The Dual Function of Sugar Carriers: Transport and Sugar Sensing

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., The 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., 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 involved in phloem been to as or as et al., Sucrose in the of sink be directly transporter or the of sucrose into and by by uptake transporter the that transport on the of plant in phloem, the and cells are present in species which are as and To the required for the be The of via the phloem et al., that be by plant been identified in the by of by and by the its of in the sucrose may be into the or via the apoplasm. The loading sucrose from the mesophyll or the vascular and into the phloem sap sink the by also occurs the of the phloem or a sucrose at the sink of sucrose and other into sink may or sucrose transporters In to and cells in the sink may to its by as The transport system consist of a for uptake and a for by the its of in the sucrose may be into the or via the apoplasm. The loading sucrose from the mesophyll or the vascular and into the phloem sap sink the by also occurs the of the phloem or a sucrose at the sink of sucrose and other into sink may or sucrose transporters In to and cells in the sink may to its by as The transport system consist of a for uptake and a for the of the entire of the transport occurs only in such as the the is that plants may different of phloem in different tissues or may be to and on uptake and are required for the which serves as a for sugars and other 1999, in this issue). of sucrose into the SEs is to the the of the phloem conduits so as to the of the phloem The of translocation in the phloem is from to (Köckenberger et al., The phloem, osmotic on the functions of types of that sucrose to in the that provide the energy for and that derived from the xylem a of et al., 1999, in this for a of et al., 1999, in this issue). other such as and also to the driving force of the sap and the of and at sink tissues essential for the osmotic is that the be from phloem cells are connected to mesophyll cells, such be in the different cell types in leaves are in and in the of plants as or for the regulated of has been and Oparka et al., the numerous required for long-distance transport only sucrose and uptake transporters been identified at the molecular is sucrose is also or the are related in to the uptake transporters et al., The sucrose which in many cases with the sucrose be responsible for of sucrose et al., et al., 1997) and may represent a sucrose transporter transport also been identified in a variety of plant species and et al., and and that are and and are for transport and transporters from by their the of to the of from cells the of the plant transporter gene and In to the transporters which as the transporter is a et al., et al., this in the transport and transporter genes are proteins of transporters are to in The that genes transporters from expression of the plant genes in et al., The of plant transporters by et al., The transporter family in as in in of and multiple genes been from other characterized by expression in and to as a et al., et al., The expression of plant transporters that proteins in uptake in sink tissues and of expression also that plant transporters are highly such as in response to or et al., of fixed carbon. The expression of transporters in sink also for phloem or and In this plant sink tissues may in a to that by that to for this in plants is the of plant and transporters and in are from in are from The sugar family in genes et al., 1997; reviewed in and 1997), with members to the and The with to their with for uptake from for to for et al., The expression of genes is regulated by and the transporter and as Sucrose transport been in a variety of and reviewed in Ward et al., To plant sucrose a that to sucrose but of sucrose to the of a sucrose The in a of the transport The cells on sucrose as the carbon source and to plant sucrose transporters from and potato by et al., transport studies of and of plant sucrose transporters identified so far are energy and to that as The for in to be in the of et al., et al., 1996). for the sucrose transporters and The genes highly consist of and are related to the transporter family in many such as and plants in Ward et al., 1997; et al., for the sucrose transporters been characterized by the in et al., et al., The of to be with in from sugar leaves et al., The family to the of in plants and for of Sucrose sucrose of and transporters in the et al., in which the and plant sucrose in the on sucrose as the carbon source only a sucrose transporter is in the The or of the to on sucrose or is sucrose sucrose transporter for of Sucrose sucrose of and transporters in the et al., in which the and plant sucrose in the on sucrose as the carbon source only a sucrose transporter is in the The or of the to on sucrose or is sucrose sucrose transporter on the transport of that the transporter be involved in phloem loading and be present at the of In