Investigating Effects of Bordered Pit Membrane Morphology and Properties on Plant Xylem Hydraulic Functions—A Case Study from 3D Reconstruction and Microflow Modelling of Pit Membranes in Angiosperm Xylem

Abstract

Pit membranes in between neighboring conduits of xylem play a crucial role in plant water transport. In this review, the morphological characteristics, chemical composition and mechanical properties of bordered pit membranes were summarized and linked with their functional roles in xylem hydraulics. The trade-off between xylem hydraulic efficiency and safety was closely related with morphology and properties of pit membranes, and xylem embolism resistance was also determined by the pit membrane morphology and properties. Besides, to further investigate the effects of bordered pit membranes morphology and properties on plant xylem hydraulic functions, here we modelled three-dimensional structure of bordered pit membranes by applying a deposition technique. Based on reconstructed 3D pit membrane structures, a virtual fibril network was generated to model the microflow pattern across inter-vessel pit membranes. Moreover, the mechanical behavior of intervessel pit membranes was estimated from a single microfibril's mechanical property. Pit membranes morphology varied among different angiosperm and gymnosperm species. Our modelling work suggested that larger pores of pit membranes do not necessarily contribute to major flow rate across pit membranes; instead, the obstructed degree of flow pathway across the pit membranes plays a more important role. Our work provides useful information for studying the mechanism of microfluid flow transport across pit membranes and also sheds light on investigating the response of pit membranes both at normal and stressed conditions, thus improving our understanding on functional roles of pit membranes in xylem hydraulic function. Further work could be done to study the morphological and mechanical response of bordered pit membranes under different dehydrated conditions, as well as the related microflow behavior, based on our constructed model.

Pore constrictions in intervessel pit membranes provide a mechanistic explanation for xylem embolism resistance in angiosperms

“…Second, estimations based on the Young-Laplace equation should be interpreted with caution due to various poorly known parameters and processes when applying this formula to xylem conduits. Embolism formation in a multiphase environment under negative pressure is highly complicated by, for instance, dynamic surface tension, line tension, the contact angle of the gas-liquid interface within the pit membrane, and highly variable pore sizes (Choat et al, 2004;Law et al, 2017;Schenk et al, 2017;Satarifard et al, 2018;Li et al, 2020;Yang et al, 2020;Zhang et al, 2020). Moreover, pore constrictions and porosity could change if pit membranes become deflected and aspirated against the pit border, which could cause pit membrane shrinkage, reduced porosity and constrictivity, or rearrangement of microfibrils (Tixier et al, 2014;Zhang et al, 2017Zhang et al, , 2020Kotowska et al, 2020).…”

“…Further progress in understanding embolism spreading in angiosperm xylem will strongly depend on the development of realistic three-dimensional pit membrane and vessel network models (Gaiselmann et al, 2014;Mrad et al, 2018;Li et al, 2020), combined with careful simulations of the chemical and physical interactions within a multiphase environment of gas, water, cellulose, and surfactants. Table S1 Dataset of the 31 angiosperm species studied, with reference to the anatomical and hydraulic traits measured.…”

Xylem Functional Traits as Indicators of Health in Mediterranean Forests

“…The hypothesis that other xylem functional traits may perform better as indicators of Mediterranean forest decline and dieback under increasing drought than the traits examined here cannot be ruled out. Future research may address this point, hopefully with common-garden replicated experiments in which wider ranges of xylem traits are studied, possibly including less frequently investigated traits, such as porosity and surface characteristics of pit membranes connecting xylem conduits [102,103], with more careful attention being paid to plant hydraulic segmentation [2], junction-constricted zones and root tissues, changes in the allometry of xylem traits [104]. Also, the increasingly available evidence that hydraulic vulnerability is likely to involve extra-xilary variables should be considered [105•, 107].…”

Three-dimensional imaging of xylem at cell wall level through near field nano holotomography

“…light and electron microscopy), the possibility of non-destructive 3D examinations of the internal plant structure. This advantage has often been used for studies on the hydraulic architecture of trees and other xylary plants 10 – 14 representing one of the major trends in the field of tree-water relations since a few decades 15 – 18 . Several anatomical traits like tracheid diameter in softwoods and vessel size in hardwoods play a role in determining the trade-off between hydraulic efficiency and hydraulic safety, whereby pits with their membranes are believed to represent the key structure in this complex system 19 , 20 .…”

“…However, microCT can barely reach the resolution needed to visualize the pit membrane. Pit membranes may vary distinctly in their thickness from 100 nm up to over 1 µm, whereby the majority has a thickness of below 500 nm, especially intervessel pits in angiosperms 18 , 23 .…”