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FEBS Letters 581 (2007) 2318–2324 Minireview The monosaccharide transporter(-like) gene family in Arabidopsis Michael Büttner* Molekulare Pflanzenphysiologie, Universität Erlangen-Nürnberg, Staudtstraße 5, D-91058 Erlangen, Germany Received 14 February 2007; revised 6 March 2007; accepted 7 March 2007 Available online 15 March 2007 Edited by Ulf-Ingo Flügge and Julian Schroeder Abstract The availability of complete plant genomes has greatly influenced the identification and analysis of phylogenetically related gene clusters. In Arabidopsis, this has revealed the existence of a monosaccharide transporter(-like) gene family with 53 members, which play a role in long-distance sugar partitioning or sub-cellular sugar distribution and catalyze the transport of hexoses, but also polyols and in one case also pentoses and tetroses. An update on the currently available information on these Arabidopsis monosaccharide transporters, on their sub-cellular localization and physiological function will be given. Ó 2007 Federation of European Biochemical Societies. Published by Elsevier B.V. All rights reserved. Keywords: Monosaccharide transport; Hexoses; Polyols; Sugar compartmentation; Sink development 1. Introduction In higher plants, sugars play important roles as nutrients as well as signal molecules during the entire life cycle. While the green phototrophic parts of the plant (source) synthesize sugars as products of their photosynthetic activity during the day, non-green parts (sink) depend on a constant import of carbohydrates delivered via the phloem. In addition, source and sink cells allocate sugars between different cellular compartments. This distribution of sugars on the sub-cellular level but also for long-distance transport requires several essential transport steps across membranes [1]. In most higher plants, sucrose is the main transport form for carbon partitioning between source and sink via the phloem [2]. Upon release from the phloem, sucrose is either directly transported into sink cells or, after cleavage of sucrose by an extracellular invertase, the monosaccharides glucose and fructose taken up [3]. There is evidence, that the decision whether sucrose or monosaccharides are delivered greatly influences developmental aspects, as could be demonstrated for the seed development in fava bean [4,5]. In addition to long-distance carbon partitioning, sugars are also distributed on the single cell level into different organelles, depending on the actual requirements. During the day, many plant species use up to half of their assimilated carbon for * Fax: +49 (0) 9131/852 8751. E-mail address: [email protected] starch synthesis and transient storage in chloroplasts of source leaves [6]. At night, transitory starch is degraded phosphorolytically or hydrolytically (primary pathway for export) to release glucose or maltose, respectively [6,7], which can then be exported from the chloroplast. There is a number of biochemical studies providing direct evidence for glucose transport across the chloroplast envelope [8,9]. Furthermore, hexoses can be imported into the vacuole for transient or long-term storage. Experiments on isolated vacuoles provided biochemical evidence for the uptake of hexoses into these organelles , and both mechanisms, passive diffusion as well as active transport have been suggested [10]. Besides plastids and vacuoles there might be other sub-cellular compartments that require the uptake of hexoses and recently it was shown that also mitochondria import glucose [11]. The application of a non-aqueous fractionation technique allowed estimates of the relative amounts of sugars in sub-cellular compartments. Measurements of sugar concentrations in a variety of plants revealed that in leaves the vast majority of glucose is found in the vacuole [12–17] (Lohaus G., personal communication). Besides glucose and fructose, sugar alcohols like sorbitol, mannitol and myo-inositol are found in many plants [18] and may also be transported into vacuoles [19,20]. The transport of sugars across membrane barriers is greatly mediated by transport proteins, which catalyze either passive (but selective) diffusion or energy-dependent active transport thereby allowing accumulation of sugar substrates. Despite the long-standing knowledge of long-distance sugar partitioning and sub-cellular sugar compartmentation, the molecular cloning and characterization of the corresponding transport proteins from higher plants