The Dual Function of Sugar Carriers: Transport and Sugar Sensing

Abstract

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. 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 (Köckenberger 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 (Sjölund, 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 of sucrose transport from source to sink is not for plant, and may the of sucrose in the the to the several cell types: mesophyll cells, cells, phloem and of sucrose is to via from the of to the in many species, is not well connected to the cells for the of sucrose into the been from mesophyll cells, the and transport the and direct via plasmodesmata. The to which plants of and plants is a that phloem loading the transmembrane transport of sucrose and other into the For such as in we a of sucrose transport the translocation In the transport be of sucrose into the cell directly from the mesophyll cell transporter this transporter be a or sucrose been et al., 1993). at one transporter is required for uptake into the phloem transporter These loading are required at of such as during for sugar from leaves or for of that of sucrose the translocation is to with the phloem, for in stems transporter and In sink by transmembrane of sucrose transporter or plasmodesmata. Sucrose transporters inv