aloni, S. Gotz, A. Weilmunster, A. Koops, L. Temguia, I. Mistrik, J. Pavlovkin, U. Rascher, et al. Vascularization, High-Volume Solution Flow, and Localized Roles for Enzymes of Sucrose Metabolism during Tumorigenesis by Agrobacterium tumefaciens Plant Physiology, November 1, 2003; 133(3): 1024 - 1037. [Abstract] [Full Text] [PDF]

				L. Lejay, X. Gansel, M. Cerezo, P. Tillard, C. Muller, A. Krapp, N. von Wiren, F. Daniel-Vedele, and A. Gojon Regulation of Root Ion Transporters by Photosynthesis: Functional Importance and Relation with Hexokinase PLANT CELL, September 1, 2003; 15(9): 2218 - 2232. [Abstract] [Full Text] [PDF]

				S. R. Tabaei-Aghdaei, R. S. Pearce, and P. Harrison Sugars regulate cold-induced gene expression and freezing-tolerance in barley cell cultures J. Exp. Bot., June 1, 2003; 54(387): 1565 - 1575. [Abstract] [Full Text] [PDF]

				N. Yoshimoto, E. Inoue, K. Saito, T. Yamaya, and H. Takahashi Phloem-Localizing Sulfate Transporter, Sultr1;3, Mediates Re-Distribution of Sulfur from Source to Sink Organs in Arabidopsis Plant Physiology, April 1, 2003; 131(4): 1511 - 1517. [Abstract] [Full Text] [PDF]

				K. M. Wright, A. G. Roberts, H. J. Martens, N. Sauer, and K. J. Oparka Structural and Functional Vein Maturation in Developing Tobacco Leaves in Relation to AtSUC2 Promoter Activity Plant Physiology, April 1, 2003; 131(4): 1555 - 1565. [Abstract] [Full Text] [PDF]

				S. Cortes, M. Gromova, A. Evrard, C. Roby, A. Heyraud, D. B. Rolin, P. Raymond, and R. M. Brouquisse In Plants, 3-O-Methylglucose Is Phosphorylated by Hexokinase But Not Perceived as a Sugar Plant Physiology, February 1, 2003; 131(2): 824 - 837. [Abstract] [Full Text] [PDF]

				T. Roitsch, M. E. Balibrea, M. Hofmann, R. Proels, and A. K. Sinha Extracellular invertase: key metabolic enzyme and PR protein J. Exp. Bot., January 3, 2003; 54(382): 513 - 524. [Abstract] [Full Text] [PDF]

				S. M. Sherson, H. L. Alford, S. M. Forbes, G. Wallace, and S. M. Smith Roles of cell-wall invertases and monosaccharide transporters in the growth and development of Arabidopsis J. Exp. Bot., January 3, 2003; 54(382): 525 - 531. [Abstract] [Full Text] [PDF]

				K. Juergensen, J. Scholz-Starke, N. Sauer, P. Hess, A. J.E. van Bel, and F. M.W. Grundler The Companion Cell-Specific Arabidopsis Disaccharide Carrier AtSUC2 Is Expressed in Nematode-Induced Syncytia Plant Physiology, January 1, 2003; 131(1): 61 - 69. [Abstract] [Full Text] [PDF]

				C. Kuhn, M.-R. Hajirezaei, A. R. Fernie, U. Roessner-Tunali, T. Czechowski, B. Hirner, and W. B. Frommer The Sucrose Transporter StSUT1 Localizes to Sieve Elements in Potato Tuber Phloem and Influences Tuber Physiology and Development Plant Physiology, January 1, 2003; 131(1): 102 - 113. [Abstract] [Full Text] [PDF]

				R. Atanassova, M. Leterrier, C. Gaillard, A. Agasse, E. Sagot, P. Coutos-Thevenot, and S. Delrot Sugar-Regulated Expression of a Putative Hexose Transport Gene in Grape Plant Physiology, January 1, 2003; 131(1): 326 - 334. [Abstract] [Full Text] [PDF]

				J. Oliveira, R. M. Tavares, and H. Geros Utilization and Transport of Glucose in Olea Europaea Cell Suspensions Plant Cell Physiol., December 15, 2002; 43(12): 1510 - 1517. [Abstract] [Full Text] [PDF]

