Ontogenetic scaling of phloem sieve tube anatomy and hydraulic resistance with tree height in Quercus rubra.

PREMISE: The dimensions of phloem sieve elements have been shown to vary as a function of tree height, decreasing hydraulic resistance as the transport pathway lengthens. However, little is known about ontogenetic patterns of sieve element scaling. Here we examine within a single species (Quercus rubra) how decreases in hydraulic resistance with distance from the plant apex are mediated by overall plant size. METHODS: We sampled and imaged phloem tissue at multiple heights along the main stem and in the live crown of four size classes of trees using fluorescence and scanning electron microscopy. Sieve element length and radius, the number of sieve areas per compound plate, pore number, and pore radius were used to calculate total hydraulic resistance at each sampling location. RESULTS: Sieve element length varied with tree size, while sieve element radius, sieve pore radius, and the number of sieve areas per compound plate varied with sampling position. When data from all size classes were aggregated, all four variables followed a power-law trend with distance from the top of the tree. The net effect of these ontogenetic scalings was to make total hydraulic sieve tube resistance independent of tree height from 0.5 to over 20 m. CONCLUSIONS: Sieve element development responded to two pieces of information, tree size and distance from the apex, in a manner that conserved total sieve tube resistance across size classes. A further differentiated response between the phloem in the live crown and in the main stem is also suggested.

Maintenance of carbohydrate transport in tall trees.

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.