did not succeed for decades. For a long time it was assumed, that each plant has only one transporter for monosaccharides and one transporter for sucrose. However, after the isolation of the first sugar transport protein (AtSTP1) from a higher plant by using the HUP1 gene from the unicellular alga Chlorella kessleri as probe [21,22], things turned out to be more complicated. Further screening approaches using PCR or heterologous hybridization lead to the identification of a family of 14 AtSTP genes in Arabidopsis [23]. While for the uptake of hexoses across the plasma membrane the transport proteins have been identified for a variety of plants [1,24], we are only beginning to identify the proteins responsible for hexose transport on the sub-cellular level (Fig. 2). Only after the completion of the Arabidopsis genome, phylogenetic analysis revealed the existence of a monosaccharide transporter(-like) Gene Family with 53 members, which include good candidates for intra-cellular transporters of 0014-5793/$32.00 Ó 2007 Federation of European Biochemical Societies. Published by Elsevier B.V. All rights reserved. doi:10.1016/j.febslet.2007.03.016 M. Büttner / FEBS Letters 581 (2007) 2318–2324 and sugar alcohols (see also SUBA: the Arabidopsis Subcellular Database; http://www.suba.bcs.uwa.edu.au). The present review tries to summarize the currently available information on these Arabidopsis monosaccharide transporters, on their sub-cellular localization and physiological function. 2. Arabidopsis monosaccharide transporter(-like) gene family The MST(-like) family includes 53 genes with significant homology to known monosaccharide transporters (http:// www.arabidopsis.org/browse/genefamily/Monos.jsp). As depicted in the phylogenetic tree of Fig. 1, these genes can be grouped into seven distinct sub-families, which clearly have one common origin. All of these transporters share strong similarities in their membrane topology with 12 predicted membrane spanning domains (http://aramemnon.botanik. uni-koeln.de). Within the sub-families, the homologies are quite high, ranging from 42% to 96% similarity. When the subfamilies are compared to each other, the degree of homology significantly drops supporting the grouping of these genes into distinct families. Although in some cases the overall homology to the already characterized sugar transporters is relatively low, all of these proteins show conserved amino acid clusters including two known sugar transport signatures (http://ca.expasy.org/ cgi-bin/nicedoc.pl?PDOC00190), which strongly support a function of these proteins as sugar transporters. 3. AtSTP (Sugar Transport Protein) genes To date, the AtSTPs represent the best characterized family of hexose transporters in Arabidopsis. All known AtSTPs are 2319 plasma membrane proteins and catalyze the uptake of hexoses from the apoplastic space into the cell. AtSTP1 was the first monosaccharide transporter identified in a higher plant [21]. Expression in Schizosaccharomyces pombe and Xenopus oocytes revealed that AtSTP1 is a high-affinity monosaccharide/ proton symporter capable of transporting a range of hexoses but not fructose [25]. AtSTP1 is most abundant in germinating seeds and seedling roots [26], where it accounts for up to 60% of the monosaccharide transport capacity as was shown by uptake studies with an Atstp1 mutant line. Furthermore, AtSTP1 is expressed in guard cells of cotyledons, rosette leaves, sepals, ovaries and stems [27]. In this cell type, AtSTP1 expression is strongly increased in the dark and also diurnally regulated with a peak around midday, which is paralleled by an accumulation of sucrose in guard cells. Thus, a function of AtSTP1 in monosaccharide import into guard cells during the night and a possible role in osmoregulation during the day was suggested [27]. The AtSTP4 gene encodes another high-affinity hexose transporter and is expressed in root tips, pollen tubes, and leaves. Interestingly, AtSTP4 expression strongly increases in response to wounding and pathogen attack [28]. Moreover, the coordinated expression of AtSTP4 and the invertase gene Atbfruct1 (AtcwINV1; At3g13790) in the host response to powdery mildew infection could be demonstrated [29], further supporting the functional interaction of STPs and cell wall invertases in the supply of sink tissues with hexoses. The high-affinity hexose transporter AtSTP2 is found specifically in pollen, where it most likely is responsible for the uptake of glucose derived from callose degradation during early phases of pollen maturation [30]. Surprisingly, three more hexose transporter genes, AtSTP6, AtSTP9 and AtSTP11, were found to be expressed in pollen during different stages of pollen development [31–33]. AtSTP6 expression is confined to the Fig. 1. Phylogenetic tree of the monosaccharide transporter(-like) gene family in Arabidopsis. The complete protein sequences of the MSTs were aligned using the Clustal X algorithm and a phylogenetic tree was constructed using the TreeView 1.6 software. Sub-family names, Munich Information Center for Protein Sequences (MIPS) codes and gene names (where available) are indicated. 