Discerning the Difference Between Lumens and Scalariform Perforation Plates in Impeding Water Flow in Single Xylem Vessels and Vessel Networks in Cotton

Abstract

The geometrical structure and spatial arrangement of lumens, bordered pits, and scalariform perforation plates in xylem vessels modulate water flow from roots to leaves. Understanding their respective hydraulic functions is essential to unveil how plants regulate their hydraulic networks to facilitate the ascent of sap under biotic and abiotic stresses but is challenging because of the opaque nature of the vessel networks and water flow within them. We made the first-ever effort to discern the difference between lumens and scalariform perforation plates in cotton in impeding water flow in single vessels and vessel networks using X-ray tomography and porescale numerical simulation. Three-dimensional structures of xylem vessels in the stem of two cotton cultivars were acquired non-invasively using X-ray computed tomography (CT) at high spatial resolution, and a lattice Boltzmann model was developed to simulate water flow through the xylem networks at micrometer scale. The detailed water velocity and pressure simulated using the model were used to calculate the hydraulic resistance caused by the lumens and the scalariform perforation plates in individual vessels and the vessel networks of the two cotton cultivars. The results showed that the hydraulic resistance spiked whenever water flowed across a perforation plate and that the overall hydraulic resistance caused by the perforation plates in an individual vessel accounted for approximately 54% of the total resistance of the vessel. We also calculated the hydraulic conductance of individual vessels and vessel networks using the simulated water velocity and pressure at micrometer scale and compared it with those estimated from the Hagen Poiseuille (HP) equation as commonly used in the literature by approximating the xylem vessels in the cotton as isolated tubes. While it was found that the HP equation overestimated the hydraulic conductance by more than 200%, the overestimate was largely due to the incapability of the HP equation to represent the perforation plates rather than its approximation of the irregular vessels by circular tubes.

Optimizing Crop Water Use for Drought and Climate Change Adaptation Requires a Multi-Scale Approach

“…The utility of reduced root axial conductance capacity for late season soil water conservation in wheat has been further supported in recent work (Hendel et al, 2021). There may also be the possibility for longitudinal adjustments of xylem conduits (Meunier et al, 2017), regulation at the root to shoot junction (Meunier et al, 2018), as well as among the various attributes of protoxylem and metaxylem vessels, their pits (Xu et al, 2020) or perforation plates (Gao et al, 2020b). These may be part of a suite of embolism response traits and do not preclude the possibility that embolism is itself a means of restricting transpiration (McCully, 1999), in which aquaporins play a key recovery role (Secchi et al, 2017).…”

Root Phenotyping and Root Water Uptake Calculation Using Soil Water Contents Measured in a Winter Wheat Field

“…The importance of root traits in water uptake has been intensively studied over the past decades (Javaux et al, 2013;Lynch, 2013;Lynch, 2019;Postma et al, 2014), but Fig. 5 shows that other factors are equally important in mediating root water uptake and should be considered in screening drought-tolerant varieties (Gao et al, 2020;Sun et al, 2021;Wang et al, 2020).…”

“…The origin of the isotopes flowing through the stem (hence its associated water) can be tracked down to soil based on mass balance (Brooks et al, 2010;Liu et al, 2021;Ma and Song, 2016;Schwendenmann et al, 2015). While isotope method has been widely used, it neglects that the movement of isotopes from the location they are taken from soil to the location in the stem where they are sampled is not a convective process as presumed by the mass-balance method; they mixes with isotopes taken by roots from other places in the soil due to interconnectedness of the xylems and variation of water velocities in and between the xylems (Ehleringer and Dawson, 1992;Gao et al, 2020). Apart from these hydrodynamic mixings, there are other error sources that affect the isotope method (von Freyberg et al, 2020).…”

Xylem perforation plate phenotypes affect water use and drought adaptation in maize (Zea maysL.)

“…2001; Sperry et al ., 2006; Christman & Sperry, 2010), in other work, the Hagen-Poiseuille lumen resistivity is much less than the measured value, suggesting a significant effect of perforation plates on axial conductance (Sperry et al ., 2005). For example, Gao et al ., (2020) found that estimates of hydraulic conductance in xylem vessels of cotton calculated from the Hagen-Poiseuille equation were overestimated by more than 200%, largely due to the inability of the equation to represent perforation plates. Ultimately, the hydraulic resistance of these perforation plates is a function of their structure and the distance between successive plates along the length of the conduit, or the length of the vessel elements (Fig.…”