Is Decreased Xylem Sap Surface Tension Associated With Embolism and Loss of Xylem Hydraulic Conductivity in Pathogen-Infected Norway Spruce Saplings?

Increased abiotic stress along with increasing temperatures, dry periods and forest disturbances may favor biotic stressors such as simultaneous invasion of bark beetle and ophiostomatoid fungi. It is not fully understood how tree desiccation is associated with colonization of sapwood by fungi. A decrease in xylem sap surface tension (sigma(xylem)) as a result of infection has been hypothesized to cause xylem embolism by lowering the threshold for air-seeding at the pits between conduits and disruptions in tree water transport. However, this hypothesis has not yet been tested. We investigated tree water relations by measuring the stem xylem hydraulic conductivity (K-stem), sigma(xylem), stem relative water content (RWCstem), and water potential (psi(stem)), and canopy conductance (g(canopy)), as well as the compound composition in xylem sap in Norway spruce (Picea abies) saplings. We conducted our measurements at the later stage ofEndoconidiophora polonicainfection when visible symptoms had occurred in xylem. Saplings of two clones (44 trees altogether) were allocated to treatments of inoculated, wounded control and intact control trees in a greenhouse. The saplings were destructively sampled every second week during summer 2016. sigma(xylem), K(stem)and RWC(stem)decreased following the inoculation, which may indicate that decreased sigma(xylem)resulted in increased embolism. g(canopy)did not differ between treatments indicating that stomata responded to psi(stem)rather than to embolism formation. Concentrations of quinic acid, myo-inositol, sucrose and alkylphenol increased in the xylem sap of inoculated trees. Myo-inositol concentrations also correlated negatively with sigma(xylem)and K-stem. Our study is a preliminary investigation of the role of sigma(xylem)inE. polonicainfected trees based on previous hypotheses. The results suggest thatE. polonicainfection can lead to a simultaneous decrease in xylem sap surface tension and a decline in tree hydraulic conductivity, thus hampering tree water transport.Peer reviewe

Is Decreased Xylem Sap Surface Tension Associated With Embolism and Loss of Xylem Hydraulic Conductivity in Pathogen-Infected Norway Spruce Saplings?

Increased abiotic stress along with increasing temperatures, dry periods and forest disturbances may favor biotic stressors such as simultaneous invasion of bark beetle and ophiostomatoid fungi. It is not fully understood how tree desiccation is associated with colonization of sapwood by fungi. A decrease in xylem sap surface tension (sigma(xylem)) as a result of infection has been hypothesized to cause xylem embolism by lowering the threshold for air-seeding at the pits between conduits and disruptions in tree water transport. However, this hypothesis has not yet been tested. We investigated tree water relations by measuring the stem xylem hydraulic conductivity (K-stem), sigma(xylem), stem relative water content (RWCstem), and water potential (psi(stem)), and canopy conductance (g(canopy)), as well as the compound composition in xylem sap in Norway spruce (Picea abies) saplings. We conducted our measurements at the later stage ofEndoconidiophora polonicainfection when visible symptoms had occurred in xylem. Saplings of two clones (44 trees altogether) were allocated to treatments of inoculated, wounded control and intact control trees in a greenhouse. The saplings were destructively sampled every second week during summer 2016. sigma(xylem), K(stem)and RWC(stem)decreased following the inoculation, which may indicate that decreased sigma(xylem)resulted in increased embolism. g(canopy)did not differ between treatments indicating that stomata responded to psi(stem)rather than to embolism formation. Concentrations of quinic acid, myo-inositol, sucrose and alkylphenol increased in the xylem sap of inoculated trees. Myo-inositol concentrations also correlated negatively with sigma(xylem)and K-stem. Our study is a preliminary investigation of the role of sigma(xylem)inE. polonicainfected trees based on previous hypotheses. The results suggest thatE. polonicainfection can lead to a simultaneous decrease in xylem sap surface tension and a decline in tree hydraulic conductivity, thus hampering tree water transport.Peer reviewe

