Xylem vulnerability to embolism is emerging as a major factor in drought-induced tree mortality events across the globe. However, we lack understanding of how and to what extent climate has shaped ...vascular properties or functions. We investigated the evolution of xylem hydraulic function and diversification patterns in Australia’s most successful gymnosperm clade, Callitris, the world’s most drought-resistant conifers.
For all 23 species in this group, we measured embolism resistance (P
50), xylem specific hydraulic conductivity (K
s), wood density, and tracheary element size from natural populations. We investigated whether hydraulic traits variation linked with climate and the diversification of this clade using a time-calibrated phylogeny.
Embolism resistance varied widely across the Callitris clade (P
50: −3.8 to −18.8 MPa), and was significantly related to water scarcity, as was tracheid diameter. We found no evidence of a safety-efficiency tradeoff; K
s and wood density were not related to rainfall. Callitris diversification coincides with the onset of aridity in Australia since the early Oligocene.
Our results highlight the evolutionary lability of xylem traits with climate, and the leading role of aridity in the diversification of conifers. The uncoupling of safety from other xylem functions allowed Callitris to evolve extreme embolism resistance and diversify into xeric environments.
Water inside plants forms a continuous chain from water in soils to the water evaporating from leaf surfaces. Failures in this chain result in reduced transpiration and photosynthesis and are caused ...by soil drying and/or cavitation‐induced xylem embolism. Xylem embolism and plant hydraulic failure share several analogies to ‘catastrophe theory’ in dynamical systems. These catastrophes are often represented in the physiological and ecological literature as tipping points when control variables exogenous (e.g., soil water potential) or endogenous (e.g., leaf water potential) to the plant are allowed to vary on time scales much longer than time scales associated with cavitation events. Here, plant hydraulics viewed from the perspective of catastrophes at multiple spatial scales is considered with attention to bubble expansion within a xylem conduit, organ‐scale vulnerability to embolism, and whole‐plant biomass as a proxy for transpiration and hydraulic function. The hydraulic safety‐efficiency tradeoff, hydraulic segmentation and maximum plant transpiration are examined using this framework. Underlying mechanisms for hydraulic failure at fine scales such as pit membranes and cell‐wall mechanics, intermediate scales such as xylem network properties and at larger scales such as soil–tree hydraulic pathways are discussed. Understudied areas in plant hydraulics are also flagged where progress is urgently needed.
Summary statement
Hydraulic failure in plants and tipping points in ecosystem processes are examples of catastrophes in dynamical systems. Here, these phenomena are reviewed at bubble, xylem network and whole‐plant scales and the underlying mechanisms that result in these catastrophes are explored.
Summary
The long‐standing hypothesis that the isotopic composition of plant stem water reflects that of source water is being challenged by studies reporting bulk water from woody stems with an ...isotopic composition that cannot be attributed to any potential water source. The mechanism behind such source–stem water isotopic offsets is still poorly understood.
Using a novel technique to extract selectively sap water from xylem conduits, we show that, in cut stems and potted plants, the isotopic composition of sap water reflects that of irrigation water, demonstrating unambiguously that no isotopic fractionation occurs during root water uptake or sap water extraction. By contrast, water in nonconductive xylem tissues is always depleted in deuterium compared with sap water, irrespective of wood anatomy.
Previous studies have shown that isotopic heterogeneity also exists in soils at the pore scale in which water adsorbed onto soil particles is more depleted in deuterium than unbound water. Data collected at a riparian forest indicated that sap water matches best unbound soil water from depth below −70 cm, while bulk stem and soil water differ markedly.
We conclude that source–stem isotopic offsets can be explained by micrometre‐scale heterogeneity in the isotope ratios of water within woody stems and soil micro‐pores.
The vast majority of measurements in the field of plant hydraulics have been on small‐diameter branches from woody species. These measurements have provided considerable insight into plant ...functioning, but our understanding of plant physiology and ecology would benefit from a broader view, because branch hydraulic properties are influenced by many factors. Here, we discuss the influence that other components of the hydraulic network have on branch vulnerability to embolism propagation. We also modelled the impact of changes in the ratio of root‐to‐leaf areas and soil texture on vulnerability to hydraulic failure along the soil‐to‐leaf continuum and showed that hydraulic function is better maintained through changes in root vulnerability and root‐to‐leaf area ratio than in branch vulnerability. Differences among species in the stringency with which they regulate leaf water potential and in reliance on stored water to buffer changes in water potential also affect the need to construct embolism resistant branches. Many approaches, such as measurements on fine roots, small individuals, combining sap flow and psychrometry techniques, and modelling efforts, could vastly improve our understanding of whole‐plant hydraulic functioning. A better understanding of how traits are coordinated across the whole plant will improve predictions for plant function under future climate conditions.
