Journal of Experimental Botany

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Journal of Experimental Botany, Vol. 54, No. 382, pp. 525-531, January 1, 2003
© 2003 Oxford University Press

Roles of cell-wall invertases and monosaccharide transporters in the growth and development of Arabidopsis

Received 8 April 2002; Accepted 13 September 2002

Sarah M. Sherson, Heather L. Alford, Susan M. Forbes, Graham Wallace and Steven M. Smith^1,

Institute of Cell and Molecular Biology, University of Edinburgh, The King’s Buildings, Mayfield Road, Edinburgh EH9 3JH, UK

¹ To whom correspondence should be addressed. Fax: +44 (0)131 650 5392. e-mail: s.smith{at}ed.ac.uk

	Abstract

Top Abstract Sugars and the control... Hexose sensing Cell-wall invertases in... Arabidopsis plasma membrane... The specific case of... Future research References

 
The hydrolysis of sucrose by cell-wall invertases (cwINV) and the subsequent import of hexoses into target cells appears to be crucial for appropriate metabolism, growth and differentiation in plants. Hexose uptake from the apoplast is catalysed by monosaccharide/H⁺ symporters (Sugar Transport Proteins or STPs), which have the potential to sense sugars. Import of extracellular hexoses may generate signals to orchestrate cellular activities, or simply feed metabolic pathways distinct from those fed by sucrose. It is predicted that Arabidopsis has six cwINV genes and at least 14 STP genes. These genes show different spatial and temporal patterns of expression, and several knock-out mutants have been isolated for analysis. AtSTP1 transports glucose, galactose, xylose, and mannose, but not fructose. It accounts for the majority of the AtSTP activity in vegetative tissues and its activity is markedly repressed by treatment with exogenous sugars. These observations are consistent with a role in the retrieval of cell-wall-derived sugars, for example, during carbohydrate limitation or cell expansion. The AtSTP1 gene is also expressed in developing seeds, where it might be responsible for the uptake of glucose derived from imported sucrose. The large number of AtcwINV and AtSTP genes, together with complex patterns of expression for each, and the possibility that each protein may have more than one physiological function, provides the plant with the potential for a multiplicity of patterns of monosaccharide utilization to direct growth and differentiation or to respond flexibly to changing environmental conditions.

Key words: Arabidopsis thaliana, cell wall, invertase, mutant, seed development, sugar sensing, sugar transport.

	Sugars and the control of plant growth and development

Top Abstract Sugars and the control... Hexose sensing Cell-wall invertases in... Arabidopsis plasma membrane... The specific case of... Future research References

 
In addition to serving as a source of carbon and energy, sugars are key signalling molecules which can potentially regulate cell division, growth, differentiation, metabolism, and resource allocation in plants (Koch, 1996; Smeekens, 2000). Sucrose is of central importance as a product of photosynthesis and the form in which most carbohydrate is transported between cells and throughout the plant. It is ideally suited to serve as a signalling molecule to co-ordinate source–sink relationships and resource utilization. Evidence for sucrose sensing is provided by the sucrose-induced expression of a sucrose transporter gene (Chiou and Bush, 1998) and repression of translation of ATB2 transcription factor mRNA (Rook et al., 1998). The regulation of metabolism and development by palatinose, a sucrose analogue, further suggests a regulatory role for sucrose (Fernie et al., 2001; Bornke et al., 2002).

In Vicia faba seed development there is a marked switch from hexose to sucrose provision to the embryo, which correlates with a switch from the cell division and morphogenesis phase to the cotyledon expansion and resource accumulation phase (Weber et al., 1997). When embryos at the cell division phase are isolated and incubated with sucrose, nuclear expansion and starch accumulation are promoted, whereas in the presence of hexoses, cell division activity is maintained (Weber et al., 1996). This observation provides strong evidence that these sugars are regulating cell division and differentiation. A similar switch in sugar provision occurs in potato (Solanum tuberosum) as stolons undergo the transition to tuberization (Viola et al., 2001).

