skip to main content

Title: Coordination and trade‐offs between leaf and stem hydraulic traits and stomatal regulation along a spectrum of isohydry to anisohydry

The degree of plant iso/anisohydry, a widely used framework for classifying species‐specific hydraulic strategies, integrates multiple components of the whole‐plant hydraulic pathway. However, little is known about how it associates with coordination of functional and structural traits within and across different organs. We examined stem and leaf hydraulic capacitance and conductivity/conductance, stem xylem anatomical features, stomatal regulation of daily minimum leaf and stem water potential (Ψ), and the kinetics of stomatal responses to vapour pressure deficit (VPD) in six diverse woody species differing markedly in their degree of iso/anisohydry. At the stem level, more anisohydric species had higher wood density and lower native capacitance and conductivity. Like stems, leaves of more anisohydric species had lower hydraulic conductance; however, unlike stems, their leaves had higher native capacitance at their daily minimum values of leaf Ψ. Moreover, rates of VPD‐induced stomatal closure were related to intrinsic rather than native leaf capacitance and were not associated with species' degree of iso/anisohydry. Our results suggest a trade‐off between hydraulic storage and efficiency in the leaf, but a coordination between hydraulic storage and efficiency in the stem along a spectrum of plant iso/anisohydry.

more » « less
Author(s) / Creator(s):
 ;  ;  ;  ;  ;  ;  
Publisher / Repository:
Date Published:
Journal Name:
Plant, Cell & Environment
Page Range / eLocation ID:
p. 2245-2258
Medium: X
Sponsoring Org:
National Science Foundation
More Like this
  1. Abstract

    Over the past decade, the concept of isohydry or anisohydry, which describes the link between soil water potential (ΨS), leaf water potential (ΨL), and stomatal conductance (gs), has soared in popularity. However, its utility has recently been questioned, and a surprising lack of coordination between the dynamics of ΨLandgsacross biomes has been reported. Here, we offer a more expanded view of the isohydricity concept that considers effects of vapour pressure deficit (VPD) and leaf area index (AL) on the apparent sensitivities of ΨLandgsto drought. After validating the model with tree‐ and ecosystem‐scale data, we find that within a site, isohydricity is a strong predictor of limitations to stomatal function, though variation in VPD and leaf area, among other factors, can challenge its diagnosis. Across sites, the theory predicts that the degree of isohydricity is a good predictor of the sensitivity ofgsto declining soil water in the absence of confounding effects from other drivers. However, if VPD effects are significant, they alone are sufficient to decouple the dynamics of ΨLandgsentirely. We conclude with a set of practical recommendations for future applications of the isohydricity framework within and across sites.

    more » « less
  2. Abstract

    Isohydry (maintenance of plant water potential at the cost of carbon gain) and anisohydry (gas exchange maintenance at the cost of declining plant water status) make up two ends of a stomatal drought response strategy continuum. However, few studies have merged measures of stomatal regulation with xylem hydraulic safety strategies based on in situ field measurements. The goal of this study was to characterize the stomatal and xylem hydraulic safety strategies of woody species in the biodiverse Mediterranean‐type ecosystem region of California. Measurements were conducted in situ when California was experiencing the most severe drought conditions in the past 1,200 years. We found coordination among stomatal, hydraulic, and standard leaf functional traits. For example, stem xylem vulnerability to cavitation (P50) was correlated with the water potential at stomatal closure (Pclose); more resistant species had a more negative water potential at stomatal closure. The degree of isohydry–anisohydry, defined at Pclose–P50, was correlated with the hydraulic safety margin across species; more isohydric species had a larger hydraulic safety margin. In addition, we report for the first time Pclosevalues below −10 MPa. Measuring these traits in a biodiverse region under exceptional drought conditions contributes to our understanding of plant drought responses.