Evaluating theories of drought-induced vegetation mortality using a multimodel– experiment framework

Model–data comparisons of plant physiological processes provide an understanding of mechanisms underlying vegetation responses to climate. We simulated the physiology of a pi~non pine–juniper woodland (Pinus edulis–Juniperus monosperma) that experienced mortality during a 5 yr precipitation-reduction experiment, allowing a framework with which to examine our knowledge of drought-induced tree mortality. We used six models designed for scales ranging from individual plants to a global level, all containing state-of-the-art representations of the internal hydraulic and carbohydrate dynamics of woody plants. Despite the large range of model structures, tuning, and parameterization employed, all simulations predicted hydraulic failure and carbon starvation processes co-occurring in dying trees of both species, with the time spent with severe hydraulic failure and carbon starvation, rather than absolute thresholds per se, being a better predictor of impending mortality. Model and empirical data suggest that limited carbon and water exchanges at stomatal, phloem, and below-ground interfaces were associated with mortality of both species. The model–data comparison suggests that the introduction of a mechanistic process into physiology-based models provides equal or improved predictive power over traditional process-model or empirical thresholds. Both biophysical and empirical modeling approaches are useful in understanding processes, particularly when the models fail, because they reveal mechanisms that are likely to underlie mortality. We suggest that for some ecosystems, integration of mechanistic pathogen models into current vegetation models, and evaluation against observations, could result in a breakthrough capability to simulate vegetation dynamics.Keywords: carbon starvation, hydraulic failure, process-based models, cavitation, dynamic global vegetation models (DGVMs), die off, photosynthesi

New insights into the covariation of stomatal, mesophyll and hydraulic conductances from optimization models incorporating nonstomatal limitations to photosynthesis

Optimization models of stomatal conductance (g(s)) attempt to explain observed stomatal behaviour in terms of cost-benefit tradeoffs. While the benefit of stomatal opening through increased CO2 uptake is clear, currently the nature of the associated cost(s) remains unclear. We explored the hypothesis that g(s) maximizes leaf photosynthesis, where the cost of stomatal opening arises from nonstomatal reductions in photosynthesis induced by leaf water stress. We analytically solved two cases, CAP and MES, in which reduced leaf water potential leads to reductions in carboxylation capacity (CAP) and mesophyll conductance (g(m)) (MES). Both CAP and MES predict the same one-parameter relationship between the intercellular:atmospheric CO2 concentration ratio (c(i)/c(a)) and vapour pressure deficit (VPD, D), viz. c(i)/c(a) approximate to xi/xi (xi+D), as that obtained from previous optimization models, with the novel feature that the parameter xi is determined unambiguously as a function of a small number of photosynthetic and hydraulic variables. These include soil-to-leaf hydraulic conductance, implying a stomatal closure response to drought. MES also predicts that g(s)/g(m) is closely related to c(i)/c(a) and is similarly conservative. These results are consistent with observations, give rise to new testable predictions, and offer new insights into the covariation of stomatal, mesophyll and hydraulic conductances.Peer reviewe

Leaf carbon and water status control stomatal and nonstomatal limitations of photosynthesis in trees

Photosynthetic rate is concurrently limited by stomatal limitations and nonstomatal limitations (NSLs). However, the controls on NSLs to photosynthesis and their coordination with stomatal control on different timescales remain poorly understood. According to a recent optimization hypothesis, NSLs depend on leaf osmotic or water status and are coordinated with stomatal control so as to maximize leaf photosynthesis. Drought and notching experiments were conducted on Pinus sylvestris, Picea abies, Betula Pendula and Populus tremula seedlings in glasshouse conditions to study the dependence of NSLs on leaf osmotic and water status, and their coordination with stomatal control, on timescales of minutes and weeks, to test the assumptions and predictions of the optimization hypothesis. Both NSLs and stomatal conductance followed power-law functions of leaf osmotic concentration and leaf water potential. Moreover, stomatal conductance was proportional to the square root of soil-to-leaf hydraulic conductance, as predicted by the optimization hypothesis. Though the detailed mechanisms underlying the dependence of NSLs on leaf osmotic or water status lie outside the scope of this study, our results support the hypothesis that NSLs and stomatal control are coordinated to maximize leaf photosynthesis and allow the effect of NSLs to be included in models of tree gas-exchange.Peer reviewe

