Title: The xylem of anisohydric Quercus alba L. is more vulnerable to embolism than isohydric codominants
Abstract
The coordination of plant leaf water potential (ΨL) regulation and xylem vulnerability to embolism is fundamental for understanding the tradeoffs between carbon uptake and risk of hydraulic damage. There is a general consensus that trees with vulnerable xylem more conservatively regulate ΨLthan plants with resistant xylem. We evaluated if this paradigm applied to three important eastern US temperate tree species,Quercus albaL.,Acer saccharumMarsh. andLiriodendron tulipiferaL., by synthesizing 1600 ΨLobservations, 122 xylem embolism curves and xylem anatomical measurements across 10 forests spanning pronounced hydroclimatological gradients and ages. We found that, unexpectedly, the species with the most vulnerable xylem (Q. alba) regulated ΨLless strictly than the other species. This relationship was found across all sites, such that coordination among traits was largely unaffected by climate and stand age.Quercusspecies are perceived to be among the most drought tolerant temperate US forest species; however, our results suggest their relatively loose ΨLregulation in response to hydrologic stress occurs with a substantial hydraulic cost that may expose them to novel risks in a more drought‐prone future.
Miller, Megan L.; Roddy, Adam B.; Brodersen, Craig R.; McElrone, Andrew J.; Johnson, Daniel M.(
, American Journal of Botany)
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.
Drought events may increase the likelihood that the plant water transport system becomes interrupted by embolism. Yet our knowledge about the temporal frequency of xylem embolism in the field is frequently lacking, as it requires detailed, long‐term measurements.
We measured xylem embolism resistance and midday xylem water potentials during the consecutive summers of 2019 and 2020 to estimate maximum levels of embolism in leaf and stem xylem of ten temperate angiosperm tree species. We also studied vessel and pit membrane characteristics based on light and electron microscopy to corroborate potential differences in embolism resistance between leaves and stems.
Apart fromA.pseudoplatanusandQ.petraea, eight species experienced minimum xylem water potentials that were close to or below those required to initiate embolism. Water potentials corresponding to ca. 12% loss of hydraulic conductivity (PLC) could occur in six species, while considerable levels of embolism around 50% PLC were limited toB.pendulaandC.avellana. There was a general agreement in embolism resistance between stems and leaves, with leaves being equally or more resistant than stems. Also, xylem embolism resistance was significantly correlated to intervessel pit membrane thickness (TPM) for stems, but not to vessel diameter and total intervessel pit membrane surface area of a vessel.
Our data indicate that low amounts of embolism occur in most species during moderate summer drought, and that considerable levels of embolism are uncommon. Moreover, our experimental andTPMdata show that leaf xylem is generally no more vulnerable than stem xylem.
Smith‐Martin, Chris M.; Muscarella, Robert; Ankori‐Karlinsky, Roi; Delzon, Sylvain; Farrar, Samuel L.; Salva‐Sauri, Melissa; Thompson, Jill; Zimmerman, Jess K.; Uriarte, María(
, Functional Ecology)
Abstract
Severe droughts have led to lower plant growth and high mortality in many ecosystems worldwide, including tropical forests. Drought vulnerability differs among species, but there is limited consensus on the nature and degree of this variation in tropical forest communities. Understanding species‐level vulnerability to drought requires examination of hydraulic traits since these reflect the different strategies species employ for surviving drought.
Here, we examined hydraulic traits and growth reductions during a severe drought for 12 common woody species in a wet tropical forest community in Puerto Rico to ask: Q1. To what extent can hydraulic traits predict growth declines during drought? We expected that species with more hydraulically vulnerable xylem and narrower safety margins (SMP50) would grow less during drought. Q2. How does species successional association relate to the levels of vulnerability to drought and hydraulic strategies? We predicted that early‐ and mid‐successional species would exhibit more acquisitive strategies, making them more susceptible to drought than shade‐tolerant species. Q3. What are the different hydraulic strategies employed by species and are there trade‐offs between drought avoidance and drought tolerance? We anticipated that species with greater water storage capacity would have leaves that lose turgor at higher xylem water potential and be less resistant to embolism forming in their xylem (P50).
We found a large range of variation in hydraulic traits across species; however, they did not closely capture the magnitude of growth declines during drought. Among larger trees (≥10 cm diameter at breast height—DBH), some tree species with high xylem embolism vulnerability (P50) and risk of hydraulic failure (SMP50) experienced substantial growth declines during drought, but this pattern was not consistent across species. We found a trade‐off among species between drought avoidance (capacitance) and drought tolerating (P50) in this tropical forest community. Hydraulic strategies did not align with successional associations. Instead, some of the more drought‐vulnerable species were shade‐tolerant dominants in the community, suggesting that a drying climate could lead to shifts in long‐term forest composition and function in Puerto Rico and the Caribbean.
