Why is there more than one mechanism of phloem loading?

Background/Question/Methods

Plants transport food over long distances in the phloem by an osmotically driven pressure-flow mechanism. The starting point is the leaves where sucrose is loaded into the phloem of small veins that permeate the photosynthetic tissue. Interestingly, there are three known mechanisms of phloem loading. In one, sucrose enters the cell wall space (apoplast) and is subsequently taken up into the phloem by sucrose-proton co-transporters on the plasma membranes. The other two mechanisms are symplastic, the sucrose passing from photosynthetic cells into the phloem through plasmodesmata, the minute pores that connect plant cells. One of the symplastic mechanisms is thermodynamically active, driven by the synthesis and trapping of larger sugars, raffinose and stachyose, in the phloem. The second symplastic mechanism is not as well studied but appears to be passive in the sense that sucrose is carried into the phloem by diffusion or by bulk flow down its concentration gradient. Evidence for passive loading is, to date, primarily correlative, based on plasmodesmatal counts and analysis of sugar gradients within leaves. Most herbs use the apoplastic, transporter driven process, while most trees rely on the putative passive loading mechanism.

Results/Conclusions

To test the passive loading model we transformed poplar (Populus tremula X P. alba) plants with constructs that drive invertase expression in the apoplast. In plants that load from the apoplast, this technique inhibits loading since sucrose is hydrolyzed en route to the phloem. Apoplastic invertase had essentially no effect on growth or photosynthesis, indicating that sucrose follows the symplastic, rather than apoplastic, route into the phloem. We suggest that each of the three loading mechanisms confers specific advantages. Active loading, either by transporters or by polymer trapping, allows plants to maintain low overall foliar sucrose levels and still have high sucrose content in the phloem to drive long-distance transport. Maintaining low foliar sucrose concentration reduces inventory costs and accelerates plant growth. Passive loading may be more common in trees because they must store solute in their leaves to offset low whole-plant hydraulic conductance in the xylem, thus negating the major advantage conferred by active loading. It is also possible that a symplastic loading route into the phloem provides plants with the opportunity to deliver other beneficial molecules to the phloem and to sink tissues without the need for specific transporters.