Capacitive effect of cavitation in xylem conduits: results from a dynamic model

Embolisms decrease plant hydraulic conductance and therefore reduce the ability of the xylem to transport water to leaves provided that embolized conduits are not refilled. However, as a xylem conduit is filled with gas during cavitation, water is freed to the transpiration stream and this transiently increases xylem water potential. This capacitive effect of embolism formation on plant function has not been explicitly quantified in the past. A dynamic model is presented that models xylem water potential, xylem sap flow and cavitation, taking into account both the decreasing hydraulic conductance and the water release effect of xylem embolism. The significance of the capacitive effect increases in relation to the decreasing hydraulic conductance effect when transpiration rate is low in relation to the total amount of water in xylem conduits. This ratio is typically large in large trees and during drought

New insights into the covariation of stomatal, mesophyll and hydraulic conductances from optimization models incorporating nonstomatal limitations to photosynthesis

Optimization models of stomatal conductance (gs) attempt to explain observed stomatal behaviour in terms of cost--benefit tradeoffs. While the benefit of stomatal opening through increased CO2 uptake is clear, currently the nature of the associated cost(s) remains unclear. We explored the hypothesis that gs maximizes leaf photosynthesis, where the cost of stomatal opening arises from nonstomatal reductions in photosynthesis induced by leaf water stress. We analytically solved two cases, CAP and MES, in which reduced leaf water potential leads to reductions in carboxylation capacity (CAP) and mesophyll conductance (gm) (MES). Both CAP and MES predict the same one-parameter relationship between the intercellular : atmospheric CO2 concentration ratio (ci/ca) and vapour pressure deficit (VPD, D), viz. ci/ca ≈ ξ/(ξ + √D), as that obtained from previous optimization models, with the novel feature that the parameter ξ is determined unambiguously as a function of a small number of photosynthetic and hydraulic variables. These include soil-to-leaf hydraulic conductance, implying a stomatal closure response to drought. MES also predicts that gs/gm is closely related to ci/ca and is similarly conservative. These results are consistent with observations, give rise to new testable predictions, and offer new insights into the covariation of stomatal, mesophyll and hydraulic conductances.This study was supported by the Australian Research Council (DP160103436), the Academy of Finland (Centre of Excellence 272041, 118780 and Academy Professor 1284701, 1282842), the Knut and Alice Wallenberg Foundation (2015.0047) and the University of Helsinki (AtMath project)

An empirical method that separates irreversible stem radial growth from bark water content changes in trees: theory and case studies

Substantial uncertainty surrounds our knowledge of tree stem growth, with some of the most basic questions, such as when stem radial growth occurs through the daily cycle, still unanswered. We employed high-resolution point dendrometers, sap flow sensors, and developed theory and statistical approaches, to devise a novel method separating irreversible radial growth from elastic tension-driven and elastic osmotically driven changes in bark water content. We tested this method using data from five case study species. Experimental manipulations, namely a field irrigation experiment on Scots pine and a stem girdling experiment on red forest gum trees, were used to validate the theory. Time courses of stem radial growth following irrigation and stem girdling were consistent with a-priori predictions. Patterns of stem radial growth varied across case studies, with growth occurring during the day and/or night, consistent with the available literature. Importantly, our approach provides a valuable alternative to existing methods, as it can be approximated by a simple empirical interpolation routine that derives irreversible radial growth using standard regression techniques. Our novel method provides an improved understanding of the relative source–sink carbon dynamics of tree stems at a sub-daily time scale.This research was funded by the Natural Environment Research Council (NERC) grant NE/I011749/1 to MM and PM. MM was also supported by a Western Sydney University Eminent Research Visitor grant (11/022839) and a CSIRO President visiting fellowshi