Maintenance of carbohydrate transport in tall trees

Abstract

Trees present a critical challenge to long-distance transport because as a tree grows in height and the transport pathway increases in length, the hydraulic resistance of the vascular tissue should increase. This has led many to question whether trees can rely on a passive transport mechanism to move carbohydrates from their leaves to their roots. Although species that actively load sugars into their phloem, such as vines and herbs, can increase the driving force for transport as they elongate, it is possible that many trees cannot generate high turgor pressures because they do not use transporters to load sugar into the phloem. Here, we examine how trees can maintain efficient carbohydrate transport as they grow taller by analysing sieve tube anatomy, including sieve plate geometry, using recently developed preparation and imaging techniques, and by measuring the turgor pressures in the leaves of a tall tree in situ. Across nine deciduous species, we find that hydraulic resistance in the phloem scales inversely with plant height because of a shift in sieve element structure along the length of individual trees. This scaling relationship seems robust across multiple species despite large differences in plate anatomy. The importance of this scaling becomes clear when phloem transport is modelled using turgor pressures measured in the leaves of a mature red oak tree. These pressures are of sufficient magnitude to drive phloem transport only in concert with structural changes in the phloem that reduce transport resistance. As a result, the key to the long-standing mystery of how trees maintain phloem transport as they increase in size lies in the structure of the phloem and its ability to change hydraulic properties with plant height.

Computational models evaluating the impact of sieve plates and radial water exchange on phloem pressure gradients

“…Münch thought that this was necessary to prevent pressure loss along the pathway (Münch, , p. 56). This assumption is consistent with the frequent use of the Hagen–Poiseuille equation in models of phloem transport (e.g., Epron, Dannoura, Ishida, & Kosugi, ; Savage et al, ; Thompson & Holbrook, ). Use of Poiseuille‐driven flow has been justified as long as extra equations are included to account for radial water exchange (Thompson & Holbrook, ).…”

“…We found that the most important sieve plate traits that impact plate resistance were total pore area and shape. Previous methodologies take into account the variability of pore radii in their models (Liesche et al, ; Savage et al, ) but assume pores are always circular. However, our results indicate that assuming pore shape as being circular instead of using their actual shape may underestimate pore flow by as much as twofold in comparison with past work (e.g., Jensen, Mullendore, et al, ; Thompson & Holbrook, ).…”

“…In future research, it would be useful to consider more fully the number of pores and total pore area occurring on plates of varying angles. Across a number of tree species, the number of sieve areas within a plate increase with steeper plate angle (Savage et al, ). Thus, sieve tubes may additionally reduce resistance over length by generating steeper angle sieve plates that may possess greater total pore area.…”

“…A challenge to phloem transport arises from the fact that resistance scales linearly with phloem path length (De Schepper, De Swaef, Bauweraerts, & Steppe, ; Savage et al, ; Turgeon, ). This has cast doubt on the feasibility of maintaining sugar transport over long distances in trees.…”

“…lumen (Jensen, Mullendore, et al, 2012;Liesche, Pace, Xu, Li, & Chen, 2017;Savage et al, 2017). However, other examples show conductivity reductions due to plates of up to 88% (Thompson & Holbrook, 2003a).…”