The Role of Phloem Loading Reconsidered

Abstract

It is generally assumed that the primary role of phloem loading is to drive long-distance transport by elevating hydrostatic pressure in sieve elements. This concept is consistent with the fact that, in many plants, energy is used to increase the concentrations of photoassimilates in the leaf phloem to levels well above those in mesophyll cells. However, on the basis of recent data, these fundamental assumptions need reevaluation. The data indicate that a large number of woody species—plants with the longest transport distances—load solute passively by maintaining high concentrations of Suc, and in some cases sugar alcohol, in mesophyll cells. Here I suggest that the adaptive advantage of active phloem loading, in the evolutionary sense, is to permit plants to maintain low foliar concentrations of nonstructural carbohydrates (NSCs), i.e. sugars, sugar alcohols, and starch. Economic considerations of inventory costs indicate that maintaining low NSC levels in leaves improves return on investment in carbohydrate synthesis, leading to a substantial increase in growth potential. Münch (1930) did not invoke active phloem loading in his model of long-distance transport. He assumed that the solute produced by photosynthesis generates sufficient hydrostatic pressure in mesophyll cells to drive transport from leaves to sink organs through the symplast. However, subsequent research indicated that the sugar concentration in the phloem is much higher than in mesophyll cells (for an early review, see Crafts, 1961). As the Münch hypothesis gained acceptance, so too did the notion that the role of loading is to energetically concentrate sugars in the phloem, increasing turgor and thereby providing the motivating force for pressure flow. This interpretation of the role of phloem loading has persisted. However, when one considers the primary finding—that there is a disparity in photoassimilate concentrations between the phloem and photosynthetic cells—it is equally reasonable to postulate that the adaptive advantage is derived from keeping the concentrations of these compounds low in the mesophyll. Viewed this way, active phloem loading allows plants to maintain low photoassimilate concentrations in leaves and at the same time elevate pressure in the phloem sufficiently to enable long-distance transport. To understand the difference between these two views, it is important to make the distinction between active and passive loading. In active loading, metabolic energy is used to pump photoassimilate into the phloem, against a concentration gradient. Two species-specific, active mechanisms are known (Fig. 1). In apoplastic loading, the proton motive force is used to carry Suc, and in some cases sugar alcohols, into the phloem via transporters (Lalonde et al., 2004; Sauer, 2007; Braun and Slewinski, 2009). The second mechanism, polymer trapping (Schulz, 2005; Turgeon and Wolf, 2009), is also active although the initial step is not. In the initial step, Suc diffuses from the mesophyll into the minor vein companion cells through plasmodesmata. The Suc in the companion cells is then used to synthesize raffinose and stachyose, a process that increases the concentrations of these sugars in the sieve element-companion cell complex. Although polymer trapping does not involve active transport in the formal sense of moving ions or molecules across a membrane, it is thermodynamically active overall; energy is used to create a concentration difference between the mesophyll and the phloem. There is now convincing evidence, by four independent protocols—histochemistry (Pristupa, 1983), microdissection of minor vein phloem (Haritatos et al., 1996), plasmolysis (Turgeon and Hepler, 1989), and analysis of aphid stylet sap (Voitsekhovskaja et al., 2006)—that the solute concentration in the phloem of polymer trap species is close to, or as high as, that found in plants that load via the apoplast. The polymer trap hypothesis is supported by recent evidence that loading is insensitive to down-regulation of the Suc transporter (Zhang and Turgeon, 2009), but highly sensitive to down-regulation of raffinose and stachyose synthesis (McCaskill and Turgeon, 2007). Schematic diagrams of putative phloem-loading strategies at the minor vein (A–C) and whole leaf (D–F) levels. In A and D, Suc diffuses through plasmodesmata (gaps in walls) into the minor vein companion cells (CC) and sieve elements (SE), a passive process. The Suc concentration in mesophyll cells (M), and therefore the entire leaf, is high; the Suc concentration in the veins is slightly lower. In B and E, Suc diffuses through plasmodesmata into the minor vein CCs (intermediary cells) and is converted to raffinose and stachyose, thus actively elevating the transport sugar concentration in the phloem by polymer trapping; this allows the mesophyll cells to maintain low Suc levels. In C and F, Suc is pumped from the apoplast into the minor vein phloem by transporters (yellow circle), which also