The activity of cell-wall invertase (cwINV) will determine whether a cell is provided with apoplastic sucrose or hexoses (Fig. 1). Therefore, cwINV plays a pivotal role in the control of many aspects of plant metabolism, growth and development. In developing Vicia faba seeds, a decline in cwINV activity is observed as the switch is made from hexose to sucrose provision to the embryo. However, the clearest demonstrations of the importance of cwINV come from analyses of the miniature1 mutant of maize (Zea mays) and of antisense inhibition of cwINV synthesis in carrot (Daucus carrota). Seeds of the miniature1 mutant are small because an endosperm-specific cwINV is absent and the endosperm fails to develop (Cheng et al., 1996). Antisense inhibition of cwINV synthesis in carrot roots abolishes tap root formation and leads to increased foliar growth (Tang et al., 1999). In both cases provision of apoplastic hexoses is apparently required for normal development.

View larger version (35K): [in this window] [in a new window]   Fig. 1. Apoplastic sugar uptake and metabolism. Broken arrows represent potential signals. Uncertainty about the route of fructose uptake is indicated by a dashed arrow and question mark. Key: SUC, sucrose transporter; STP, sugar transport protein; FRK, fructokinase; HXK, hexokinase; GK, galactokinase.

 

	Hexose sensing

Top Abstract Sugars and the control... Hexose sensing Cell-wall invertases in... Arabidopsis plasma membrane... The specific case of... Future research References

 
In Saccharomyces cerevisiae, the plasma-membrane-localized, hexose-transporter-like proteins RGT2 and SNF3, sense glucose and relay a signal to a transduction pathway which ultimately leads to the regulation of expression of genes including those encoding functional hexose transporters (Ozcan et al., 1998). Thus extracellular glucose triggers the synthesis of the hexose transporters which catalyse its uptake. It is proposed that a similar glucose-transporter-like protein (RCO3) in Neurospora crassa functions as a sensor rather than a transporter (Madi et al., 1997). In mammals, the glucose transporter GLUT1 has been proposed to function in the sensing, transduction and amplification of a glucose signal without requiring the glucose to be transported (Bandyopadhyay et al., 2000). Furthermore, it has been proposed that a large cytoplasmic loop in the GLUT2 glucose transporter of hepatic cells is involved in glucose signalling (Guillemain et al., 2000). In plants, there are several reports that 3-O-methylglucose (3OMG) and 6-deoxyglucose (6DOG) can trigger changes in plant gene expression (Godt et al., 1995; Roitsch et al., 1995; Martin et al., 1997). These molecules can be transported into plant cells and it is generally believed that they are not metabolized (although this has not been confirmed in the experiments cited). One interpretation of these observations is that glucose (or 3OMG or 6DOG) is sensed by a cell-surface receptor such as a hexose-transporter-type protein (Fig. 1), but no sensor has yet been described.

There are many examples in which hexose metabolism is required for sensing (Rolland et al., 2001). Numerous reports show that substrates for hexokinase cause changes in gene expression, which has led to the proposal that hexokinase is a sugar sensor in yeast and plants (Rolland et al., 2001). While there is still no direct evidence for this (Halford et al., 1999), it is apparent that hexokinase is a key component in the sensing of its substrates (Fig. 1). In pancreatic beta cells it has been proposed that glucokinase may be a sensor, but current evidence suggests that it is simply a rate-limiting step in glucose metabolism, which in turn generates a signal (Rolland et al., 2001).

Galactokinase (GK) is another potential sugar-sensing molecule. In Kluyveromyces lactis, GK has been shown to be a bifunctional protein. In addition to its catalytic activity, in the presence of galactose and ATP it migrates to the nucleus and relieves transcriptional repression of genes required for galactose utilization (Zenke et al., 1996). In Saccharomyces cerevisiae, a protein (Gal3p) with homology to GK, carries out the same function instead of the enzymically-active GK. The plant and fungal GK enzymes are highly conserved (Kaplan et al., 1997). These observations raise the possibility that GK could be a sugar sensor in plants (Fig. 1). Much work is still required to establish how hexose metabolism generates signals in plants, but it is clear that hexoses have important roles to play in the control of growth and development.