that SUT1 are phloem associated et al., and the of SUT1 and genes direct the expression of genes in and phloem and and SUT1 from play a role not only in phloem loading but also in of sucrose from sieve tubes the translocation transporter To expression at the studies been to In major and with specific in et al., and 1996). By and SUT1 to the of SEs of and et al., The in sucrose transporter localization in and major with and may be to in loading the transporters in and major not to be of which may to be identified in be with a of sucrose different in as to SEs such a is by analyses In experiments at the the localization of proteins to SEs in a SUT1 to SEs, at the of et al., In of SUT1 expression a the in transgenic plants to of sucrose from leaves et al., 1996). These indicate that of the SUT1 gene occurs in and, in with of and provide for of plant and SUT1 the that and SEs. These may at however, of is to in and during and in In and from the gene are in (Lucas et al., studies in that identified in phloem sap of that species is of a of including the SUT1 et al., The transport of such as and proteins the of of et al., 1998; also and 1999, in this issue). The of in this and many to be highly to into organelles such as and 1999, in this and the and 1999, in this issue). in two for the of SUT1 be is as of a the the phloem for or is in the and the is within the at the plasmodesmatal via the system and 1996). phloem proteins the for and been to from cell to cell et al., 1997; et al., 1998; and in this issue). proteins been identified in the phloem of which to be specific for SEs, and et al., et al., 1997; et al., The role of most of proteins in the phloem is and their and are not The of proteins in the phloem also is The of in phloem sap may indicate that is is to in the phloem sap and SEs are living cells the that a nucleus and many other organelles (Sjölund, SEs are thought to be on for many functions, but the of this be the actual of SEs are For is not SEs In CCs, on the other the expression of the gene has been demonstrated and et al., 1999, in this issue). SEs in the supply of to SEs be with phloem sap has been to of in the of et al., the of in SEs may be on a supply of or from CCs, by analogy to SUT1 et al., the other SEs not a or the force to phloem loading is only in CCs, plasmodesmatal are for the of this driving force and a for into SEs 1996). In of and other and SEs is for long-distance and to development at the in response to and in and 1996). SUT1 In species, SUT1 is in the occurs in are two SUT1 may be by transport SUT1 may in and to SEs may via the or that are plasmodesmata. These are not and in sieve SUT1 In species, SUT1 is in the occurs in are two SUT1 may be by transport SUT1 may in and to SEs may via the or that are plasmodesmata. These are not and in sieve sucrose transport by SUT1 is essential for phloem a in transport carbon and In SUT1 plants et al., et al., sucrose and is to in the and the in is In SUT1 plants at leaves that and of of the depends on the of the and et al., 1996). of occurs of potato leaves are so as to phloem translocation et al., into is also in a of studies in which is et al., and direct of and at the that the of in tissues to the that of loading a sugar the to sugar and levels et al., of from leaves of plants show in phloem transport et al., With less transport to the plants and also in transgenic potato plants in which loading is by the of a in cell of leaves et al., et al., In of SUT1 also to and of in leaves et al., The of recently fixed is to levels in plants to and to be Thus, to be for phloem loading at in in potato plants in which SUT1 in of the et al., 1996). however, not to the of SUT1 the actual of SUT1 and sucrose transport in the phloem by levels of SUT1 expression in mesophyll cells et al., 1996). The are in with that SUT1 in is essential for phloem also other members of the gene family. analysis of the role of members of the gene family will such as the of in The of this for transport has been demonstrated in the of et al., et al., 1998; et al., 1998; also et al., 1999, in this issue). of in sugar transport is in in several sucrose and to be into sink tissues in and expression has been in tissues et al., and the direct of such in sink tissues In several plant species, such as and sucrose transporter genes been as in et al., and et al., 1997; et al., 1997; et al., 1998; and 1998; et al., of show highly specific expression For in is in et al., and sucrose transporter be in the cells of from seeds and et al., 1997; et al., 1997; et al., are also in source a in phloem loading in leaves and in members of the family are required in such as and sucrose transporter has been identified in and sink sucrose transporters in direct transport into sink cells or in sucrose sink that involved in regulation of phloem or has been in by in source for from in sink tissues for from phloem and and involved in storage in to be identified Sucrose in companion sieve sink source vascular bundle. of or localization has been demonstrated several