Vulnerability to embolism in branches has been the primary focus of research in plant hydraulics. However, co‐occurring species exhibit large amounts of variation in this metric because of differences in other aspects of the hydraulic network, including differences in root‐to‐leaf ratio, regulation of leaf water potential, and reliance on stored water.
Summary
Wood anatomical traits shape a xylem segment’s hydraulic efficiency and resistance to embolism spread due to declining water potential. It has been known for decades that variations in ...conduit connectivity play a role in altering xylem hydraulics. However, evaluating the precise effect of conduit connectivity has been elusive. The objective here is to establish an analytical linkage between conduit connectivity and grouping and tissue‐scale hydraulics.
It is hypothesized that an increase in conduit connectivity brings improved resistance to embolism spread due to increased hydraulic pathway redundancy. However, an increase in conduit connectivity could also reduce resistance due to increased speed of embolism spread with respect to pressure. We elaborate on this trade‐off using graph theory, percolation theory and computational modeling of xylem. The results are validated using anatomical measurements of Acer branch xylem.
Considering only species with vessels, increases in connectivity improve resistance to embolism spread without negatively affecting hydraulic conductivity. The often measured grouping index fails to capture the totality of the effect of conduit connectivity on xylem hydraulics.
Variations in xylem network characteristics, such as conduit connectivity, might explain why hypothesized trends among woody species, such as the ‘safety‐efficiency’ trade‐off hypothesis, are weaker than expected.
Plant xylem response to drought is routinely represented by a vulnerability curve (VC). Despite the significance of VCs, the connection between anatomy and tissue‐level hydraulic response to drought ...remains a subject of inquiry. We present a numerical model of water flow in flowering plant xylem that combines current knowledge on diffuse‐porous anatomy and embolism spread to explore this connection. The model produces xylem networks and uses different parameterizations of intervessel connection vulnerability to embolism spread: the Young–Laplace equation and pit membrane stretching. Its purpose is upscaling processes occurring on the microscopic length scales, such as embolism propagation through pit membranes, to obtain tissue‐scale hydraulics. The terminal branch VC of Acer glabrum was successfully reproduced relying only on real observations of xylem tissue anatomy. A sensitivity analysis shows that hydraulic performance and VC shape and location along the water tension axis are heavily dependent on anatomy. The main result is that the linkage between pit‐scale and vessel‐scale anatomical characters, along with xylem network topology, affects VCs significantly. This work underscores the importance of stepping up research related to the three‐dimensional network structure of xylem tissues. The proposed model's versatility makes it an important tool to explore similar future questions.
This work introduces a new open source numerical model of plant xylem. The subject of inquiry is the link between wood anatomy and plant water use, especially vulnerability to embolism under drought. The model successfully reproduces empirical vulnerability curves of Acer terminal branches. The results of this study underscore the importance of stepping up research on the effects of xylem network topology on whole‐plant hydraulics.
Understanding mass transport of photosynthates in the phloem of plants is necessary for predicting plant carbon allocation, productivity, and responses to water and thermal stress. Several hypotheses ...about optimization of phloem structure and function and limitations of phloem transport under drought have been proposed and tested with models and anatomical data. However, the true impact of radial water exchange of phloem conduits with their surroundings on mass transport of photosynthates has not been addressed. Here, the physics of the Munch mechanism of sugar transport is re-evaluated to include local variations in viscosity resulting from the radial water exchange in two dimensions (axial and radial) using transient flow simulations. Model results show an increase in radial water exchange due to a decrease in sap viscosity leading to increased sugar front speed and axial mass transport across a wide range of phloem conduit lengths. This increase is around 40% for active loaders (e.g. crops) and around 20% for passive loaders (e.g. trees). Thus, sugar transport operates more efficiently than predicted by previous models that ignore these two effects. A faster front speed leads to higher phloem resiliency under drought because more sugar can be transported with a smaller pressure gradient.
