Hydraulic stress limits thermal acclimation in trees under chronic drought

Alyssa T. Kullberg; Arianna Milano; Alvaro Poretti; Yike Ma; Patrick Favre; Kate M. Johnson; Giovanni Bortolami; Maxwell Bergström; Thibaut Juillard; Jin Wu; Zhengfei Guo; Jonas Gisler; Marcus Schaub; Charlotte Grossiord

doi:10.1073/pnas.2531865123

journal article Open Access Apr 06, 2026

Hydraulic stress limits thermal acclimation in trees under chronic drought

Alyssa T. Kullberg

Arianna Milano

Alvaro Poretti Yike Ma Patrick Favre

Kate M. Johnson Giovanni Bortolami

Maxwell Bergström Thibaut Juillard

Jin Wu

Zhengfei Guo Jonas Gisler Marcus Schaub

Charlotte Grossiord

Proceedings of the National Academy of Sciences Vol. 123 No. 15 · Proceedings of the National Academy of Sciences

View at Publisher Save 10.1073/pnas.2531865123

Abstract

The capacity of trees to withstand intensifying hot drought events depends on the coordination between hydraulic safety and leaf thermoregulation, yet the limits of this coordination under chronic stress remain poorly understood. Here, we show that 5 y of chronic soil moisture limitation fundamentally constrains the capacity of leaves to maintain adequate thermoregulation. Focusing on two temperate tree species with contrasting water-use strategies, European beech (
Fagus sylvatica
) and downy oak (
Quercus pubescens
), which were subjected to a 5-y manipulation of soil moisture and air temperature, we tested how acclimation influences leaf thermoregulation, hydraulic safety margins (HSMs), thermal safety margins (TSMs), and leaf scorching. Under sustained heating with ample soil water availability, both species acclimated to maintain stable leaf temperature and positive TSMs despite warmer conditions, demonstrating that thermal acclimation is possible without hydraulic stress. By contrast, chronic soil drought narrowed HSMs and weakened evaporative cooling, reducing leaf thermoregulation capacity. When drought and heat co-occurred, stomatal closure triggered a runaway feedback loop: Impaired water transport led to loss of cooling, causing breaching of critical thermal thresholds. These events coincided with failures of photosystem II and scorching in drought-vulnerable beech, linking drought-induced stomatal limitation directly to thermal injury. Our results reveal that oak and beech can acclimate to warming alone, but not to simultaneous heat and drought, which together drive a hydraulic–thermal cascade exceeding both safety margins. This interaction sets fundamental limits on the resilience of temperate forests to future hot droughts.

Topics

No keywords indexed for this article. Browse by subject →

References

53

[1]

A global overview of drought and heat-induced tree mortality reveals emerging climate change risks for forests

Craig D. Allen, Alison K. Macalady, Haroun Chenchouni et al.

Forest Ecology and Management 10.1016/j.foreco.2009.09.001

[2]

10.1111/nph.16485

[3]

10.1111/nph.70661

[4]

10.1007/s11120-013-9874-6

[5]

10.1093/aob/mcaf080

[6]

10.1111/ele.12374

[7]

10.3389/fpls.2019.00103

[8]

10.5194/bg-20-1155-2023

[9]

Mechanisms of woody-plant mortality under rising drought, CO2 and vapour pressure deficit

Nate G. McDowell, Gerard Sapes, Alexandria Pivovaroff et al.

Nature Reviews Earth & Environment 10.1038/s43017-022-00272-1

[10]

T. J. Brodribb, J. Powers, H. Cochard, B. Choat, Hanging by a thread?. Forests and drought. Science 368, 261–266 (2020).

[11]

Global convergence in the vulnerability of forests to drought

Brendan Choat, Steven Jansen, Tim J. Brodribb et al.

Nature 10.1038/nature11688

[12]

10.1104/pp.87.3.577

[13]

10.1104/pp.88.3.574

[14]

10.1146/annurev.pp.31.060180.002423

[15]

10.1071/fp10034

[16]

10.1016/j.tree.2015.09.006

[17]

10.1073/pnas.2205682119

[18]

10.3390/plants13233405

[19]

10.1104/pp.112.198424

[20]

10.1111/nph.15922

[21]

10.1093/treephys/tpac007

[22]

10.1093/treephys/tpac143

[23]

10.1111/nph.12907

[24]

10.1093/treephys/tpr101

[25]

A. T. Kullberg, K. J. Feeley, Limited acclimation of leaf traits and leaf temperatures in a subtropical urban heat island. Tree Physiol. 42, 2266–2281 (2022).

[26]

10.1016/j.ufug.2020.126771

[27]

10.1093/treephys/tpx005

[28]

10.1111/gcb.13477

[29]

10.1111/1365-2435.13658

[30]

10.1111/pce.13133

[31]

10.1111/1365-2435.14657

[32]

10.1016/j.agrformet.2022.108827

[33]

10.1007/978-94-017-7291-4_2

[34]

10.1371/journal.pone.0185481

[35]

10.1111/nph.19358

[36]

10.1111/pce.12141

[37]

10.1073/pnas.2408583121

[38]

10.1016/j.scitotenv.2022.159017

[39]

10.1111/gcb.17439

[40]

10.1016/j.scitotenv.2022.157915

[41]

10.1111/1365-2435.14562

[42]

A first assessment of the impact of the extreme 2018 summer drought on Central European forests

Bernhard Schuldt, Allan Buras, Matthias Arend et al.