Read the freePlain Language Summaryfor this article on the Journal blog.
Rodríguez‐Gamir, Juan; Xue, Jianming; Clearwater, Michael J.; Meason, Dean F.; Clinton, Peter W.; Domec, Jean‐Christophe(
, Plant, Cell & Environment)
Abstract
Stomatal regulation is crucial for forest species performance and survival on drought‐prone sites. We investigated the regulation of root and shoot hydraulics in threePinus radiataclones 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 inKroot‐rcaused a decrease in leaf‐specific whole‐plant hydraulic conductance (Kplant‐l). Among clones, the larger the decrease inKplant‐l, the more stomata closed in response to drought. Rewatering resulted in a quick recovery ofKroot‐randgs. Our results demonstrated that the reduction inKplant‐l, attributed to a down regulation of aquaporin activity in roots, was linked to the isohydric stomatal behaviour, resulting in a nearly constant Ψleafas water stress started. We concluded that higherKplant‐lis associated with water stress resistance by sustaining a less negative Ψleafand delaying stomatal closure.
Pivovaroff, Alexandria L.; Cook, Victoria M. W.; Santiago, Louis S.(
, Plant, Cell & Environment)
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.
Benson, Michael C., Miniat, Chelcy F., Oishi, Andrew C., Denham, Sander O., Domec, Jean‐Christophe, Johnson, Daniel M., Missik, Justine E., Phillips, Richard P., Wood, Jeffrey D., and Novick, Kimberly A. The xylem of anisohydric Quercus alba L. is more vulnerable to embolism than isohydric codominants. Plant, Cell & Environment 45.2 Web. doi:10.1111/pce.14244.
Benson, Michael C., Miniat, Chelcy F., Oishi, Andrew C., Denham, Sander O., Domec, Jean‐Christophe, Johnson, Daniel M., Missik, Justine E., Phillips, Richard P., Wood, Jeffrey D., & Novick, Kimberly A. The xylem of anisohydric Quercus alba L. is more vulnerable to embolism than isohydric codominants. Plant, Cell & Environment, 45 (2). https://doi.org/10.1111/pce.14244
Benson, Michael C., Miniat, Chelcy F., Oishi, Andrew C., Denham, Sander O., Domec, Jean‐Christophe, Johnson, Daniel M., Missik, Justine E., Phillips, Richard P., Wood, Jeffrey D., and Novick, Kimberly A.
"The xylem of anisohydric Quercus alba L. is more vulnerable to embolism than isohydric codominants". Plant, Cell & Environment 45 (2). Country unknown/Code not available: Wiley-Blackwell. https://doi.org/10.1111/pce.14244.https://par.nsf.gov/biblio/10361760.
@article{osti_10361760,
place = {Country unknown/Code not available},
title = {The xylem of anisohydric Quercus alba L. is more vulnerable to embolism than isohydric codominants},
url = {https://par.nsf.gov/biblio/10361760},
DOI = {10.1111/pce.14244},
abstractNote = {Abstract The coordination of plant leaf water potential (ΨL) regulation and xylem vulnerability to embolism is fundamental for understanding the tradeoffs between carbon uptake and risk of hydraulic damage. There is a general consensus that trees with vulnerable xylem more conservatively regulate ΨLthan plants with resistant xylem. We evaluated if this paradigm applied to three important eastern US temperate tree species,Quercus albaL.,Acer saccharumMarsh. andLiriodendron tulipiferaL., by synthesizing 1600 ΨLobservations, 122 xylem embolism curves and xylem anatomical measurements across 10 forests spanning pronounced hydroclimatological gradients and ages. We found that, unexpectedly, the species with the most vulnerable xylem (Q. alba) regulated ΨLless strictly than the other species. This relationship was found across all sites, such that coordination among traits was largely unaffected by climate and stand age.Quercusspecies are perceived to be among the most drought tolerant temperate US forest species; however, our results suggest their relatively loose ΨLregulation in response to hydrologic stress occurs with a substantial hydraulic cost that may expose them to novel risks in a more drought‐prone future.},
journal = {Plant, Cell & Environment},
volume = {45},
number = {2},
publisher = {Wiley-Blackwell},
author = {Benson, Michael C. and Miniat, Chelcy F. and Oishi, Andrew C. and Denham, Sander O. and Domec, Jean‐Christophe and Johnson, Daniel M. and Missik, Justine E. and Phillips, Richard P. and Wood, Jeffrey D. and Novick, Kimberly A.},
}
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