skip to main content


Title: The dynamic multi‐functionality of leaf water transport outside the xylem
Summary

A surge of papers have reported low leaf vulnerability to xylem embolism during drought. Here, we focus on the less studied, and more sensitive, outside‐xylem leaf hydraulic responses to multiple internal and external conditions. Studies of 34 species have resolved substantial vulnerability to dehydration of the outside‐xylem pathways, and studies of leaf hydraulic responses to light also implicate dynamic outside‐xylem responses. Detailed experiments suggest these dynamic responses arise at least in part from strong control of radial water movement across the vein bundle sheath. While leaf xylem vulnerability may influence leaf and plant survival during extreme drought, outside‐xylem dynamic responses are important for the control and resilience of water transport and leaf water status for gas exchange and growth.

 
more » « less
Award ID(s):
2017949
NSF-PAR ID:
10427698
Author(s) / Creator(s):
 ;  ;  ;  
Publisher / Repository:
Wiley-Blackwell
Date Published:
Journal Name:
New Phytologist
Volume:
239
Issue:
6
ISSN:
0028-646X
Page Range / eLocation ID:
p. 2099-2107
Format(s):
Medium: X
Sponsoring Org:
National Science Foundation
More Like this
  1. Abstract

    Recent findings suggest that tree mortality and post‐drought recovery of gas exchange can be predicted from loss of function within the water transport system. Understanding the susceptibility of plants to hydraulic damage requires knowledge about the vulnerability of different plant organs to stress‐induced hydraulic dysfunction. This is particularly important in the context of vulnerability segmentation between plant tissues which is believed to protect more energetically ‘costly’ tissues, such as woody stems, by sacrificing ‘cheaper’ leaves early under drought conditions.

    Differences in vulnerability segmentation between co‐occurring plant species could explain divergent behaviours during drought, yet there are few studies considering how this characteristic may vary within a plant community. Here we investigated community‐wide vulnerability segmentation by comparing leaf/shoot and stem vulnerability in all coexistent dominant canopy and understory woody species in a diverse dry sclerophyll woodland community, including multiple angiosperms and one gymnosperm.

    Previously published terminal leaf/shoot vulnerability to loss of water transport capacity was compared with stem xylem vulnerability to embolism measured on the same species at the same site. We calculated hydraulic safety margins for stems to determine variation in the risk of hydraulic failure during drought among species.

    The xylem of all species was found to be highly resistant to hydraulic dysfunction, with only two of the eight species exhibiting significantly different vulnerability to the overall mean. No evidence of vulnerability segmentation between shoots/leaves and stems was found in seven of the eight species.

    Phylogenetically diverse canopy and understory species in this evergreen sclerophyll woodland appear to have evolved similar strategies of drought resistance, including low xylem vulnerability to embolism and general lack of vulnerability segmentation. This convergence in hydraulic safety indicates a lack of hydraulic niche partitioning in this woodland community.

    A freeplain language summarycan be found within the Supporting Information of this article.

     
    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. Lawson, Tracy (Ed.)
    Abstract Drought decreases water transport capacity of leaves and limits gas exchange, which involves reduced leaf leaf hydraulic conductance (Kleaf) in both the xylem and outside-xylem pathways. Some literature suggests that grapevines are hyper-susceptible to drought-induced xylem embolism. We combined Kleaf and gas exchange measurements, micro-computed tomography of intact leaves, and spatially explicit modeling of the outside-xylem pathways to evaluate the role of vein embolism and Kleaf in the responses of two different grapevine cultivars to drought. Cabernet Sauvignon and Chardonnay exhibited similar vulnerabilities of Kleaf and gs to dehydration, decreasing substantially prior to leaf xylem embolism. Kleaf and gs decreased by 80% for both cultivars by Ψ leaf approximately –0.7 MPa and –1.2 MPa, respectively, while leaf xylem embolism initiated around Ψ leaf = –1.25 MPa in the midribs and little to no embolism was detected in minor veins even under severe dehydration for both cultivars. Modeling results indicated that reduced membrane permeability associated with a Casparian-like band in the leaf vein bundle sheath would explain declines in Kleaf of both cultivars. We conclude that during moderate water stress, changes in the outside-xylem pathways, rather than xylem embolism, are responsible for reduced Kleaf and gs. Understanding this mechanism could help to ensure adequate carbon capture and crop performance under drought. 
    more » « less
  4. Premise

    Because of its broad range in the neotropical rainforest and within tree canopies, the tank bromeliadGuzmania monostachiawas investigated as a model of how varying leaf hydraulic conductance (Kleaf) could help plants resist and recover from episodic drought. The two pathways ofKleaf, inside and outside the xylem, were also examined to determine the sites and causes of major hydraulic resistances within the leaf.

    Methods

    We measured leaf hydraulic conductance for plants in the field and laboratory under wet, dry, and rewetted conditions and applied physiological, anatomical, and gene expression analysis with modeling to investigate changes inKleaf.

    Results

    After 7 d with no rain in the field or 14 days with no water in the glasshouse,Kleafdecreased by 50% yet increased to hydrated values within 4 d of tank refilling. Staining to detect embolism combined with modeling indicated that changes outside the xylem were of greater importance toKleafthan were changes inside the xylem and were associated with changes in intercellular air spaces (aerenchyma), aquaporin expression and inhibition, and cuticular conductance.

    Conclusions

    Low values for all conductances during drying, particularly in pathways outside the xylem, lead to hydraulic resilience for this species and may also contribute to its broad environmental tolerances.

     
    more » « less
  5. Premise

    The young seedling life stage is critical for reforestation after disturbance and for species migration under climate change, yet little is known regarding their basic hydraulic function or vulnerability to drought. Here, we sought to characterize responses to desiccation including hydraulic vulnerability, xylem anatomical traits, and impacts on other stem tissues that contribute to hydraulic functioning.

    Methods

    Larix occidentalis,Pseudotsuga menziesii, andPinus ponderosa(all ≤6 weeks old) were imaged using x‐ray computed microtomography during desiccation to assess seedling biomechanical responses with concurrently measured hydraulic conductivity (ks) and water potential (Ψ) to assess vulnerability to xylem embolism formation and other tissue damage.

    Results

    In non‐stressed samples for all species, pith and cortical cells appeared circular and well hydrated, but they started to empty and deform with decreasingΨwhich resulted in cell tearing and eventual collapse. Despite the severity of this structural damage, the vascular cambium remained well hydrated even under the most severe drought. There were significant differences among species in vulnerability to xylem embolism formation, with 78% xylem embolism inL. occidentalisbyΨof −2.1 MPa, but only 47.7% and 62.1% inP. ponderosaandP. menziesiiat −4.27 and −6.73 MPa, respectively.

    Conclusions

    Larix occidentalisseedlings appeared to be more susceptible to secondary xylem embolism compared to the other two species, but all three maintained hydration of the vascular cambium under severe stress, which could facilitate hydraulic recovery by regrowth of xylem when stress is relieved.

     
    more » « less