2320 latest stage in pollen development, when the exine is formed and the grain is fully developed [32]. AtSTP9, the only AtSTP known to be specific for glucose, shows an interesting regulation. While the AtSTP9 mRNA was already detectable during early pollen development, the AtSTP9 protein is found only after pollen germination in the pollen tube [31]. A similar regulation was also found for the AtSTP4 gene (R. Stadler, personal communication). This preloading of pollen with transcripts has already been described for other genes that play a role in pollen germination and/or pollen tube growth [34]. Finally, AtSTP11 was characterized as a pollen tube-specific monosaccharide transporter [33]. In view of the high number of AtSTPs found in pollen it is surprising that no hexose transporter was identified in the female gametophyte to date. Recently, another high-affinity hexose transporter gene, AtSTP13, was shown to be expressed in vascular tissue of petals and to be induced during programmed cell death (PCD), suggesting that hexose transport plays a role in PCD in plants [35]. All so far characterized AtSTPs are high-affinity hexose transporters ðK Glc M 10-100 lMÞ found in sink tissues with one exception: AtSTP3 has an unusually low affinity for glucose ðK Glc M 2 mMÞ and the AtSTP3 gene is expressed in green tissues, where it is proposed to have a function in sugar retrieval [23]. Interestingly, AtSTP3 is also inducible by wounding and pathogen attack. In summary, the AtSTPs are high-affinity (except AtSTP3) monosaccharide/H+ symporters of the plasma membrane, which have Km-values for glucose in the micro-molar range and accept a broad spectrum of monosaccharide substrates (except AtSTP9). The observed AtSTP expression profiles suggest important roles during sink development (except for AtSTP3). 4. AtVGT (Vacuolar Glucose Transporter)-like genes As shown in Fig. 1, the sub-family which stands closest to the AtSTPs is comprised of three genes, At3g03090, At5g17010 and At5g59250, which in several databases are annotated as putative sugar transporters similar to the bacterial xylose permease LbXylT (gi:2895856; Acc AF045552). However, LbXylT shows significant homology to most MSTlike Transporters ranging from 26% to 42%. In fact, the polyol transporter PLT6 shows the highest homology to LbXylT, and several other transporters from different MST-like sub-families share the same degree of similarity to this bacterial xylose transporter as the VGT-like proteins, indicating that the homology does not necessarily reflect substrate specificity. Recently, two genes from this family, AtVGT1 (At3g03090) and AtVGT2 (At5g17010), have been shown to localize to the vacuolar membrane [36]. For AtVGT1, active transport of glucose but not xylose was demonstrated by functional expression in yeast and uptake studies in isolated yeast vacuoles. AtVGT1 is strongly expressed in pollen, at basal levels in leaves and stems and not detectable in roots. The analysis of Atvgt1 mutant lines indicate an important function of this vacuolar glucose transporter during developmental processes like seed germination and flowering [36]. In contrast, the gene product of At5g5925, the third member of this sub-group, seems to be localized in the chloroplast membrane. The encoded protein has an N-terminal extension carrying a potential plastid target signal and was identified in chloroplast membrane prepara- M. Büttner / FEBS Letters 581 (2007) 2318–2324 tions during independent proteomic approaches (see SUBA database: http://www.suba.bcs.uwa.edu.au). 