Given the importance of cwINV and hexose transorters in plant metabolism, and the possibility that plant hexose transporters or transporter-like proteins might also function in sugar sensing (Lalonde et al., 1999), Arabidopsis thaliana has been adopted as a model to investigate the function of these proteins further.

	Cell-wall invertases in Arabidopsis

Top Abstract Sugars and the control... Hexose sensing Cell-wall invertases in... Arabidopsis plasma membrane... The specific case of... Future research References

 
In plant cells, invertases are found in the cell wall (cwINV), vacuole (vacINV) and cytosol (cytINV). cwINV and vacINV are both acid invertases and their amino acid sequences are more closely related to each other than to the cytINV (neutral) invertases (Sturm, 1999; Sturm and Tang, 1999). Six putative cwINV genes have been identified in the Arabidopsis thaliana genome (AtcwINV genes). Two of these genes have previously been studied and are referred to as ßFRUCT1 and ßFRUCT2 (Tymowska-Lalanne and Kreis, 1998). Since the putative vacINV genes were referred to as ßFRUCT3 and ßFRUCT4 (Tymowska-Lalanne and Kreis, 1998), a revised nomenclature has been adopted here specifically for the AtcwINV genes (Fig. 2). AtcwINV1 has been reported to be expressed in stems, leaves and roots, but not in cotyledons or flowers, while AtcwINV2 expression was flower-specific (Tymowska-Lalanne and Kreis, 1998). Gene-specific primers have been used in RT-PCR reactions to investigate expression of all six genes, and results were obtained for AtcwINV1 and ATcwINV2 that were broadly consistent with Tymowska-Lalanne and Kreis (1998) except that expression of AtcwINV1 is detected in flowers (Fig. 2). All six genes show distinct levels and spatial patterns of expression (Fig. 2). Remarkably, five of the six AtcwINV genes are expressed in developing Arabidopsis seeds (Fig. 2), and of these, four appear to be expressed more strongly in the cell division stages (SM Sherson, unpublished results). While the precise temporal and spatial patterns of expression of these genes remain to be determined, these observations are consistent with the proposal that cwINVs have important roles in seed development.

View larger version (23K): [in this window] [in a new window]   Fig. 2. The Arabidopsis cwINV gene family. Gene sequences were aligned using Clustal W and the phylogenetic tree derived using a PULP (Version 3.1) Heuristic search, with mid-point branching. The relative levels of expression of each gene were determined by RT-PCR using gene-specific primers and RNA from 3-d-old seedlings, expanding rosette leaves, flowers, and developing seeds removed from green siliques. (+) expression, (–) no expression detected (SM Sherson, unpublished results).

 
To investigate the specific functions of AtcwINVs in growth and development, knock-out (KO) mutants (Thorneycroft et al., 2001) were sought for each gene. To date, KOs for four genes have been isolated and none show an abnormal growth phenotype, (SM Sherson, unpublished results). Detailed analysis of these mutants is expected to provide important information on the function of individual cwINV enzymes.

cwINV activity is potentially regulated by specifc inhibitor proteins (Greiner et al., 2000). Therefore, the presence of such proteins should be considered in the context of cwINV activity. The Arabidopsis genome contains approximately 15 genes encoding proteins with sequence similarity to tobacco and tomato cwINV inhibitor proteins. However, the expression patterns of these genes has not yet been investigated.