				R. Datta, K. C. Chamusco, and P. S. Chourey Starch Biosynthesis during Pollen Maturation Is Associated with Altered Patterns of Gene Expression in Maize Plant Physiology, December 1, 2002; 130(4): 1645 - 1656. [Abstract] [Full Text] [PDF]

				M. Stitt Imaging of metabolites by using a fusion protein between a periplasmic binding protein and GFP derivatives: From a chimera to a view of reality PNAS, July 23, 2002; 99(15): 9614 - 9616. [Full Text] [PDF]

				A. Reinders, W. Schulze, C. Kuhn, L. Barker, A. Schulz, J. M. Ward, and W. B. Frommer Protein-Protein Interactions between Sucrose Transporters of Different Affinities Colocalized in the Same Enucleate Sieve Element PLANT CELL, July 1, 2002; 14(7): 1567 - 1577. [Abstract] [Full Text] [PDF]

				F. Rolland, B. Moore, and J. Sheen Sugar Sensing and Signaling in Plants PLANT CELL, May 1, 2002; 14(90001): S185 - 205. [Full Text] [PDF]

				A. K. Sinha, M. G. Hofmann, U. Romer, W. Kockenberger, L. Elling, and T. Roitsch Metabolizable and Non-Metabolizable Sugars Activate Different Signal Transduction Pathways in Tomato Plant Physiology, April 1, 2002; 128(4): 1480 - 1489. [Abstract] [Full Text] [PDF]

				Y. Fujiki, M. Ito, T. Itoh, I. Nishida, and A. Watanabe Activation of the Promoters of Arabidopsis Genes for the Branched-Chain {alpha}-Keto Acid Dehydrogenase Complex in Transgenic Tobacco BY-2 Cells under Sugar Starvation Plant Cell Physiol., March 1, 2002; 43(3): 275 - 280. [Abstract] [Full Text] [PDF]

				C. Oesterhelt and W. Gross Different Sugar Kinases Are Involved in the Sugar Sensing of Galdieria sulphuraria Plant Physiology, January 1, 2002; 128(1): 291 - 299. [Abstract] [Full Text] [PDF]

				S. Roulin and U. Feller Reversible accumulation of (1->3,1->4)-{beta}-glucan endohydrolase in wheat leaves under sugar depletion J. Exp. Bot., December 1, 2001; 52(365): 2323 - 2332. [Abstract] [Full Text] [PDF]

				K. Vissenberg, J. A. Feijo, M. H. Weisenseel, and J.-P. Verbelen Ion fluxes, auxin and the induction of elongation growth in Nicotiana tabacum cells J. Exp. Bot., November 1, 2001; 52(364): 2161 - 2167. [Abstract] [Full Text] [PDF]

				U. Roessner, L. Willmitzer, and A. R. Fernie High-Resolution Metabolic Phenotyping of Genetically and Environmentally Diverse Potato Tuber Systems. Identification of Phenocopies Plant Physiology, November 1, 2001; 127(3): 749 - 764. [Abstract] [Full Text] [PDF]

				T. Furuichi, I. C. Mori, K. Takahashi, and S. Muto Sugar-Induced Increase in Cytosolic Ca2+ in Arabidopsis thaliana Whole Plants Plant Cell Physiol., October 1, 2001; 42(10): 1149 - 1155. [Abstract] [Full Text] [PDF]

				K. Ishimaru, T. Hirose, N. Aoki, S. Takahashi, K. Ono, S. Yamamoto, J. Wu, S. Saji, T. Baba, M. Ugaki, et al. Antisense Expression of a Rice Sucrose Transporter OsSUT1 in Rice (Oryza sativa L.) Plant Cell Physiol., October 1, 2001; 42(10): 1181 - 1185. [Abstract] [Full Text] [PDF]

				R. Turgeon, R. Medville, and K. C. Nixon The evolution of minor vein phloem and phloem loading Am. J. Botany, August 1, 2001; 88(8): 1331 - 1339. [Full Text]

				D. Thorneycroft, S. M. Sherson, and S. M. Smith Using gene knockouts to investigate plant metabolism J. Exp. Bot., August 1, 2001; 52(361): 1593 - 1601. [Abstract] [Full Text] [PDF]

