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HIGH IMPACT

How Sweet It Is: Identification of Vacuolar Sucrose Transporters

University of Illinois
Urbana, IL 61801

Vacuoles have diverse functions within all plant cells. Vacuoles get rid of wastes, accumulate nutrients, and regulate pressure within a cell. They are also known to store sugars. Many of the compounds within vacuoles are actively transported across the tonoplast membrane against a concentration gradient via transporters. The identification of transporters involved in vacuolar Suc transport was the focus of the study by Endler et al. (2006) titled "Identification of a Vacuolar Sucrose Transporter in Barley and Arabidopsis Mesophyll Cells by a Tonoplast Proteomic Approach." This article appeared in the May 2006 issue, and as of June 2009 it has garnered 44 citations.

	BACKGROUND

TOP BACKGROUND WHAT WAS SHOWN THE IMPACT CONCLUSION LITERATURE CITED

 
The majority of compounds found in the vacuole were imported by the use of transporters, which usually take compounds across the tonoplast via proton pumps (for review, see Neuhaus, 2007). Large concentrations of Suc, Glc, and Fru are all found within vacuoles (for review, see Neuhaus, 2007). Inhibition of Suc export increases cytoplasmic Suc concentrations, which inhibits photosynthesis (Endler et al., 2006). Suc accumulation in vacuoles is also important for primary metabolism in storage tissues (for review, see Neuhaus, 2007); however, only a small number of vacuolar transporters have been identified, despite the demonstration by numerous vacuolar localization and transport studies that a large number are present and remain uncharacterized. These transporters are vital to understanding how cytosolic homeostasis is regulated and can help to better understand complex cell processes, including sink-to-source relations.

Nine Suc transporter-like sequences (SUCs; also called SUTs) have been reported in the Arabidopsis (Arabidopsis thaliana) genome sequences: AtSUC1 to AtSUC9 (for review, see Sauer, 2007). Of these nine, all but AtSUC6 and AtSUC7 were found to encode functional Arabidopsis Suc transporters; AtSUC6 and AtSUC7 coded for nonfunctional proteins (Sauer et al., 2004; Sauer, 2007). As more plant Suc transporters were sequenced, four distinct groups emerged. One of these, group 4, was originally characterized to consist of plasma membrane-localized Suc transporters (Weise et al., 2000; Weschke et al., 2000). However, a recent study by Endler et al. (2006) found a member of this group in tonoplast membranes. The research by Endler et al. (2006) is significant in suggesting that several group 4 transporters may represent vacuolar Suc transporters that are primarily expressed in sink tissues.

	WHAT WAS SHOWN

TOP BACKGROUND WHAT WAS SHOWN THE IMPACT CONCLUSION LITERATURE CITED

 
A proteomic study of tonoplast membrane was undertaken by Endler et al (2006) to identify vacuolar membrane proteins, in particular, transporters, involved in vacuolar Suc import and release. The protein fraction from barley (Hordeum vulgare) tonoplast membranes was isolated, and 101 proteins were identified. The ratio of nonvacuolar to vacuolar proteins was low, and the authors felt confident of the purity of the preparation. Of these proteins, 60 had been identified in previous studies, while the remaining 40 had not been annotated as vacuolar proteins, including two transporters: a peptide transporter and the Suc transporter HvSUT2.

HvSUT2 had been previously identified from a barley seed library and shown to be expressed in both sink and source tissues and can facilitate Suc uptake in the yeast Saccharomyces cerevisiae (Weschke et al., 2000). Interestingly, SUT2 homologues from the Solanaceae (LeSUT4 and StSUT4) were localized to the plasma membrane in sieve tubes elements (Weise et al., 2000) as well as the endomembrane system (Chincinska et al., 2008), and not to the vacuole, suggesting a different role in the Solanaceae for SUT4, most likely involving Suc loading to the phloem. The Arabidopsis homologue to HvSUT2, AtSUT4, has also shown to be expressed in sink tissues (Weise et al., 2000), but its subcellular location was not clear. To confirm the tonoplast localization of HvSUT2 as well as the localization of AtSUT4, GFP fusion proteins were constructed with the two transporters. Transient expression in onion (Allium cepa) epidermis as well as Arabidopsis confirmed the tonoplast membrane localization to both proteins, suggesting a role for these two transporters in the exchange of sugars between the vacuole and cytoplasm rather than phloem loading, as localization studies suggest for LeSUT4 and StSUT4.