	Arabidopsis plasma membrane monosaccharide/proton symporters

Top Abstract Sugars and the control... Hexose sensing Cell-wall invertases in... Arabidopsis plasma membrane... The specific case of... Future research References

 
Hexose uptake across the plasma membrane is catalysed by monosaccharide/proton symporters, referred to as sugar transport proteins (STPs). The Arabidopsis thaliana genome contains 14 putative AtSTP genes within a family of at least 50 closely related genes. Most of these related genes are of unknown function, but several are similar to a mannitol transporter from celery (Noiraud et al., 2001). Four different AtSTP proteins have been expressed in heterologous cells (yeast and Xenopus) and shown to catalyse the uptake of exogenous sugars (reviewed by Büttner and Sauer, 2000), and a KO mutation in the AtSTP1 gene results in a decrease in uptake of exogenous monosaccharides by Arabidopsis seedlings (Sherson et al., 2000). These observations are consistent with AtSTPs functioning in the plasma membrane to import monosaccharides from the apoplast. It remains to be determined whether all 14 putative AtSTPs catalyse monosccaharide transport, and what functions other related proteins have. Furthermore, the physiological functions of AtSTPs are unclear (Büttner and Sauer, 2000).

AtSTP1 is a high-affinity (K_m^Glc 50 µM) symporter that transports several monosaccharides, but it transports fructose at a very low rate. The AtSTP1 gene is expressed strongly in leaves, but also in roots, stems, flowers, siliques, and seedlings (Fig. 3; Sauer et al., 1990; Sherson et al., 2000). AtSTP1 is active during seed germination and accounts for approximately 60% of glucose uptake activity in Arabidopsis seedlings (Sherson et al., 2000). Despite these observations, the Atstp1 KO mutant appears to grow and develop normally (Sherson et al., 2000). AtSTP2 is another high-affinity transporter but the AtSTP2 gene is expressed specifically in developing pollen. It is hypothesized that it is responsible for the uptake of glucose derived from callose degradation during pollen maturation (Truernit et al., 1999). AtSTP3 is a low-affinity transporter (K_m^Glc 2 mM Glc) and the AtSTP3 gene is expressed in green tissues, and is induced slowly by wounding (Büttner et al., 2000). AtSTP4 is a high-affinity transporter expressed in root tips, pollen tubes, and leaves. The mRNA level increases appreciably in response to wounding and pathogen attack (Truernit et al., 1996).

View larger version (56K): [in this window] [in a new window]   Fig. 3. Expression of the AtSTP1 gene. Gel blot hybridization using RNA isolated from different organs of flowering plants and an AtSTP1 cDNA probe. Wild-type and Atstp1 mutant plants were analysed. Details of plant growth, gel blot analysis and description of the Atstp1 mutant are given in Sherson et al. (2000).

 
Sequence comparisons (Büttner and Sauer, 2000) show that some AtSTP genes are closely related (eg AtSTP1 and 12; 6 and 8; 9 and 10), but in no cases are the closest relatives physically linked. Furthermore, the close relatives are not necessarily expressed co-ordinately. For example, while AtSTP1 is expressed in many vegetative and reproductive tissues, AtSTP12 is expressed predominantly in developing seeds (SM Sherson, unpublished results). In parallel with studies of AtcwINV gene expression, it was found that at least five AtSTP genes are expressed in developing seeds (SM Sherson, SM Forbes, unpublished results). The effects of KO mutations in AtSTP1 and AtSTP12 on seed development and resource acquisition are under investigation.

	The specific case of AtSTP1

Top Abstract Sugars and the control... Hexose sensing Cell-wall invertases in... Arabidopsis plasma membrane... The specific case of... Future research References

 
In order to investigate the physiological function of AtSTP1, the expression of the AtSTP1 gene was examined in more detail. Extracellular glucose often controls the expression of hexose transporter genes in other eukaryotes in order to regulate its uptake (Boles and Hollenberg, 1997). To determine if the same is true in Arabidopsis, seeds were germinated and seedlings grown for 7 d on medium containing different concentrations of glucose. Total AtSTP activity in whole seedlings was then determined by assaying uptake of [¹⁴C]3OMG (Sherson et al., 2000). The results show that AtSTP activity is markedly reduced by exogenous glucose at a concentration of 1 mM or greater (Fig. 4). By comparing results obtained from wild-type seedlings with those from the Atstp1 KO mutant, it was deduced that AtSTP1 accounts for the majority of this transport activity, and that AtSTP1 and other AtSTPs active in seedlings are repressed by high concentrations of glucose (Fig. 4). These observations imply that AtSTP1 may function to acquire apoplastic sugars when other carbohydrate supplies are limiting. The low K_m of AtSTP1 is consistent with such a role. Furthermore, the substrate specificity of AtSTP1 is similar to the sugar composition of the primary cell wall (Reiter et al., 1997), consistent with a role in salvage of cell-wall-derived sugars (Sherson et al., 2000).

