Summary: 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.

Abiotic stresses could have complex and diverse effects on the growth and development of forest trees. In this review, we summarized the responses of morphological, physiological and anatomical traits in woody plants to abiotic stresses, including drought, flood, extreme temperature, salinity, heavy metal, microplastics and combined stresses, especially from the xylem perspective. Under most abiotic stress, xylem hydraulic conductivity decreases, which is associated with leaf stomatal regulation and the inhibition of aquaporin (AQP) activity. Meanwhile, woody plants regulate the size and morphology of their roots and leaves to balance water absorption and transpiration. The anatomical traits are also altered, such as denser leaf stomata, narrower conduits and thicker cell walls. In addition, different stresses have unique effects, such as flood-induced adventitious roots and aeration tissues, forest fire-induced irreversible xylem damage, low temperature-induced tissue freezing, salt stress-induced hinderance of ion absorption and heavy metal-induced biological toxicity. Under stresses of drought, flooding and heavy metals, woody plants’ growth may occasionally be promoted. The effects of combined stress on the physiological, morphological and anatomical traits of woody plants are not simply additive, with the related mechanism to be further studied, especially in natural or near-natural conditions.

Xylem traits are critical plant functional traits associated with water transport, mechanical support, and carbohydrate and water storage. Studies on the xylem hydraulic efficiency–safety tradeoff are numerous; however, the storage function of xylem parenchyma is rarely considered. The effects of a substantial number of xylem traits on water transport, embolism resistance, mechanical support, storage capacity and nonstructural carbohydrate (NSC) content were investigated in 19 temperate broadleaf species planted in an arid limestone habitat in northern China. There was no xylem hydraulic efficiency–safety tradeoff in the 19 broadleaf species. The total parenchyma fraction was negatively correlated with the fiber fraction. Embolism resistance was positively correlated with indicators of xylem mechanical strength such as vessel wall reinforcement, vessel wall thickness and fiber wall thickness, and was negatively related to the axial parenchyma fraction, especially the paratracheal parenchyma fraction. The paratracheal parenchyma fraction was positively correlated with the ratio of the paratracheal parenchyma fraction to the vessel fraction. In addition, the xylem NSC concentration was positively related to the total parenchyma fraction and axial parenchyma fraction. There was a storage capacity–embolism resistance tradeoff in the xylem of 19 broadleaf species in arid limestone habitats. We speculate that the temperate broadleaf species may show a spectrum of xylem hydraulic strategies, from the embolism resistance strategy related to a more negative P50 (the water potential corresponding to 50% loss of xylem conductivity) to the embolization repair strategy based on more paratracheal parenchyma.

Studying how cambial age and axial height affects wood anatomical traits may improve our understanding of xylem hydraulics, heartwood formation and axial growth. Radial strips were collected from six different heights (0–11.3 m) along the main trunk of three Manchurian catalpa (Catalpa bungei) trees, yielding 88 samples. In total, thirteen wood anatomical vessel and fiber traits were observed usinglight microscopy (LM) and scanning electron microscopy (SEM), and linear models were used to analyse the combined effect of axial height, cambial age and their interaction. Vessel diameter differed by about one order of magnitude between early- and latewood, and increased significantly with both cambial age and axial height in latewood, while it was positively affected by cambial age and independent of height in earlywood. Vertical position further had a positive effect on earlywood vessel density, and negative effects on fibre wall thickness, wall thickness to diameter ratio and length. Cambial age had positive effects on the pit membrane diameter and vessel element length, while the annual diameter growth decreased with both cambial age and axial position. In contrast, early- and latewood fiber diameter were unaffected by both cambial age and axial height. We further observed an increasing amount of tyloses from sapwood to heartwood, accompanied by an increase of warty layers and amorphous deposits on cell walls, bordered pit membranes and pit apertures. This study highlights the significant effects of cambial age and vertical position on xylem anatomical traits, and confirms earlier work that cautions to take into account xylem spatial position when interpreting wood anatomical structures, and thus, xylem hydraulic functioning.

Forests are vital ecosystems that are increasingly threatened by environmental stress; exploring the possible trade-off between hydraulic safety and efficiency in plant xylem is crucial to understanding their environmental adaptation strategies. However, to date, there is no consensus whether such trade-offs exist among and within species. To better comprehend the mechanism of xylem water transport, in this review, we summarized previously published work on xylem hydraulic safety and efficiency trade-off from the inter-species, intra-species, and intra-tree perspectives and its influencing factors. We gathered data on xylem hydraulic safety and efficiency and their related anatomical traits, i.e., conduit diameter and inter-conduit pit membrane thickness, from a total of 653 plant species analyzed in 80 published papers. At the inter-species level, we confirmed that there is a weak hydraulic safety and efficiency trade-off. For gymnosperms and herbaceous species, the observed trade-off is stronger. At the intra-species level, the hydraulic safety and efficiency trade-off was found in individuals of the same species investigated in the literature. At the intra-tree level, there is a trade-off between hydraulic safety and efficiency for leaves, stems, and roots, and we confirmed the vessel widening hypothesis, i.e., vessel diameter in the outer wood increases from the top to the bottom of the tree. Additionally, pit membrane thickness increases as the tree height decreases, thus increasing the xylem hydraulic efficiency and affecting the trade-off. Finally, we discussed the environmental factors affecting the trade-off between hydraulic safety and efficiency in the xylem, such as plant habitats, temperature, rainfall, altitude, and soil. Further investigations of the bordered pit membrane from the three-dimensional perspective would be useful to understand the hydraulic safety and efficiency trade-off at the nanoscale.

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.