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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
Current Topics in Ecology

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.

Keywords

Hydraulic conductivity Plant hydraulics Plant water relations Recovery Repair 

Notes

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 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.

Author contributions

The ideas presented here were developed in collaboration by all authors during a workshop held in Jena, Germany. MZ and TK performed the literature review and conceptually organized the manuscript. TLP developed the modelling framework presented in “Modelling hydraulic recovery in vulnerability curves”; code is available upon request. All authors contributed to writing the manuscript.

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Copyright information

© The Ecological Society of Japan 2018

Authors and Affiliations

  • Tamir Klein
    • 1
  • Melanie J. B. Zeppel
    • 2
  • William R. L. Anderegg
    • 3
  • Jasper Bloemen
    • 4
  • Martin G. De Kauwe
    • 5
  • Patrick Hudson
    • 6
  • Nadine K. Ruehr
    • 7
  • Thomas L. Powell
    • 8
    • 9
  • Georg von Arx
    • 10
  • Andrea Nardini
    • 11
  1. 1.Department of Plant and Environmental SciencesWeizmann Institute of ScienceRehovotIsrael
  2. 2.GenIMPACT National Centre for Genomic Medicine, Faculty of Business and EconomicsMacquarie UniversitySydneyAustralia
  3. 3.Department of BiologyUniversity of UtahSalt Lake CityUSA
  4. 4.Institute of EcologyUniversity of InnsbruckInnsbruckAustria
  5. 5.ARC Centre of Excellence for Climate ExtremesUniversity of New South WalesSydneyAustralia
  6. 6.Department of BiologyUniversity of New MexicoAlbuquerqueUSA
  7. 7.Karlsruhe Institute of Technology (KIT)Institute of Meteorology and Climate Research-Atmospheric Environmental Research (IMK-IFU)Garmisch-PartenkirchenGermany
  8. 8.Department of Organismic and Evolutionary BiologyHarvard UniversityCambridgeUSA
  9. 9.Earth and Environmental Sciences AreaLawrence Berkeley National LaboratoryBerkeleyUSA
  10. 10.Swiss Federal Institute for Forest, Snow and Landscape Research WSLBirmensdorfSwitzerland
  11. 11.Dipartimento di Scienze della VitaUniversità di TriesteTriesteItaly

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