A comprehensive picture of phloem loading strategies

Abstract

Mechanisms of phloem loading in the minor veins of leaves are known for only a few species. We propose that there are a limited number of loading strategies for the primary photoassimilates, sucrose and sugar alcohols. These strategies can be predicted based on thermodynamic and anatomical considerations and identified by autoradiography of veins following uptake of 14 C-labeled compounds, analysis of leaf solute composition and concentrations, and plasmodesmatal counting. Experiments on 45 dicotyledonous species identified the predicted loading patterns. Over 50-fold differences in concentrations of sucrose and sugar alcohols in leaves were measured. The cumulative concentrations of transport compounds in leaves correlated with loading mechanisms, a previously unrecognized association. Comparisons of solute concentrations and osmotic potentials of whole leaves suggest that sucrose and sugar alcohols are more concentrated in the cytosol than in the vacuoles of mesophyll cells, thus increasing the driving force for passive loading in species that employ this strategy. Passive loading is more widespread than previously thought, especially in trees. The results indicate that plants have exploited all thermodynamically feasible and structurally compatible loading strategies and that these strategies can be identified with straightforward protocols.plasmodesmata ͉ polymer trap ͉ raffinose ͉ stachyose ͉ sucrose P hloem loading is the starting point for export of carbohydrates and other nutrients from leaves (1-4). To date, mechanisms of sucrose loading have been established for a relatively small number of species. Less is known about sugar alcohols, which in some plants are present in phloem sap at higher concentrations than sucrose (5-7).In many species, loading involves an apoplastic step, driven by plasma-membrane transporters and energized by the proton motive force (8). In other plants, loading is symplastic, driven by a downhill concentration gradient from the mesophyll to the phloem and requiring high plasmodesmatal densities (2, 3). In some plants that load symplastically, the process is driven by diffusion alone and is passive (9, 10). In other species that load via the symplast, sucrose from the mesophyll diffuses into specialized companion cells (CCs) in the minor veins (11), known as intermediary cells, and is converted to raffinose and stachyose. These raffinose family oligosaccharides (RFOs) are larger than sucrose and are apparently unable to diffuse back to the mesophyll through the intermediary cell plasmodesmata. The RFOs accumulate in the phloem, a process known as polymer trapping (12), to a combined concentration that is similar to that of sucrose in apoplastic loaders (13,14). Thus, there are 3 recognized strategies of sucrose loading: Apoplastic and symplastic with or without polymer trapping.It is reasonable to assume that the anatomical features associated with sucrose loading in a given sieve element-companion cell (SE-CC) complex constrain available strategies of sugar alcohol loading. If s...

Optimal concentrations in transport systems

“…While sugar concentrations observed in plants generally span a wide range, this analysis provides a rationale for the observation that plants that use active sugar loading (data shown in figure 1c) typically have a higher sugar concentration than plants that use passive loading [15]. Active loaders expend metabolic energy to increase the sugar concentration in the phloem [21]. The process is driven by membrane transporters and sugar polymerization and occurs against a sugar concentration gradient.…”

Maize SUT1 functions in phloem loading

“…1,2 In apoplastic phloem loading species, sucrose transporters (SUTs) import sucrose from the apoplast into the companion cells and/or sieve elements. [3][4][5] In dicot plants, genetic and biochemical evidence has shown that SUTs function to phloem load sucrose in leaves.…”

Phloem Loading Strategies and Water Relations in Trees and Herbaceous Plants

“…Three phloem loading strategies have been identified for Suc, two of which are thermodynamically active and the third passive (Reidel et al, 2009;Rennie and Turgeon, 2009;Turgeon, 2010a). In the more common active mechanism, apoplastic loading, Suc enters the apoplast and is pumped into sieve element-companion cell complexes by membrane-bound transporters, using energy derived from the proton motive force (Sauer, 2007).…”