5. AtTMT (Tonoplast Monosaccharide Transporter) genes The AtTMT sub-family is composed of three MST homologs with an extended middle loop between the putative transmembrane helices six and seven. Such an extended cytoplasmic domain is also present in the sucrose transporter AtSUT2/AtSUC3, which was therefore discussed as possible sugar sensor [37] due to the structural resemblance to the yeast glucose sensors SNF3 and RGT2. However, neither for AtSUT2/AtSUC3 nor for the AtTMTs a function in sugar sensing could be demonstrated so far. Proteomic studies of the Arabidopsis and barley tonoplast indicated the presence of AtTMT transporters in the vacuolar membrane [38,39]. This could be further supported in a recent study by Wormit and coworkers, showing that AtTMT-GFP fusions localize to the tonoplast and that Attmt mutant lines upon cold stress accumulate less glucose in the vacuole than wildtype plants [40]. AtTMT1 and AtTMT2 expression is induced by stresses like drought, salt and cold and by sugars indicating that AtTMTs play a role in vacuolar hexose transport, mainly under stress conditions. (For additional information on vacuolar transporters see also E. Neuhaus, ‘‘Vacuolar transport’’; in this issue). 6. AtpGlcT (Plastidic Glucose Transporter) genes/AtSGB1 (Suppressor of G Protein Beta1) Using a differential labeling strategy, a putative glucose transporter pGlcT of the chloroplast inner envelope membrane was identified in spinach [41]. The corresponding gene in Arabidopsis has three close homologs (43–71% amino acid similarity), which together form the sub-family of putative plastidic glucose transporters, named after the spinach pGlcT. A function of pGlcTs in the export of glucose derived from the amylolytic breakdown of transitory starch was suggested [41], however, a direct proof of transport activity as well as a mutant analysis to support this function is missing to date. Interestingly, it was recently suggested that plastidic glucose efflux is an active process coupled with the transport of a proton [9]. (For detailed information on chloroplast glucose transporters see also Weber and Fischer, ‘‘Plastid Transport’’; in this issue). Despite the high homology (42–69% similarity) within this sub-family, not all members are found in plastids. Recently, SGB1 (suppressor of G protein beta1) was identified as a Golgi-localized hexose transporter homolog [42]. Arabidopsis agb1 mutant seedlings, which lack the b-subunit (AGB1) of the heterotrimeric G protein complex, have reduced number of cells due to altered cell division in the hypocotyl and are D -glucose hypersensitive. In a screen for gain-of-function suppressors of the agb1 mutation, SGB1 was found to restore cell number and hypocotyl length. Some components of the newly synthesized cell wall like pectins and xyloglucans are assembled in the Golgi. One explanation, how SGB1 overexpression could rescue hypocotyl length in the agb1 mutant, could be elevated glucose transport into the Golgi thereby increasing cell wall synthesis [42]. It will be interesting to see, whether this sub-family is further divided into groups with different sub-cellular localization and function. M. Büttner / FEBS Letters 581 (2007) 2318–2324 7. AtPLT (Polyol Transporter) genes Polyols are osmotically active solutes that accumulate in a number of plants in response to cold, water or salt stress [18]. The first plant mannitol transporter AgMaT1 was isolated from celery by complementation of a yeast mutant [43]. Also in Arabidopsis, sugar alcohols seem to play a role and the corresponding transport proteins have been identified and partially characterized [44–46], but so far the physiological functions of these transporters are unclear. Within the MST(-like) family, six genes share significant homology with previously identified polyol transporters. Analysis of AtPLT5, the first member of this sub-group, revealed that this transporter resides in the plasma membrane and is a broad-spectrum H+-symporter for linear polyols, such as sorbitol, xylitol, erythritol, or glycerol, but also the cyclic polyol myo-inositol and different hexoses and pentoses including ribose, tetroses and a sugar acid [44,45]. AtPLT5 is primarily expressed in sink tissues, most strongly in the root elongation zone, but also in the vascular tissue of leaves and some floral organs like siliques and the floral abscission zone [44,45]. Polyols are also found in the vacuole. In celery, mannitol is transiently stored in the vacuoles of the parenchyma cells of petioles where it crosses the tonoplast by passive diffusion [20]. In contrast, sorbitol is actively transported into vacuoles in apple fruit [19]. However, none of the AtPLT gene products was localized to the tonoplast so far. 8. AtINT (Inositol Transporter) genes Inositol (in muscle cells called myo-inositol) is an ubiquitous cellular component in a variety of organisms including plants. 