				L. M. Provencher, L. Miao, N. Sinha, and W. J. Lucas Sucrose Export Defective1 Encodes a Novel Protein Implicated in Chloroplast-to-Nucleus Signaling PLANT CELL, May 1, 2001; 13(5): 1127 - 1141. [Abstract] [Full Text]

				J. W. Patrick and C. E. Offler Compartmentation of transport and transfer events in developing seeds J. Exp. Bot., April 1, 2001; 52(356): 551 - 564. [Abstract] [Full Text] [PDF]

				A. R. Fernie, U. Roessner, and P. Geigenberger The Sucrose Analog Palatinose Leads to a Stimulation of Sucrose Degradation and Starch Synthesis When Supplied to Discs of Growing Potato Tubers Plant Physiology, April 1, 2001; 125(4): 1967 - 1977. [Abstract] [Full Text]

				S.-H. Kwak and S. H. Lee The Regulation of Ornithine Decarboxylase Gene Expression by Sucrose and Small Upstream Open Reading Frame in Tomato (Lycopersicon esculentum Mill) Plant Cell Physiol., March 1, 2001; 42(3): 314 - 323. [Abstract] [Full Text] [PDF]

				N. Noiraud, L. Maurousset, and R. Lemoine Identification of a Mannitol Transporter, AgMaT1, in Celery Phloem PLANT CELL, March 1, 2001; 13(3): 695 - 705. [Abstract] [Full Text]

				O. Oswald, T. Martin, P. J. Dominy, and I. A. Graham Plastid redox state and sugars: Interactive regulators of nuclear-encoded photosynthetic gene expression PNAS, January 24, 2001; (2001) 21449998. [Abstract] [Full Text]

				U. Roessner, A. Luedemann, D. Brust, O. Fiehn, T. Linke, L. Willmitzer, and A. R. Fernie Metabolic Profiling Allows Comprehensive Phenotyping of Genetically or Environmentally Modified Plant Systems PLANT CELL, January 1, 2001; 13(1): 11 - 29. [Abstract] [Full Text]

				Y.-L. Ruan, D. J. Llewellyn, and R. T. Furbank The Control of Single-Celled Cotton Fiber Elongation by Developmentally Reversible Gating of Plasmodesmata and Coordinated Expression of Sucrose and K+ Transporters and Expansin PLANT CELL, January 1, 2001; 13(1): 47 - 60. [Abstract] [Full Text]

				J. R. Gottwald, P. J. Krysan, J. C. Young, R. F. Evert, and M. R. Sussman Genetic evidence for the in planta role of phloem-specific plasma membrane sucrose transporters PNAS, November 16, 2000; (2000) 250473797. [Abstract] [Full Text]

				Y. Fujiki, M. Ito, I. Nishida, and A. Watanabe Multiple Signaling Pathways in Gene Expression during Sugar Starvation. Pharmacological Analysis of din Gene Expression in Suspension-Cultured Cells of Arabidopsis Plant Physiology, November 1, 2000; 124(3): 1139 - 1148. [Abstract] [Full Text]

				K. Toyofuku, M. Kasahara, and J. Yamaguchi Characterization and Expression of Monosaccharide Transporters (OsMSTs) in Rice Plant Cell Physiol., August 1, 2000; 41(8): 940 - 947. [Abstract] [Full Text] [PDF]

				A. Weise, L. Barker, C. Kühn, S. Lalonde, H. Buschmann, W. B. Frommer, and J. M. Ward A New Subfamily of Sucrose Transporters, SUT4, with Low Affinity/High Capacity Localized in Enucleate Sieve Elements of Plants PLANT CELL, August 1, 2000; 12(8): 1345 - 1356. [Abstract] [Full Text]

				J. Rexach, E. Fernández, and A. Galván The Chlamydomonas reinhardtii Nar1 Gene Encodes a Chloroplast Membrane Protein Involved in Nitrite Transport PLANT CELL, August 1, 2000; 12(8): 1441 - 1454. [Abstract] [Full Text]

				L. Barker, C. Kühn, A. Weise, A. Schulz, C. Gebhardt, B. Hirner, H. Hellmann, W. Schulze, J. M. Ward, and W. B. Frommer SUT2, a Putative Sucrose Sensor in Sieve Elements PLANT CELL, July 1, 2000; 12(7): 1153 - 1164. [Abstract] [Full Text]

