Distinct xylem responses to acute vs prolonged drought in pine trees

Marceau Guérin; Georg von Arx; Dario Martin-Benito; Laia Andreu-Hayles; Kevin L Griffin; Nate G McDowell; William Pockman; Pierre Gentine

doi:10.1093/treephys/tpz144

Distinct xylem responses to acute vs prolonged drought in pine trees

Tree Physiol. 2020 May 11;40(5):605-620. doi: 10.1093/treephys/tpz144.

Authors

Marceau Guérin¹, Georg von Arx², Dario Martin-Benito^{3

4}, Laia Andreu-Hayles⁵, Kevin L Griffin⁶, Nate G McDowell⁷, William Pockman⁸, Pierre Gentine^{1

9}

Affiliations

¹ Department of Earth and Environmental Engineering, Columbia University, New York, NY 10027, USA.
² Forest Dynamics Research Unit, Swiss Federal Institute for Forest, Snow and Landscape Research WSL, Zürcherstrasse 111 CH-8903 Birmensdorf, Switzerland.
³ INIA, CIFOR, Ctra La Coruña km 7.5, 28040 Madrid, Spain.
⁴ Forest Ecology, Department of Environmental Sciences, Swiss Federal Institute of Technology, ETH Zurich, Universitätstrasse 16, 8092 Zürich, Switzerland.
⁵ Tree-Ring Laboratory, Lamont-Doherty Earth Observatory of Columbia University, 61 Route 9 W, Palisades, NY 10964, USA.
⁶ Department of Earth and Environmental Sciences, Lamont-Doherty Earth Observatory of Columbia University, Palisades, NY 10964, USA.
⁷ Pacific Northwest National Laboratory, 902 Battelle Boulevard, Richland, WA 99354, USA.
⁸ Biology Department, MSC03 202, University of New Mexico, Albuquerque, NM 87131, USA.
⁹ Earth Institute, Columbia University, Hogan Hall, 2910 Broadway, New York, NY 10027, USA.

PMID: 31976523
DOI: 10.1093/treephys/tpz144

Abstract

Increasing dryness challenges trees' ability to maintain water transport to the leaves. Most plant hydraulics models use a static xylem response to water stress. Yet, in reality, lower soil moisture and warmer temperatures during growing seasons feed back onto xylem development. In turn, adjustments to water stress in the newly built xylem influence future physiological responses to droughts. In this study, we investigate the annual variation of anatomical traits in branch xylem in response to different soil and atmospheric moisture conditions and tree stress levels, as indicated by seasonal predawn leaf water potential (ΨL,pd). We used a 6-year field experiment in southwestern USA with three soil water treatments applied to Pinus edulis Engelm trees-ambient, drought (45% rain reduction) and irrigation (15-35% annual water addition). All trees were also subject to a natural 1-year acute drought (soil and atmospheric) that occurred during the experiment. The irrigated trees showed only moderate changes in anatomy-derived hydraulic traits compared with the ambient trees, suggesting a generally stable, well-balanced xylem structure under unstressed conditions. The artificial prolonged soil drought increased hydraulic efficiency but lowered xylem construction costs and decreased tracheid implosion safety ((t/b)2), suggesting that annual adjustments of xylem structure follow a safety-efficiency trade-off. The acute drought plunged hydraulic efficiency across all treatments. The combination of acute and prolonged drought resulted in vulnerable and inefficient new xylem, disrupting the stability of the anatomical trade-off observed in the rest of the years. The xylem hydraulic traits showed no consistent direct link to ΨL,pd. In the future, changes in seasonality of soil and atmospheric moisture are likely to have a critical impact on the ability of P. edulis to acclimate its xylem to warmer climate. Furthermore, the increasing frequency of acute droughts might reduce hydraulic resilience of P. edulis by repeatedly creating vulnerable and less efficient anatomical structure.

Keywords: carbon costs; hydraulic efficiency; hydraulic safety; tracheid; trade-off; water transport; wood anatomy.

Publication types

Research Support, Non-U.S. Gov't
Research Support, U.S. Gov't, Non-P.H.S.

MeSH terms

Droughts*
Pinus*
Rain
Trees
Water
Xylem

Substances

Water