PerspectivePlant Science

SWEET! The Pathway Is Complete

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Science  13 Jan 2012:
Vol. 335, Issue 6065, pp. 173-174
DOI: 10.1126/science.1216828

Photosynthesis in plants leads to the accumulation of carbohydrates (e.g., sugars, starch), upon which all terrestrial life depends. In most plants, sucrose is the principal carbohydrate transported long-distance in the veins to support the growth and development of roots, flowers, fruits, and seeds. Sucrose can be directly stored in specialized tissues, such as fruits or the stems of sugarcane and sweet sorghum, or it can be converted into starch in cereal seeds and potato tubers. Thus, proper control of carbohydrate partitioning is fundamental to crop yield and human nutrition and to the development of plant-based biofuels. Given the importance of this process, it may come as a surprise that until now, we did not understand the entire pathway for the export of sucrose from leaves. On page 207 of this issue, Chen et al. (1) identify and characterize the long-sought missing player in sucrose transport, the sucrose effluxer.

Carbon assimilation in mature leaves results in a surplus of carbohydrates, which are exported through the veins to nonphotosynthetic tissues (27). Sucrose is synthesized in leaf mesophyll cells and diffuses cell-to-cell through plasmodesmata (conduits spanning the cell wall and connecting adjacent cells) toward the vein (see the figure). Within the veins, the phloem is the specialized tissue involved in long-distance sucrose transport. The phloem contains three cell types: parenchyma cells, companion cells, and sieve elements. In the majority of crop plants, the companion cells and sieve elements are not connected by plasmodesmata to the other cells in the leaf; therefore, sucrose must be effluxed from the phloem parenchyma cell to the cell wall space (apoplast) before being imported into the companion cells and/or sieve elements by sucrose transporters located on their plasma membranes (27). The portions of the sucrose transport pathway from the mesophyll cell to the phloem parenchyma cell, and from the apoplast into the companion cell and sieve element, have been well characterized. However, the mechanism of sucrose efflux into the apoplast, the last unresolved step in the sucrose phloem loading pathway, remained a mystery (8). The sucrose effluxer was finally identified by Chen et al. through an elegant approach that combined cell biology, biochemistry, genomics, and genetics.

Sucrose partitioning in plants.

Sucrose is synthesized in leaf mesophyll cells and diffuses through plasmodesmata into phloem parenchyma cells. SWEET proteins facilitate sucrose efflux into the cell wall (apoplast). Sucrose transporters import sucrose into companion cells and/or sieve elements. Sucrose is transported through sieve elements out of leaves to nonphotosynthetic tissues, such as roots, stem, and fruits.

CREDIT: Y. HAMMOND/SCIENCE

A key that enabled this breakthrough was the development of fluorescence resonance energy transfer (FRET) optical sensors that could be used in cells to report the sugar concentration in the cytoplasm (9, 10). A sugar-binding protein domain was placed between variants of cyan fluorescent protein and yellow fluorescent protein. When the sensor protein binds sugar, it undergoes a conformational shift that alters the fluorescence, such that a change in the amount of fluorescence emitted can be used to monitor changes in sugar concentration. By expressing such an optical sensor for glucose or sucrose, root cells were observed to rapidly transport the sugars across cellular membranes in response to concentration gradients (11). This led to the hypothesis that novel membrane proteins mediate sugar transport because the expression patterns and biochemical transport properties observed were inconsistent with known sugar transporters.

To identify these unknown proteins, Chen et al. previously used a human cell line to coexpress the glucose sensor and a collection of Arabidopsis proteins containing multiple membrane-spanning domains (12). The authors found that a specific SWEET protein could take up glucose from the cell culture medium. SWEETs are membrane proteins that transport glucose molecules across a membrane down a concentration gradient. Phylogenetic analysis revealed that SWEET genes are evolutionarily conserved from plants to humans. There are 17 SWEET genes in Arabidopsis and 21 in rice. Intriguingly, different bacterial or fungal pathogens obtain carbohydrates from plants by increasing the expression of different plant SWEET genes (12).

Chen et al. determined that AtSWEET11 and 12 (and OsSWEET11 and 14 in rice) transport sucrose in Arabidopsis (1). Both transporters localize to the plasma membrane and are expressed in a subset of leaf phloem parenchyma cells, proximal to the companion cells and sieve elements. Mutations in either the AtSWEET11 or 12 genes produced no obvious phenotypes, but double mutants (atsweet11;12) showed moderate defects in sucrose phloem transport and an excessive accumulation of carbohydrates in the leaves. A third gene, AtSWEET13, showed increased expression in the atsweet11;12 double mutant background and may partially compensate for their function. Hence, these SWEET genes are genetically redundant, which likely explains why earlier genetic screens failed to identify the efflux step. Collectively, the data demonstrate that the AtSWEET11 and 12 genes encode the missing link in sucrose phloem loading, the sucrose effluxer.

The identification of SWEET proteins as sucrose facilitators raises a number of questions. Are the regulation and localization of SWEETs and sucrose transporters coordinated to maximize phloem loading efficiency and minimize any potential loss of sucrose to the apoplast (and thereby to pathogens)? Additionally, AtSWEET11 and 12 are expressed in most Arabidopsis tissues; what other roles beyond phloem loading might they play? One possibility is that they may function in sucrose efflux to seeds (13). Another is that during long-distance transport, SWEETs may facilitate the “leakage” of sucrose from the phloem to nourish adjacent stem tissues (14). If so, manipulating SWEET expression could enhance carbohydrate delivery to developing seeds to increase yield, or it could increase the sucrose concentration in the storage cells of sugarcane or sweet sorghum stems to improve biofuel production.

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