Xylem embolism refilling and resilience against drought-induced mortality in woody plants: processes and trade-offs

Tamir Klein*, Melanie J.B. Zeppel, William R.L. Anderegg, Jasper Bloemen, Martin G. De Kauwe, Patrick Hudson, Nadine K. Ruehr, Thomas L. Powell, Georg von Arx, Andrea Nardini

*Corresponding author for this work

Research output: Contribution to journalArticle (Academic Journal)peer-review

52 Citations (Scopus)

Abstract

Understanding which species are able to recover from drought, under what conditions, and the mechanistic processes involved, will facilitate predictions of plant mortality in response to global change. In response to drought, some species die because of embolism-induced hydraulic failure, whilst others are able to avoid mortality and recover, following rehydration. Several tree species have evolved strategies to avoid embolism, whereas others tolerate high embolism rates but can recover their hydraulic functioning upon drought relief. Here, we focus on structures and processes that might allow some plants to recover from drought stress via embolism reversal. We provide insights into how embolism repair may have evolved, anatomical and physiological features that facilitate this process, and describe possible trade-offs and related costs. Recent controversies on methods used for estimating embolism formation/repair are also discussed, providing some methodological suggestions. Although controversial, embolism repair processes are apparently based on the activity of phloem and ray/axial parenchyma. The mechanism is energetically demanding, and the costs to plants include metabolism and transport of soluble sugars, water and inorganic ions. We propose that embolism repair should be considered as a possible component of a ‘hydraulic efficiency-safety’ spectrum. We also advance a framework for vegetation models, describing how vulnerability curves may change in hydrodynamic model formulations for plants that recover from embolism.

Original languageEnglish
Pages (from-to)839-855
Number of pages17
JournalEcological Research
Volume33
Issue number5
DOIs
Publication statusPublished - 1 Sep 2018

Bibliographical note

Funding Information:
Acknowledgements The paper was inspired by an International Interdisciplinary Workshop on Tree Mortality at the Max-Planck for Biogeochemsitry in Jena, Germany (October 2014). Two anonymous reviewers have helped improving the text by providing insightful comments. Funding support was provided in full or in part as follows: MZ by ARC DECRA DE120100518. TK by the Benoziyo Fund for the Advancement of Science; Mr. and Mrs. Norman Reiser, together with the Weizmann Center for New Sci- entists; and the Edith and Nathan Goldberg Career Development Chair. WRLA by a NOAA Climate and Global Change Postdoctoral fellowship, administered by the University Corporation of Atmospheric Research. JB by the Austrian Science Fund (FWF): M1757-B22 through the Lise Meitner Program. PJH by the University of New Mexico. NKR by the German Federal Ministry of Education and Research (BMBF), through the Helmholtz Association and its research programme ATMO and by the German Research Foundation through its Emmy Noether Programme (RU 1657/2-1). TLP by student research funding from the OEB department at Harvard University and by the Office of Biological and Environmental Research, US Department of Energy, NGEE-Tropics project. GvA by the Swiss State Secretariat for Education, Research and Innovation SERI (SBFI C14.0104 and C12.0100). The authors declare no conflict of interest. W.R.L.A. acknowledges funding from NSF 1714972 and from the USDA National Institute of Food and Agriculture, Agricultural and Food Research Initiative Competitive Programme, Ecosystem Services and Agro-ecosystem Management, grant no. 2017-05521.

Funding Information:
The paper was inspired by an International Interdisciplinary Workshop on Tree Mortality at the Max-Planck for Biogeochemsitry in Jena, Germany (October 2014). Two anonymous reviewers have helped improving the text by providing insightful comments. Funding support was provided in full or in part as follows: MZ by ARC DECRA DE120100518. TK by the Benoziyo Fund for the Advancement of Science; Mr. and Mrs. Norman Reiser, together with the Weizmann Center for New Scientists; and the Edith and Nathan Goldberg Career Development Chair. WRLA by a NOAA Climate and Global Change Postdoctoral fellowship, administered by the University Corporation of Atmospheric Research. JB by the Austrian Science Fund (FWF): M1757-B22 through the Lise Meitner Program. PJH by the University of New Mexico. NKR by the German Federal Ministry of Education and Research (BMBF), through the Helmholtz Association and its research programme ATMO and by the German Research Foundation through its Emmy Noether Programme (RU 1657/2-1). TLP by student research funding from the OEB department at Harvard University and by the Office of Biological and Environmental Research, US Department of Energy, NGEE-Tropics project. GvA by the Swiss State Secretariat for Education, Research and Innovation SERI (SBFI C14.0104 and C12.0100). The authors declare no conflict of interest. W.R.L.A. acknowledges funding from NSF 1714972 and from the USDA National Institute of Food and Agriculture, Agricultural and Food Research Initiative Competitive Programme, Ecosystem Services and Agro-ecosystem Management, grant no. 2017-05521.

Publisher Copyright:
© 2018, The Ecological Society of Japan.

Keywords

  • Hydraulic conductivity
  • Plant hydraulics
  • Plant water relations
  • Recovery
  • Repair

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