View larger version (41K): [in this window] [in a new window]   Fig. 4. Repression of STP activity by growth of Arabidopsis seedlings on glucose. Wild-type and Atstp1 mutant seedlings were germinated on half-strength Murashige and Skoog medium and grown in the light in the presence of different concentrations of glucose, as described in Sherson et al. (2000). Rates of uptake of [14C]3OMG were assayed as described in Sherson et al. (2000). The rates of uptake due to AtSTP1 activity were derived from the difference between rates of uptake for wild type and Atstp1 mutant (G Wallace, unpublished results).

 
To extend this investigation on the role of AtSTP1, the AtSTP1 promoter was linked to the luciferase reporter gene and introduced into Arabidopsis plants. Imaging of luciferase in 14-d-old plantlets shows that AtSTP1 expression is strongest in young expanding leaves (Fig. 5a), but is also observed in roots (Fig. 5b). These observations are consistent with a role in the uptake of glucose derived from the hydrolysis of apoplastic sucrose in sink tissues. However, the rate of fructose uptake into Arabidopsis plantlets is very much slower than that of glucose (G Wallace, unpublished results), and none of the AtSTPs characterized so far, transports fructose. Therefore, the proposal that AtSTP1 functions in the uptake of monosaccharides released from the cell wall such as during cell expansion, and potentially in other circumstances (Fig. 1), is favoured.

View larger version (79K): [in this window] [in a new window]   Fig. 5. Imaging of AtSTP1 gene expressison with a LUC reporter gene. A 3 kbp AtSTP1 gene promoter fragment was linked to the firefly luciferase gene and introduced into Arabidopsis plants using Agrobacterium-mediated transformation. Plants were grown on half-strength Murashige and Skoog medium in continuous light for 14 d as described in Sherson et al. (2000), then painted with 5 mM luciferin (in 0.01% Triton X-100), dark-incubated for 5 min to reduce chemiluminescence before imaging photon emission using an Andor CCD camera. Images are false-coloured such that increasing photon emission is represented progressively by blue, green, red, yellow, and white. (a) plant viewed from above showing emission predominantly from youngest leaves. (b) plant viewed longitudinally showing emission from shoot and root (HL Alford, unpublished results).

 

	Future research

Top Abstract Sugars and the control... Hexose sensing Cell-wall invertases in... Arabidopsis plasma membrane... The specific case of... Future research References

 
No fructose transporters have yet been identified in Arabidopsis, and there is so far little evidence that the AtSTPs currently characterized are involved in the uptake of hexoses derived from sucrose. Co-expression of specific AtcwINV and AtSTP genes would provide evidence for such a functional link, but so far none exists. Identification of AtSTPs which transport fructose will represent an important advance, and may then help to identify sink tissues in which extensive apoplastic sucrose hydrolysis and hexose uptake occur. The sensing of fructose uptake or phosphorylation would potentially provide the cell with a means to distinguish sucrose-derived hexoses from cell-wall- or callose-derived hexoses, and so to adjust to different physiological states. Whether fructose sensing occurs is speculative at this stage.

It is clear that cwINVs and STPs have very important roles in plant metabolism, growth and development, and that higher plants contain multiple genes encoding these proteins. Arabidopsis currently provides the best opportunity to determine the functions of these proteins through the application of functional genomics resources. KO mutants can not only be used to investigate the functions of individual genes systematically, but can be exploited as recipients for transgenes to engineer novel patterns of cwINV and STP synthesis in order to test the hypothesis that these proteins can direct growth and differentiation in plants.

	Acknowledgement

 
The authors are grateful to the Biotechnology and Biological Sciences Research Council, UK, for financial support.

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