2321 It is mostly phosphorylated and functions in cellular signalling (inositol triphosphate, IP3), as structural component of membranes (phosphatidylinositol) and as storage form of phosphorus in seeds (phytate). The four members of the Arabidopsis MST(-like) family show strong homology to myoinositol transporters from yeast and human and to the myo-inositol transporters MITR1 and MITR2 from Mesembryanthemum crystallinum (common ice plant) [47]. In contrast to MITR1 and MITR2, which are thought to catalyze Na+/myo-inositol symport and were localized in the tonoplast, the Arabidopsis AtINT4 is a highly specific myo-inositol/proton symporter and was found in the plasma membrane [46]. AtINT4 is strongly expressed in pollen and phloem companion cells, where it could function in phloem loading with myo-inositol, possibly to allow raffinose synthesis [46]. MITR1 and MITR2 from M. crystallinum were found in the tonoplast and are thought to play a role in salt tolerance. Interestingly, in a recent proteome analysis, AtINT1, another member of this Arabidopsis sub-family, was also identified as a vacuolar membrane protein. However, since proteomic approaches often produce a small number of false-positives, this result has to be reconfirmed by an independent method. 9. AtERD6-like genes The 19 AtERD6-like genes represent the least investigated sub-group in the MST(-like) family, which share 48–95% similarity with each other. The AtERD6-homologs were named after the ERD6 (early-responsive to dehydration) gene, which is coding for a putative sugar transporter [48]. The ERD6 gene is induced upon dehydration and cold treatment, but expression studies in yeast were not successful in proving sugar Fig. 2. Schematic illustration of the sub-cellular distribution of monosaccharides and the localization determined for MST(-like) transporters. The transport direction for glucose, fructose and polyols into the cell and within the cell is indicated by arrows and the corresponding transporter names are given in boxes (STP: Sugar Transport Protein, VGT: Vacuolar Glucose Transporter, TMT: Tonoplast Monosaccharide Transporter, pGlcT: Plastidic Glucose Transporter, SGB1: Suppressor of G protein Beta1, PLT: Polyol Transporter, INT: Inositol Transporter, ERD6-like: earlyresponsive to dehydration). 2322 transport activity [48]. Furthermore, this family includes two closely related MST homologs, SFP1 and SFP2 (sugar-porter family protein), that are found as tandem genes on chromosome 5 [49]. Both genes are differentially regulated and SFP1 was shown to be senescence-induced, which is paralleled by an accumulation of monosaccharides in such tissues. However, for both, SFP1 and SFP2, the functional characterization is missing so far. Interestingly, some AtERD6 genes show high homology to a putative sugar transporter from Beta vulgaris, that was shown to be located in the vacuolar membrane by co-localization studies, but also for this sugar beet homolog transport activity could not be demonstrated [50]. A similar localization for at least some members of the AtERD6 subgroup was suggested by expression studies of GFP fusion proteins (Büttner and Hannich, unpublished results). This is further supported by the identification of At1g75220 and At1g19450, the two AtERD6 members most homologous to the sugar beet transporter, in a recent proteomic search for tonoplast proteins [39]. The AtERD6 genes also show considerable homology to the mammalian GLUT family. These glucose transporters are facilitators, which raises the possibility that the AtERD6 transporters differ from the known plant monosaccharide transporters mechanistically. So far, such sugar transporters that facilitate an energy-independent monosaccharide transport (influx and/or efflux) have not been identified in plants. Possibly, AtERD6 homologs play a role in the transport of sugars out of the vacuole during conditions, where a re-allocation of carbohydrates is important (Fig. 2). Such conditions include senescence, wounding, pathogen attack, C/N-starvation as well as diurnal changes in transient storage of sugars in the vacuole. According to the Genevestigator database (https://www.genevestigator.ethz.ch), several of the AtERD6 genes are strongly regulated in response to some of these developmental and environmental signals. 