Defining plant hydraulic traits is central to the quantification of ecohydrological processes ranging from land‐atmosphere interactions, to tree mortality and water‐carbon budgets. A key plant trait ...is the xylem specific hydraulic conductivity (Kx), that describes the plant's vascular system capacity to transport water. While xylem's vessels and tracheids are dead upon maturity, the xylem is neither inert nor deadwood, various components of the sapwood and surrounding tissue remaining alive and functional. Moreover, the established definition of Kx assumes linear relations between water flux and pressure gradient by tacitly considering the xylem as a “passive conduit”. Here, we re‐examine this notion of an inert xylem by systematically characterizing xylem flow in several woody plants using Kx measurements under constant and cyclic pressure gradients. Results show a temporal and pressure gradient dependence of Kx. Additionally, microscopic features in “living branches” are irreversibly modified upon drying of the xylem, thus differentiating the macroscopic definition of Kx for living and dead xylem. The findings highlight the picture of the xylem as a complex and delicate conductive system whose hydraulic behaviour transcends a passive gradient‐based flow. The study sheds new light on xylem conceptualization, conductivity measurement protocols, in situ long‐distance water transport and ecosystem modelling.
Xylem flow measurements using freshly cut branches show temporal and pressure‐dependent decrease in xylem hydraulic conductivity with active wound response of living xylem tissue. Results have notable implications for plant water relations and xylem conceptualization as a complex living system.
Water transport from soils to the atmosphere is critical for plant growth and survival. However, we have a limited understanding about many portions of the whole-tree hydraulic pathway, because the ...vast majority of published information is on terminal branches. Our understanding of mature tree trunk hydraulic physiology, in particular, is limited. The hydraulic vulnerability segmentation hypothesis (HVSH) stipulates that distal portions of the plant (leaves, branches and roots) should be more vulnerable to embolism than trunks, which are nonredundant organs that require a massive carbon investment. In the current study, we compared vulnerability to loss of hydraulic function, leaf and xylem water potentials and the resulting hydraulic safety margins (in relation to the water potential causing 50% loss of hydraulic conductivity) in leaves, branches, trunks and roots of four angiosperms and four conifer tree species. Across all species, our results supported strongly the HVSH as leaves and roots were less resistant to embolism than branches or trunks. However, branches were consistently more resistant to embolism than any other portion of the plant, including trunks. Also, calculated whole-tree vulnerability to hydraulic dysfunction was much greater than vulnerability in branches. This was due to hydraulic dysfunction in roots and leaves at less negative water potentials than those causing branch or trunk dysfunction. Leaves and roots had narrow or negative hydraulic safety margins, but trunks and branches maintained positive safety margins. By using branch-based hydraulic information as a proxy for entire plants, much research has potentially overestimated embolism resistance, and possibly drought tolerance, for many species. This study highlights the necessity to reconsider past conclusions made about plant resistance to drought based on branch xylem only. This study also highlights the necessity for more research of whole-plant hydraulic physiology to better understand strategies of plant drought tolerance and the critical control points within the hydraulic pathway.
Stomatal regulation is crucial for forest species performance and survival on drought‐prone sites. We investigated the regulation of root and shoot hydraulics in three Pinus radiata clones exposed to ...drought stress and its coordination with stomatal conductance (gs) and leaf water potential (Ψleaf). All clones experienced a substantial decrease in root‐specific root hydraulic conductance (Kroot‐r) in response to the water stress, but leaf‐specific shoot hydraulic conductance (Kshoot‐l) did not change in any of the clones. The reduction in Kroot‐r caused a decrease in leaf‐specific whole‐plant hydraulic conductance (Kplant‐l). Among clones, the larger the decrease in Kplant‐l, the more stomata closed in response to drought. Rewatering resulted in a quick recovery of Kroot‐r and gs. Our results demonstrated that the reduction in Kplant‐l, attributed to a down regulation of aquaporin activity in roots, was linked to the isohydric stomatal behaviour, resulting in a nearly constant Ψleaf as water stress started. We concluded that higher Kplant‐l is associated with water stress resistance by sustaining a less negative Ψleaf and delaying stomatal closure.
Reduced root hydraulic conductance, due to down‐regulation of root aquaporin activity under water stress, decreased whole‐plant hydraulic conductance, which was coupled with the stomatal closure to prevent the decline in leaf water potential in Pinus radiata.
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