	THE IMPACT

TOP BACKGROUND WHAT WAS SHOWN THE IMPACT CONCLUSION LITERATURE CITED

 
A Suc transporter homologous to HvSUT2, LjSUT4, was characterized from Lotus japonicus (Reinders et al., 2008) and shown to transport a variety of glucosides with a low affinity for Suc, as was seen with AtSUT4 (Weise et al., 2000). Transport by LjSUT4 was demonstrated to be proton coupled and sensitive to the addition of the protonophore carbonyl cyanide m-chlorophenylhydrazone. As was found in barley (Endler et al., 2006), LjSUT4-GFP fusion constructs were localized to the vacuolar membrane in Arabidopsis and, in addition, the legume Medicago truncatula. The authors of this study have proposed that LjSUT4 is involved in the uptake of Suc from the vacuole to the cytoplasm and, since it has the ability to transport other glucosides, might play a role in multiple pathways for exporting Glc conjugates from the vacuole.

Knowing the transporters involved in Suc exchange between the vacuole and cytoplasm has the potential for a greater application. When exploring potential crops for bioenergy production, it is desirable to move away from using foodstock crops or converting land from foodstock to bioenergy crops. The ability to use agronomically marginal or degraded lands is preferred but limited by the plants that will grow in such an environment, especially in arid conditions. One group of plants that can be used is Crassulacean acid metabolism plants, which are very water use efficient. However, there is a tradeoff with plants adapted to life in water-limiting environments in the form of a constraint to carbon sequestration. To fully utilize Crassulacean acid metabolism plants as a biofuel source or further as a crop plant, more studies must be conducted on the molecular, biochemical, and physiological levels (for review, see Borland et al., 2009). Knowing the transporters involved in Suc exchange between the vacuole and cytoplasm is one piece to the puzzle, as it will further the understanding of how photoassimiliates are moved between these two compartments during the day/night cycle.

	CONCLUSION

TOP BACKGROUND WHAT WAS SHOWN THE IMPACT CONCLUSION LITERATURE CITED

 
The identification of members of the group 4 Suc transporters, HvSUT2, AtSUT4 (Endler et al., 2006), and now LjSUT4 (Reinders et al., 2008), as tonoplast localized suggests a role in the exchange of glucosides between the cytoplasm and vacuole. The identification of these transporters and further elucidation of how they are regulated will enable a greater understanding of the movement of Suc within a cell and ultimately through the plant.

	FOOTNOTES

 
www.plantphysiol.org/cgi/doi/10.1104/pp.109.900295

	LITERATURE CITED

TOP BACKGROUND WHAT WAS SHOWN THE IMPACT CONCLUSION LITERATURE CITED

 
Borland AM, Griffiths H, Hartwell J, Smith JAC (2009) Exploiting the potential of plants with Crassulacean acid metabolism for bioenergy production on marginal lands. J Exp Bot (in press)

Chincinska IA, Liesche J, Krugel U, Michalska J, Geigenberger P, Grimm B, Kuhn C (2008) Sucrose transporter StSUT4 from potato affects flowering, tuberization, and shade avoidance response. Plant Physiol 146: 515–528[Abstract/Free Full Text]

Endler A, Meyer S, Schelbert S, Schneider T, Weschke W, Peters SW, Keller F, Baginsky S, Martinoia E, Schmidt UG (2006) Identification of a vacuolar sucrose transporter in barley and Arabidopsis mesophyll cells by a tonoplast proteomic approach. Plant Physiol 141: 196–207[Abstract/Free Full Text]

Neuhaus HE (2007) Transport of primary metabolites across the plant vacuolar membrane. FEBS Lett 581: 2223–2226[CrossRef][Web of Science][Medline]

Reinders A, Sivitz AB, Starker CG, Gantt JS, Ward JM (2008) Functional analysis of LjSUT4, a vacuolar sucrose transporter from Lotus japonicus. Plant Mol Biol 68: 289–299[CrossRef][Web of Science][Medline]

Sauer N (2007) Molecular physiology of higher plant sucrose transporters. FEBS Lett 581: 2309–2317[CrossRef][Medline]

Sauer N, Ludwig A, Knoblauch A, Rothe P, Gahrtz M, Klebl F (2004) AtSUC8 and AtSUC9 encode functional sucrose transporters, but the closely related AtSUC6 and AtSUC7 genes encode aberrant proteins in different Arabidopsis ecotypes. Plant J 40: 120–130[CrossRef][Web of Science][Medline]

Weise A, Barker L, Kuhn C, Lalonde S, Buschmann H, Frommer WB, Ward JM (2000) A new subfamily of sucrose transporters, SUT4, with low affinity/high capacity localized in enucleate sieve elements of plants. Plant Cell 12: 1345–1355[Abstract/Free Full Text]

Weschke W, Panitz R, Sauer N, Wang Q, Neubohn B, Weber H, Wobus U (2000) Sucrose transport into barley seeds: molecular characterization of two transporters and implications for seed development and starch accumulation. Plant J 21: 455–467[CrossRef][Web of Science][Medline]

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