10. Conclusions The availability of complete plant genomes has greatly influenced the identification and analysis of phylogenetically related gene clusters. In Arabidopsis, this has lead to an enormous progress in the elucidation of common functional characteristics but also divergence within gene families like the monosaccharide transporter(-like) gene family. In deed, MST genes form distinct sub-families share certain features, however, the currently available data also show that the degree of homology does not necessarily reflect sub-cellular localization or substrate specificity. So far, substrate sugars known to be transported by MSTs include mainly hexoses, but also polyols and in one case (AtPLT5) also pentoses and tetroses. 11. Monosaccharide transporters in other plants The number of EST libraries and even complete genomes from different plant species is constantly growing. The evolutionary aspects of plant monosaccharide transporters have been addressed recently by Johnson et al. [51], and in this excellent study the authors conclude that the seven MST sub-families of Arabidopsis are ancient in land plants and all have homologs present in land plants at least 400 million years M. Büttner / FEBS Letters 581 (2007) 2318–2324 ago. In some cases, the analysis of the corresponding orthologs in other plants might help to elucidate the biological function of MST(-like) transporters. 12. Future goals Despite the appreciable progress in the analysis of MST(like) transporters in Arabidopsis, important questions concerning individual members but also entire sub-families have to be addressed in the future. (i) There is an exceptionally high number of AtSTPs expressed in pollen. This is particularly surprising, since in vitro pollen germination requires sucrose and the addition of glucose leads to an instantaneous burst of the pollen tubes [52]. AtSTPs are found during different stages of pollen development, however, knockouts mutants of individual AtSTPs are fertile and not affected in pollen maturation [31–33]. The importance of sugar supply during this essential step in plant reproduction has to be further demonstrated by the analysis of multiple AtSTP knockout mutants to determine the distinct roles of individual AtSTPs during pollen development, germination, and pollen tube growth. (ii) Another open question is how fructose, which is generated by sucrose-cleavage in the apoplast, enters the cell. Only two of the so far characterized AtSTPs transport fructose at significant rates but they are not expressed in all sink tissues [32,35]. Either the AtSTP transport properties found in heterologous systems do not completely reflect the in planta situation, or another family of plasma membrane transporters is responsible for the fructose uptake (Fig. 2), as recently suggested for AtPLT5 [44,45]. (iii) Candidates from different sub-families have been localized to the same compartment. This was found for AtVGTs, AtTMTs and several AtERD6-homologs in the vacuolar membrane and for pGlcT and one AtVGT-homolog in the chloroplast membrane. It will be important to sort out the individual functions and requirements of these transporters in the corresponding compartment. In addition, it was shown recently that within the plasma membrane so-called lipid rafts form microdomains leading to an intra-membrane compartmentation. Interestingly, the HUP1 hexose transporter is restricted to such microdomains in yeast [53]. It remains to be seen if this compartmentation within membranes is important for the activity/stability of plant MSTs and if it is also found in intracellular membranes. (iv) Relatively little is known about the regulation of MSTs on both, the transcriptional and post-transcriptional level. Microarray data indicate an effect of a wide range of developmental and external factors on the expression of MST genes. In grape vine, the promoter of the hexose transporter gene VvHT1 contains two sugar boxes, and its activity is induced by sucrose and glucose. Furthermore, binding of the ABA-inducible transcription factor VvMSA to these promoter boxes was demonstrated, suggesting that VvMSA is involved in a common transduction pathway of sugar and ABA signaling [54]. In addition, MST-mediated sugar transport might be regulated on the protein level. A large-scale screening for M. Büttner / FEBS Letters 581 (2007) 2318–2324 in vivo phosphorylated membrane proteins identified a phosphorylation-site in the AtSTP1 protein (Nühse T.S. and Peck S.C., personal communication) [55] and studies with kinase activators suggest that AtSTP13 is negatively regulated by phosphorylation [35]. 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