				E. Loreti, A. Alpi, and P. Perata Glucose and Disaccharide-Sensing Mechanisms Modulate the Expression of alpha -amylase in Barley Embryos Plant Physiology, July 1, 2000; 123(3): 939 - 948. [Abstract] [Full Text]

				H. Hellmann, D. Funck, D. Rentsch, and W. B. Frommer Hypersensitivity of an Arabidopsis Sugar Signaling Mutant toward Exogenous Proline Application Plant Physiology, June 1, 2000; 123(2): 779 - 789. [Abstract] [Full Text]

				J. Müller, R. A. Aeschbacher, N. Sprenger, T. Boller, and A. Wiemken Disaccharide-Mediated Regulation of Sucrose:Fructan-6-Fructosyltransferase, a Key Enzyme of Fructan Synthesis in Barley Leaves Plant Physiology, May 1, 2000; 123(1): 265 - 274. [Abstract] [Full Text]

				N. Noiraud, S. Delrot, and R. Lemoine The Sucrose Transporter of Celery. Identification and Expression during Salt Stress Plant Physiology, April 1, 2000; 122(4): 1447 - 1456. [Abstract] [Full Text]

				K. E. Koch, Z. Ying, Y. Wu, and W. T. Avigne Multiple paths of sugar-sensing and a sugar/oxygen overlap for genes of sucrose and ethanol metabolism J. Exp. Bot., February 1, 2000; 51(90001): 417 - 427. [Abstract] [Full Text]

				H. Hellmann, D. Funck, D. Rentsch, and W. B. Frommer Hypersensitivity of an Arabidopsis Sugar Signaling Mutant toward Exogenous Proline Application Plant Physiology, February 1, 2000; 122(2): 357 - 368. [Abstract] [Full Text]

				H. B. Smith Sucrose Synthase and the Fruit of Its Labor PLANT CELL, December 1, 1999; 11(12): 2261 - 2262. [Full Text]

				Y. Zeng, Y. Wu, W. T. Avigne, and K. E. Koch Rapid Repression of Maize Invertases by Low Oxygen. Invertase/Sucrose Synthase Balance, Sugar Signaling Potential, and Seedling Survival Plant Physiology, October 1, 1999; 121(2): 599 - 608. [Abstract] [Full Text]

				M. J. Chrispeels, N. M. Crawford, and J. I. Schroeder Proteins for Transport of Water and Mineral Nutrients across the Membranes of Plant Cells PLANT CELL, April 1, 1999; 11(4): 661 - 676. [Full Text]

				H. Sze, X. Li, and M. G. Palmgren Energization of Plant Cell Membranes by H+-Pumping ATPases: Regulation and Biosynthesis PLANT CELL, April 1, 1999; 11(4): 677 - 690. [Full Text]

				K. J. Oparka and R. Turgeon Sieve Elements and Companion Cells—Traffic Control Centers of the Phloem PLANT CELL, April 1, 1999; 11(4): 739 - 750. [Full Text]

				O. Oswald, T. Martin, P. J. Dominy, and I. A. Graham Plastid redox state and sugars: Interactive regulators of nuclear-encoded photosynthetic gene expression PNAS, February 13, 2001; 98(4): 2047 - 2052. [Abstract] [Full Text] [PDF]

				J. R. Gottwald, P. J. Krysan, J. C. Young, R. F. Evert, and M. R. Sussman Genetic evidence for the in planta role of phloem-specific plasma membrane sucrose transporters PNAS, December 5, 2000; 97(25): 13979 - 13984. [Abstract] [Full Text] [PDF]

This Article Full Text (PDF) Alert me when this article is cited Alert me if a correction is posted Services Email this article to a friend Similar articles in this journal Similar articles in ISI Web of Science Similar articles in PubMed Alert me to new issues of the journal Download to citation manager Citing Articles Citing Articles via HighWire Citing Articles via CrossRef Citing Articles via ISI Web of Science (203) Citing Articles via Google Scholar Google Scholar Articles by Lalonde, S. Articles by Ward, J. M. Search for Related Content PubMed PubMed Citation Articles by Lalonde, S. Articles by Ward, J. M. Agricola Articles by Lalonde, S. Articles by Ward, J. M.