    more » « less
  3. Links between the carbon and water economies of plants are coupled by combining the biochemical demand for atmospheric CO2 with gas transfer through stomates, liquid water transport in the soil-xylem hydraulic system and sucrose export in the phloem. We formulated a model to predict stomatal conductance (gs), consistent with the maximum energy circulation concept of Lotka and Odum, by maximizing the sucrose flux out of photosynthesizing leaves. The proposed modeling approach recovers all prior results derived from stomatal optimization theories and profit-maximization arguments for the xylem hydraulic system aimed at predicting gs. The novel features of this approach are its ability to 1) predict the price of losing water in carbon units using xylem and phloem properties (i.e., the marginal water use efficiency) and 2) explain why water molecules become more expensive to exchange for CO2 molecules when soil moisture becomes limiting or when plants acclimate to new elevated atmospheric CO2 concentration. On short time-scales (sub-daily), predicted gs under many environmental stimuli were consistent with measurements reported in the literature, including a general sensitivity of gs to vapor pressure deficit and leaf water potential. During progressive droughts, differences in the coordination among the leaf, xylem, and phloem functioning determine the isohydric-to-anisohydric behavior among plants. 
    more » « less
  4. Abstract

    The coordination of traits from individual organs to whole plants is under strong selection because of environmental constraints on resource acquisition and use. However, the tight coordination of traits may provide underlying mechanisms of how locally adapted plant populations can become maladapted because of climate change.

    To better understand local adaptation in intraspecific trait coordination, we studied trait variability in the widely distributed foundation tree species,Populus fremontiiusing a common garden near the mid‐elevational point of this species distribution. We examined 28 traits encompassing four spectra: phenology, leaf economic spectrum (LES), whole‐tree architecture (Corner's Rule) and wood economic spectrum (WES).

    Based on adaptive syndrome theory, we hypothesized that trait expression would be coordinated among and within trait spectra, reflecting local adaptation to either exposure to freeze‐thaw conditions in genotypes sourced from high‐elevation populations or exposure to extreme thermal stress in genotypes sourced from low‐elevation populations.

    High‐elevation genotypes expressed traits within the phenology and WES that limit frost exposure and tissue damage. Specifically, genotypes sourced from high elevations had later mean budburst, earlier mean budset, higher wood densities, higher bark fractions and smaller xylem vessels than their low‐elevation counterparts. Conversely, genotypes sourced from low elevations expressed traits within the LES that prioritized hydraulic efficiency and canopy thermal regulation to cope with extreme heat exposure, including 40% smaller leaf areas, 67% higher stomatal densities and 34% higher mean theoretical maximum stomatal conductance. Low‐elevation genotypes also expressed a lower stomatal control over leaf water potentials that subsequently dropped to pressures that could induce hydraulic failure.

    Synthesis. Our results suggest thatPopulus fremontiiexpresses a high degree of coordination across multiple trait spectra to adapt to local climate constraints on photosynthetic gas exchange, growth and survival. These results, therefore, increase our mechanistic understanding of local adaptation and the potential effects of climate change that in turn, improves our capacity to identify genotypes that are best suited for future restoration efforts.

    more » « less
  5. Abstract Background

    Despite the recognized importance of hydraulic capacitance as a mechanism used by plants to maintain hydraulic functioning during high transpiration, characterizing the dynamics of capacitance remains a challenge.


    We used a novel ‘two-balance method’ to investigate relationships between stem rehydration kinetics and other hydraulic traits in multiple tree species, and we developed a model to explore stem rehydration kinetics further.

    Key Results

    We found that: (1) rehydration time constants and the amount of water uptake occurring during rehydration differed significantly across species; (2) time constants did not change with declining water potential (Ψ), while water uptake increased at lower Ψ in some species; (3) longer time constants were associated with lower wood density, higher capacitance and less negative stem pressures causing 50 % loss of hydraulic conductivity (P50); (4) greater water uptake occurred in stems with lower wood density and less negative P50 values; and (5) the model could estimate the total hydraulic resistance of the rehydration path, which cannot be measured directly.


    Overall, the two-balance method can be used to examine rehydration dynamics quickly and thoroughly in detached woody stems. This method has the potential to improve our understanding of how capacitance functions across tree species, which is an often-overlooked component of whole-plant hydraulics.

    more » « less