Abstract
BackgroundIn contrast to man the majority of higher plants use sucrose as mobile carbohydrate. Accordingly proton-driven sucrose transporters are crucial for cell-to-cell and long-distance distribution within the plant body. Generally very negative plant membrane potentials and the ability to accumulate sucrose quantities of more than 1 M document that plants must have evolved transporters with unique structural and functional features.Methodology/Principal FindingsTo unravel the functional properties of one specific high capacity plasma membrane sucrose transporter in detail, we expressed the sucrose/H+ co-transporter from maize ZmSUT1 in Xenopus oocytes. Application of sucrose in an acidic pH environment elicited inward proton currents. Interestingly the sucrose-dependent H+ transport was associated with a decrease in membrane capacitance (Cm). In addition to sucrose Cm was modulated by the membrane potential and external protons. In order to explore the molecular mechanism underlying these Cm changes, presteady-state currents (Ipre) of ZmSUT1 transport were analyzed. Decay of Ipre could be best fitted by double exponentials. When plotted against the voltage the charge Q, associated to Ipre, was dependent on sucrose and protons. The mathematical derivative of the charge Q versus voltage was well in line with the observed Cm changes. Based on these parameters a turnover rate of 500 molecules sucrose/s was calculated. In contrast to gating currents of voltage dependent-potassium channels the analysis of ZmSUT1-derived presteady-state currents in the absence of sucrose (I = Q/τ) was sufficient to predict ZmSUT1 transport-associated currents.ConclusionsTaken together our results indicate that in the absence of sucrose, ‘trapped’ protons move back and forth between an outer and an inner site within the transmembrane domains of ZmSUT1. This movement of protons in the electric field of the membrane gives rise to the presteady-state currents and in turn to Cm changes. Upon application of external sucrose, protons can pass the membrane turning presteady-state into transport currents.
Highlights
For long distance transport from the side of production in leaves to the user tissues, sucrose is loaded into the tubelike phloem network [1]
Taken together our results indicate that in the absence of sucrose, ‘trapped’ protons move back and forth between an outer and an inner site within the transmembrane domains of ZmSUT1
This movement of protons in the electric field of the membrane gives rise to the presteady-state currents and in turn to capacitance of biological membranes (Cm) changes
Summary
For long distance transport from the side of production (source) in leaves to the user (sink) tissues, sucrose is loaded into the tubelike phloem network [1]. Phloem loading of sucrose, synthesized in photosynthetic cells (mesophyll) within the leaves, takes place in the sieve tube adjacent to companion cells. In contrast to animal cells, plants cells establish a pH gradient (acidic extracellular space) and very negative membrane potentials via plasma membrane proton pumps. From this electromotive force sucrose transporters gain energy to drive sucrose accumulation of more than 1 M. The ZmSUT1 behavior is in contrast to the animal counterpart SGLT1, which mediates sugar uptake only. These fundamental physiological differences between plant phloem- and animal blood stream sugar transporters are harbored in their unique structure-function relationships. Very negative plant membrane potentials and the ability to accumulate sucrose quantities of more than 1 M document that plants must have evolved transporters with unique structural and functional features
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