Hydraulic path length as a primary determinant of xylem anatomy in stems and leaves

Higher temperatures and more severe evaporative demands of the atmosphere are globally affecting plant communities inducing diffuse mortality events and stress conditions frequent (Allen et al., 2015; Anderegg et al., 2016; Breshears et al., 2018; N. McDowell et al., 2018; N. G. McDowell et al., 2022; Trugman et al., 2021). In particular taller plants seem to be more sensitive to critical water conditions (Bartholomew et al., 2020; Bennett, Mcdowell, et al., 2015; Fernández-de-Uña et al., 2023; Nepstad, Tohver, David, et al., 2007; Olson et al., 2021a; Olson, Soriano, Rosell, Anfodillo, Donoghue, Edwards, et al., 2018; Prendin et al., 2018; Rowland et al., 2015). The exact physiological cascade bringing to tree mortality is not fully understood but a pivotal role seems to be played by the hydraulic failure of the xylem network (Adams et al., 2017; Rowland et al., 2015). Xylem water transport efficiency is inextricably linked to hydraulic resistance to water flow in xylem conduits and we know that, hydraulic resistance in conduits is described by Poiseuille’s law (Tyree & Ewers, 1991; Vogel, 1994), describing a fluid flowing in a pipe, such as: R_h∝L/D^4 Where Rh is the hydraulic resistance, L is the length of the pipe (hydraulic path), and D is the diameter of the pipe. For many years plants hydraulic structure has been modelled ad a bunch of cylindrical pipes (Shinozaki et al., 1964), connecting stomata with root apexes. The problem with this model is that, with increasing in hydraulic path length (i.e. plant growing taller and leaves elongating) the hydraulic resistance increases dramatically, actually disfavouring growth. However, we clearly see plant growing taller and taller, competing with each other and suggesting that some evolutionary mechanism for compensating the increase in hydraulic resistance should occur. In the last 25 years an alternative model has been proposed. The Widened Pipe Model (Anfodillo et al., 2006b; Koçillari, Olson, Suweis, Rocha, Lovison, & Cardin, 2021; Olson et al., 2021a; West et al., 1999) suggests that in order to compensate for the potential increase of hydraulic resistance due to the elongation of the path length (i.e. growth), xylem conduits diameter widens from the top to the bottom of the plant (stomata to roots) following a power law (Anfodillo et al., 2006a; Koçillari et al., 2021; Olson et al., 2021; Olson & Rosell, 2013; Rosell et al., 2017), such as: D=a∙L^b Where D is the diameter of conduits at a certain distance L from the apex, a is the apical conduits diameter and b is the widening rate. Because of this basipetal widening, the narrowest conduits are found in leaves and therefore, in the laves is located up to 98% of the hydraulic resistance of the total path length from stomata to roots (Lechthaler et al., 2020a). This suggests a pivotal role of leaves in determining the hydraulic resistance of the entire xylematic structure of the plant and, consequently, its ability to cope with demanding hydraulic challenges (i.e. drought or great heights). Is, therefore, crucial to deeply understand the role of hydraulic path length and the influence of leaf position and morphology in whole plant hydraulics.