In Sucrose in companion sieve sink source vascular bundle. of or localization has been demonstrated several In is that transport sugar transport in are and that in the source and in the sink are the of is in plants et al., a for however, are in and be to uptake and is that sugar transport the distribution of within the plant In the cells only for a sugar cells, in source or sink such as or gene to the cells involved in be to and and and of sugars need to be that the cell has a of of and for sensors, as in sugar uptake to for by uptake at In multiple be for and for to the has a limited for this signal may at the to in the of of transporters also be via the such also be in or transport in plants is more is at two from one cell and into the to be is the molecular involved in sugar in to transport in plants. serve as a to the in plants. The a of many of which are involved in transmembrane For for transport et al., 1997) and for sugar transport and The of transport that are to the uptake of in response to a changing in has a system to the supply of sugars from the and the of the the of sugars is and sugar transport is regulated sugar transport the of sugars into the for for by a of and In to are to sugar concentrations. a transporter and or of proteins at the In this sugar activate a to sugar transporter genes more sugar on the other sugar the may repress transporter or via and of the the of transporters uptake at concentrations. for by a of and In to are to sugar concentrations. a transporter and or of proteins at the In this sugar activate a to sugar transporter genes more sugar on the other sugar the may repress transporter or via and of the the of transporters uptake at concentrations. in transporters functions in sugar in regulation of and transporters for sugar The and the These are to transporters but a that functions in The and regulation of and transporter for in transporters functions in sugar in regulation of and transporters for sugar The and the These are to transporters but a that functions in The and regulation of and transporter for In multiple transport for are regulated at the in response to the of For and serve as transporters and are only by levels of but at functions as a transporter and is only by of and and of that not only to the of carbon source in the but also to its are the is by different and is the into By to the uptake of the regulation of the and the regulation of be by et al., the expression of genes for the of carbon sucrose or and genes involved in be in the of of the carbon is a as The signal that of transporter genes is by the and the other the signal that is connected to the of et al., et al., In are two for proteins to act as the and the signal via other or transporters and so as to the or of the compound by such a the of the of the as the of to In has been that is during transport by the system et al., related proteins been at the of in to proteins that transporters but et al., has been recently for et al., 1998; et al., and be a not to In yeast, to be a of levels of and expression of to be a of that expression of is required at levels of for of the transporters and and et al., in and that to the of in the of been identified et al., the of and to transmembrane proteins not to be to transport and et al., The of two of of is also present in the of and in from which a and the expression of the transporter et al., In the a that is to that of and et al., to as two et al., 1998; et al., the that are required for the of the and the for the transporters and be into by to the is to that the act as transporters with a transport to of that which the signal by a during that to as has recently been identified in the of the a transmembrane related to a this at the of the a and a et al., 1998; et al., a the of genes and to to in the of et al., 1998; et al., The of the of to of and The only so far to be involved in signal transduction in are the et al., and a including the and and 1997; et al., is a that directly to of the genes et al., as a of genes in cells and as a of in cells on levels of of by is by the is of proteins The is required for regulation of and the signal by to the in response to levels of is also required for of into by in the of levels of of or its may for by the or directly its may be directly by and 1997) or may on proteins be to with et al., recently in to be required for in response to and such cells into a to a family of closely related et al., the other two members of this transporter serves as transporter and a of in or but form on of the however, is to transport its and as with the other members of the on its or In the of in yeast, to play and more direct in of and other genes The and functions of are from and to its et al., et al., in a that is by et al., In of is of and is on involved in of has not been and is that of from et al., has been that has a et al., a that is not to the signal et al., These as that its act as a the actual the of the signal is not The signal the a in the and highly in of depends on and its et