Phloem Loading Strategies and Water Relations in Trees and Herbaceous Plants    

Abstract

Most herbaceous plants employ thermodynamically active mechanisms of phloem loading, whereas in many trees, the mechanism is passive, by diffusion. Considering the different water transport characteristics of herbs and trees, we hypothesized that water relations play a role in the adoption of phloem loading strategies. We measured whole-plant hydraulic conductance (K p ), osmolality, concentrations of polar metabolites, and key inorganic ions in recently mature leaves of 45 dicotyledonous species at midafternoon. Trees, and the few herbs that load passively, have low K p , high osmolality, and high concentrations of transport sugars and total polar metabolites. In contrast, herbs that actively load sucrose alone have high K p , low osmolality, and low concentrations of sugars and total polar metabolites. Solute levels are higher in sugar alcohol-transporting species, both herbs and trees, allowing them to operate at lower leaf water potentials. Polar metabolites are largely responsible for leaf osmolality above a baseline level (approximately 300 mM) contributed by ions. The results suggest that trees must offset low K p with high concentrations of foliar transport sugars, providing the motivating force for sugar diffusion and rendering active phloem loading unnecessary. In contrast, the high K p of most herbaceous plants allows them to lower sugar concentrations in leaves. This reduces inventory costs and significantly increases growth potential but necessitates active phloem loading. Viewed from this perspective, the elevation of hydraulic conductance marks a major milestone in the evolution of the herbaceous habit, not only by facilitating water transport but also by maximizing carbon use efficiency and growth.

Nonstructural Carbon in Woody Plants

“…Although highly speculative at this point, it could be that high NSC inventories in trees serve multiple osmotic purposes. For instance, they may allow trees to overcome hydraulic constraints due to height (110,148) while supplying soluble sugars for phloem loading and long-distance transport (37).…”

Drought Effects on Photosynthesis and Implications of Photoassimilate Distribution in 11C-Labeled Leaves in the African Tropical Tree Species Maesopsis eminii Engl.

“…As in the tropics most trees are drought-deciduous or evergreen, more research on how tropical tree species load carbohydrates into the phloem is warranted. Large studies investigating phloem loading strategies show that available data on tropical species is limited [79,80,83]. Younger leaves in our study showed a relatively uniform tracer distribution throughout the mesophyll (Figure 4).…”

“…A distinct difference in tracer amount was found in the mesophyll with an accumulation pattern directed towards the major veins. According to studies by Rennie and Turgeon [82] and Fu et al [83] this indicates an active loading strategy. Alternatively, this distribution pattern could be due to rapid export of tracer out of the mesophyll, with most of the tracer already within the major veins after pulse-labeling, which still indicates active loading.…”

“…Commonly, trees use a passive loading strategy, characterized by a higher concentration of sugars in the mesophyll and a lower concentration in the veins (e.g., [32,40,82,83]). Previous 14 C labeling experiments have evaluated loading strategies of species and reported that active loaders showed higher tracer accumulation in the veins and passive loaders in the mesophyll [32,82,83]. In older leaves of M. eminii, tracer intensity was elevated near the main and secondary veins, whereas in active loaders a higher presence of tracer is expected inside the veins.…”

“…The active phloem loading strategy has been linked to (i) an increased carbon export from leaves to sinks (e.g., shoots and roots) [32,40,85]; (ii) an improved efficiency of sugar transport [58]; and (iii) an increased growth potential [40]. Active transport is less common in woody tree species, but not unique [83]. Turgeon [40] investigated why active loading is commonly found in herbaceous species, and passive loading in tree species.…”