Pit characters determine drought-induced embolism resistance of leaf xylem across 18 Neotropical tree species

Abstract

Embolism spreading in xylem is an important component of plant drought resistance. Since embolism resistance has been shown to be mechanistically linked to pit membrane characters in stem xylem, we speculate that similar mechanisms account for leaf xylem. We conducted transmission electron microscopy to investigate pit membrane characters in leaf xylem across 18 Neotropical tree species. We also conducted gold perfusion and polar lipid detection experiments on three species covering the full range of leaf embolism resistance. We then related these observations to previously published data on embolism resistance of leaf xylem. We also incorporated previously published data on stem embolism resistance and stem xylem pit membranes to investigate the link between vulnerability segmentation (i.e., difference in embolism resistance) and leaf-stem anatomical variation. Pit membrane thickness (Tpm,max) and the pit membrane thickness-to-diameter ratio (Tpm,max/Dpm) were predictive of leaf embolism resistance, especially when vestured pits were taken into account. Variation in Tpm,max/Dpm was the only trait predictive of vulnerability segmentation between leaves and stems. Gold particles of 5 and 10 nm infiltrated pit membranes in three species, while the entry of 50-nm particles was blocked. Moreover, polar lipids were associated with inner conduit walls and pits. Our results suggest that mechanisms related to embolism spreading are determined by pit membrane thickness, pore constrictions (i.e., the narrowest bottlenecks along pore pathways), and lipid surfactants, which are largely similar between leaf and stem xylem and between temperate and tropical trees. However, our mechanistic understanding of embolism propagation and the functional relevance of Tpm,max/Dpm remains elusive.

Ageing-induced shrinkage of intervessel pit membranes in xylem of Clematis vitalba modifies its mechanical properties as revealed by atomic force microscopy

“…At the pit level, Clematis should therefore be somewhat more susceptible to embolism than Fraxinus americana . Moreover, there is experimental evidence for a relationship between embolism resistance and the pit membrane diameter-to-thickness ratio ( Levionnois et al., 2021 ; Levionnois et al., 2022 ), suggesting that the deflection resistance of pit membranes may affect embolism propagation. Yet, it remains unclear how pit membrane thickness of fully hydrated, non-shrunken pit membranes may affect its elasticity modulus.…”

Linking leaf embolism resistance with pit membrane characteristics

“…Unlike T PM , Levionnois et al (2022) found pit membrane diameter ( D PM ) and the ratio between maximum pit membrane thickness to pit membrane diameter ( T PM / D PM ) to be well correlated with P 50 at the species level for non-vestured pit species. This may suggest that, unlike T PM , D PM and T PM / D PM might not exhibit a large variation within species.…”

“…E, Scanning electron microscope (SEM) image of hazelnut ( Corylus avellana ) showing a “single layer” of a pit membrane and large, artificial pores, which does not represent an intact pit membrane under natural conditions. F, TEM image showing penetration of gold particles of different sizes into a pit membrane (outlined by blue lines) of camphor tree ( Cinnamomum camphora ), that is, a method used by Levionnois et al (2022) to estimate pore constriction size. The perfusion direction of 5, 10, 20, and 50 nm particles was from right to left, with small particles going deeper into the membrane than larger ones.…”

“…Yet, unlike the case with stems, the structural determinants of embolism resistance in leaves remain largely unknown. In this issue of Plant Physiology , Levionnois et al (2022) assessed the linkage between leaf embolism resistance and pit membrane characteristics across Neotropical tree species, providing valuable insights into the xylem embolism resistance of leaves.…”

Stems matter: Xylem physiological limits are an accessible and critical improvement to models of plant gas exchange in deep time

“…Although xylem cavitation and embolism are easily observed in plants, the mechanics of xylem hydraulic failure processes in vivo remain a topic of active study in plant physiology (see Venturas et al, 2017 for a review). Recently, pit membrane characteristics (i.e., pore constrictions and pit membrane thickness) have been implicated as a primary mechanism in the mechanics of xylem hydraulic failure (Thonglim et al, 2021;Avila et al, 2022;Levionnois et al, 2022), making them an obvious target for predictive modeling. However, pit membranes are rarely preserved in the fossil record.…”