al., In the of by the et al., 1997) but is also required for the of other In with a for the of in is on the is not on a specific transporter the signal with the of into cells et al., These well with the transport is to the via and transport of which act as a for as well as a signal In the two different a has recently been to in to carbon also to be involved in of gene expression et al., of genes is regulated by sucrose and in and 1996). The of interconnected with sugar regulation the plant with to to and also to and and et al., and et al., genes be as or for and are by sugar gene expression for and storage of in source or sink et al., et al., et al., and and 1996). as the transport form of the expression of a of of genes and the from and 1997; et al., supplied sucrose of to a of et al., In sugar sugar to a of sucrose transport with a in levels of and and transport to a Sucrose repress of photosynthetic genes for and been in which sucrose is from the of such genes et al., studies indicate the of signal and transduction in which and be also been and 1996). and sucrose to different cell sucrose to storage compound in seeds et al., specific system in which a as has been identified in the of genes et al., and or that are into cells but are not by not repress gene in photosynthetic or of that are and et al., and not gene but of the Thus, is involved in a that is by studies of transgenic plants in which the expression of the genes and been et al., In the of such as and is to to concentrations. plants a sugar the to the plants et al., These a direct role for in in to its the to be more plants a in the or levels of only in plants with or expression gene expression by the sugar et al., 1996). the of sugar into cells by not the expression of genes and to be the of sugars that is the of sugar more recently identified in to be responsible for and gene In cell the expression of and sucrose genes is with et al., et al., In transgenic a to which that the for this occurs in the et identified several with sugar response that a These in which the not to a for sugar of by specific expression a in which or are at the cell et al., et al., in the of the are more levels of to a on provide for the of at the which to the system present in the of sugars as of gene is the signal transduction in which studies that to are involved in signal transduction genes been in plants with to of which the In vivo has been demonstrated in transgenic potato plants gene in such that a in sucrose expression is in and gene and gene by sugars the of and et al., in the of the regulation of and gene the of is as with specific of and and et al., of in transporters the uptake of for the sugar and be but are not for signal are not by genes or sucrose genes are via a and serve as for and repress photosynthetic genes via the Sucrose be and in the of in transporters the uptake of for the sugar and be but are not for signal are not by genes or sucrose genes are via a and serve as for and repress photosynthetic genes via the Sucrose be and in the studies that sugar transport be to the changing of the of the transport in developing leaves has that is and during maturation et al., such as and been to the of phloem and sucrose as and and In the direct of by the of et al., loading in of to be directly by and et al., a principle of such studies is the to within the sugar transporters be regulated in two major by or more by the expression of sugar transporters at the and are to et al., 1997; et al., et al., and which at the of supply for the et al., et al., et al., and also et al., 1999, in this issue). Sucrose also of two and et al., 1996). is on sugar uptake and as and These that the of expression of genes by sugars may be of a response to cell in the of abundant carbon et al., 1996). SUT1 and are in source and sink tissues et al., and The expression of the sucrose transporter SUT1 is regulated at the and et al., 1997), in with regulation of from leaves et al., SUT1 and levels be by the of and to leaves and such for of the two major genes in potato leaves et al., Sucrose to be involved in sucrose transporter at the and experiments indicate that SUT1 is also regulated at the by et al., which be responsible for of sucrose transporters in the SEs, been in the phloem sap et al., in yeast, sugars may also the of transporters et al., studies show that the of SUT1 is in the of a few et al., may indicate specific the of in the and may of as in the of transporters and et al., 1996). has been demonstrated or is also its regulation of for and a transporter in has been and sucrose and gene expression is regulated by one may a network uptake of and sucrose with the and as in members of the plant transporter that be as that transporters be involved in et al., such in that are thought to play a role in the of the plant transporter family that the at of the proteins with the in the and two genes and that are closely related to other one of the and family is characterized by the of a to be and The of the from will provide for more analysis