How to transport water over longer distances without increasing hydraulic resistance? Plants have the answer!

Since the first colonization of land, in the last 400 million of years (Raven, 2002) terrestrial vascular plants have always faced the need to transport water from ground level to the height of the leaves, where 99% of water evaporates. They developed a specialized tissue, the xylem, made of pipe-like hollow dead cells juxtaposed to each other. The diameter of these cells is found to be wider at the base of the plant and in the outermost part of the stem. Papers (Lenz et al., 2010; Rodriguez-Zaccaro et al., 2019; Shulte, 2012) and a widespread belief assume that this phenomenon is due to the age of the cambium (tissue responsible of producing xylem cells). The older the plat, the wider the conduits. We want to remark that is due to hydraulic purposes, instead (Olson et al., 2021). The first hydraulic model, known as Pipe Model (Shinozaki et al., 1964) tried to grasp the architecture of the xylem considering a plant as a system of cylindrical pipes, connecting soil to leaves. The water flux is characterized by a certain hydraulic resistance, due to the Hagen-Poiseuille law (Tyree, 1991; Zimmerman, 1983), that is proportional to pipe length and inversely proportional to the 4th power of pipe diameter. While the plant grows in height, the xylematic conduits became longer, suggesting that the hydraulic resistance should increase. This means that a taller plant could provide less water to its leaves, with obvious physiological disadvantages, compared to a smaller one. In forests, however, trees compete for the light growing taller and reaching remarkable heights (100 m in Sequoia sempervirens). It’s reasonable to think that natural selection should have favored plants with a xylem architecture which can ensure constant leaf specific conductance and, consequently, constant leaf photosynthetic productivity. In the last decades researchers highlighted that xylem architecture in plants shows a tip-to-base widening (West et al., 1999): proposing the Widened Pipe Model, in which conduits tend to widen from the apex to the base of the tree. The diameter of the xylematic conduits (d) varies with the distance from the apex of the tree (L) following a power law (Anfodillo et al., 2006) such as: 𝑑∝𝐿^b, and the exponent b has been found to be almost the same in many species (Olson et al., 2014), ranging 0.20-0.25. This ensures that the hydraulic resistance is concentrated in the uppermost few meters and is kept almost constant while the plant grows taller (Anfodillo et al., 2013). To test that Widened Pipe Model’s hydraulic implications, and not age, are responsible of xylem conduit diameter we sampled 7 trees (4 different species) in which the crown lowered deeply along the stem and measure the median of conduit area before and after the lowering of the crown. The high number of lower leaves should imply a high number of small conduits at stem base, even if the plant is older (3-4 years). In all the samples analyzed the median of lumen area was found lower (range: 7-44%) after the lowering of the crow. Our results strongly confirm that xylem conduit size is determined by hydraulic constraints and not by cambial age.