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

Abstract

Embolism spreading in angiosperm xylem occurs via mesoporous pit membranes between vessels. Here, we investigate how the size of pore constrictions in pit membranes is related to pit membrane thickness and embolism resistance.Pit membranes were modelled as multiple layers to investigate how pit membrane thickness and the number of intervessel pits per vessel determine pore constriction sizes, the probability of encountering large pores, and embolism resistance. These estimations were complemented by measurements of pit membrane thickness, embolism resistance, and number of intervessel pits per vessel in stem xylem (n = 31, 31 and 20 species, respectively).The modelled constriction sizes in pit membranes decreased with increasing membrane thickness, explaining the measured relationship between pit membrane thickness and embolism resistance. The number of pits per vessel affected constriction size and embolism resistance much less than pit membrane thickness. Moreover, a strong relationship between modelled and measured embolism resistance was observed.Pore constrictions provide a mechanistic explanation for why pit membrane thickness determines embolism resistance, which suggests that hydraulic safety can be uncoupled from hydraulic efficiency. Although embolism spreading remains puzzling and encompasses more than pore constriction sizes, angiosperms are unlikely to have leaky pit membranes, which enables tensile transport of water.

Limited plasticity in embolism resistance in response to light in leaves and stems in species with considerable vulnerability segmentation

“…These traits either impair the deformation of vessel conduits under tension (Blackman et al, 2010;Hacke et al, 2001), delay the initial seeding of embolism events, or the spread of air bubbles between conduits once an initial embolism has formed (Brodersen et al, 2014;Choat et al, 2008;Johnson et al, 2020;Kaack et al, 2021;Li et al, 2016). Unlike variation between species, we have even less of an understanding of plasticity in P 50 or which xylem traits might drive intraspecific variation in embolism resistance.…”

“…Species that present higher resistance to embolism often have higher ( t/b ) 2 and pit membrane thickness as well as decreased vessel diameter and shorter vessel lengths (Blackman et al, 2010; Brodersen et al, 2014; Choat et al, 2008; Hacke et al, 2001; Jacobsen et al, 2016; Lens et al, 2011; Li et al, 2016; Scoffoni et al, 2016). These traits either impair the deformation of vessel conduits under tension (Blackman et al, 2010; Hacke et al, 2001), delay the initial seeding of embolism events, or the spread of air bubbles between conduits once an initial embolism has formed (Brodersen et al, 2014; Choat et al, 2008; Johnson et al, 2020; Kaack et al, 2021; Li et al, 2016). Unlike variation between species, we have even less of an understanding of plasticity in P 50 or which xylem traits might drive intraspecific variation in embolism resistance.…”

A clear trade‐off between leaf hydraulic efficiency and safety in an aridland shrub during regrowth

“…The linkage between hydraulic efficiency and safety initially arises from xylem conduits. Plants with more and smaller xylem conduits, or greater pore membrane thickness to prevent cavitation due to air‐seeding, will maximize hydraulic safety (Gleason et al, 2015; Hillabrand, Hacke, & Lieffers, 2016; Jansen, Choat, & Pletsers, 2009; Kaack et al, 2021). However, small conduit diameters would sacrifice hydraulic efficiency, as high xylem efficiency occurs with larger conduits according to Poiseuille's law (Gleason et al, 2015; Pfautsch et al, 2016).…”

Tree Mortality: Testing the Link Between Drought, Embolism Vulnerability, and Xylem Conduit Diameter Remains a Priority

“…This is in contrast to freezing-induced embolism, which has a consistent and wellunderstood relationship with conduit diameter (Cavender-Bares and Holbrook, 2001;Sperry, 2003, 2006;Cavender-Bares, 2005;Sevanto et al, 2012;Savage and Cavender-Bares, 2013). Failure of water transport under drought is certain to involve multiple factors, from wood density and pit membrane characteristics to internal conduit sculpture, the types of conductive cells present in the xylem and where gas exists in the xylem (Dalla-Salda et al, 2011;Sano et al, 2011;Li et al, 2016;Guan et al, 2021;Kaack et al, 2021). But all else being equal, wider conduits tend to be longer than narrow conduits, with a higher number of pits, which are often wider and with wider membrane pores (Martínez-Vilalta et al, 2002;Jacobsen et al, 2012Jacobsen et al, , 2019.…”