Basic and Applied Ecology 10.1016/j.baae.2020.04.003

[43]

10.1111/plb.13467

[44]

A. Kullberg Data from “Hydraulic stress limits thermal acclimation in trees under chronic drought.” EnviDat. https://www.doi.org/10.16904/envidat.720. Deposited 10 November 2025.

[45]

10.1104/pp.15.01450

[46]

10.1073/pnas.0904209106

[47]

10.1104/pp.125.2.935

[48]

10.1111/j.1365-2486.2010.02375.x

[49]

10.1111/nph.70111

[50]

J. Deluigi Data from “Prolonged warming and drought reduce canopy-level net carbon uptake in beech and oak saplings despite photosynthetic and respiratory acclimation.” Dryad. https://doi.org/10.5061/dryad.fxpnvx14f. Deposited 28 March 2025. 10.1111/nph.70111

Showing 50 of 53 references

Metrics

0

Citations

53

References

Details

Published: Apr 06, 2026
Vol/Issue: 123(15)
License: View

Authors

A

Alyssa T. Kullberg

Plant Ecology Research Laboratory, School of Architecture, Civil and Environmental Engineering, École polytechnique fédérale de Lausanne; Forest and Soil Ecology Research Unit, Swiss Federal Institute for Forest, Snow, and Landscape Research

A

Arianna Milano

Plant Ecology Research Laboratory, School of Architecture, Civil and Environmental Engineering, École polytechnique fédérale de Lausanne; Forest and Soil Ecology Research Unit, Swiss Federal Institute for Forest, Snow, and Landscape Research

A

Alvaro Poretti

Plant Ecology Research Laboratory, School of Architecture, Civil and Environmental Engineering, École polytechnique fédérale de Lausanne; Forest and Soil Ecology Research Unit, Swiss Federal Institute for Forest, Snow, and Landscape Research

Y

Yike Ma

Plant Ecology Research Laboratory, School of Architecture, Civil and Environmental Engineering, École polytechnique fédérale de Lausanne

P

Patrick Favre

Plant Ecology Research Laboratory, School of Architecture, Civil and Environmental Engineering, École polytechnique fédérale de Lausanne; Forest and Soil Ecology Research Unit, Swiss Federal Institute for Forest, Snow, and Landscape Research

K

Kate M. Johnson

Centre for Ecological Research and Forestry Applications

G

Giovanni Bortolami

Plant Ecology Research Laboratory, School of Architecture, Civil and Environmental Engineering, École polytechnique fédérale de Lausanne; Forest and Soil Ecology Research Unit, Swiss Federal Institute for Forest, Snow, and Landscape Research

M

Maxwell Bergström

Plant Ecology Research Laboratory, School of Architecture, Civil and Environmental Engineering, École polytechnique fédérale de Lausanne; Forest and Soil Ecology Research Unit, Swiss Federal Institute for Forest, Snow, and Landscape Research

T

Thibaut Juillard

Plant Ecology Research Laboratory, School of Architecture, Civil and Environmental Engineering, École polytechnique fédérale de Lausanne; Forest and Soil Ecology Research Unit, Swiss Federal Institute for Forest, Snow, and Landscape Research

J

Jin Wu

School of Biological Sciences and Institute for Climate and Carbon Neutrality, The University of Hong Kong; State Key Laboratory of Agrobiotechnology, Chinese University of Hong Kong

Z

Zhengfei Guo

School of Biological Sciences and Institute for Climate and Carbon Neutrality, The University of Hong Kong

J

Jonas Gisler

Forest and Soil Ecology Research Unit, Swiss Federal Institute for Forest, Snow, and Landscape Research

M

Marcus Schaub

Forest and Soil Ecology Research Unit, Swiss Federal Institute for Forest, Snow, and Landscape Research

C

Charlotte Grossiord

Plant Ecology Research Laboratory, School of Architecture, Civil and Environmental Engineering, École polytechnique fédérale de Lausanne; Forest and Soil Ecology Research Unit, Swiss Federal Institute for Forest, Snow, and Landscape Research

Funding

Swiss National Science Foundation Award: 310030_204697

EC | Horizon Europe | Excellent Science | HORIZON EUROPE Marie Sklodowska-Curie Actions Award: 101107177

Sandoz Family Foundation Award: NA

Cite This Article

Alyssa T. Kullberg, Arianna Milano, Alvaro Poretti, et al. (2026). Hydraulic stress limits thermal acclimation in trees under chronic drought. Proceedings of the National Academy of Sciences, 123(15). https://doi.org/10.1073/pnas.2531865123

Hydraulic stress limits thermal acclimation in trees under chronic drought

You May Also Like