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Title: A test of the hydraulic vulnerability segmentation hypothesis in angiosperm and conifer tree species

Abstract

Water transport from soils to the atmosphere is critical for plant growth and survival. However, we have a limited understanding about many portions of the whole-tree hydraulic pathway, because the vast majority of published information is on terminal branches. Our understanding of mature tree trunk hydraulic physiology, in particular, is limited. The hydraulic vulnerability segmentation hypothesis (HVSH) stipulates that distal portions of the plant (leaves, branches and roots) should be more vulnerable to embolism than trunks, which are non-redundant organs that require a massive carbon investment. In the current study, we compared vulnerability to loss of hydraulic function, leaf and xylem water potentials and the resulting hydraulic safety margins (in relation to the water potential causing 50% loss of hydraulic conductivity) in leaves, branches, trunks and roots of four angiosperms and four conifer tree species. Across all species, our results supported strongly the HVSH as leaves and roots were less resistant to embolism than branches or trunks. However, branches were consistently more resistant to embolism than any other portion of the plant, including trunks. Also, calculated whole-tree vulnerability to hydraulic dysfunction was much greater than vulnerability in branches. This was due to hydraulic dysfunction in roots and leaves at lessmore » negative water potentials than those causing branch or trunk dysfunction. Leaves and roots had narrow or negative hydraulic safety margins, but trunks and branches maintained positive safety margins. By using branch-based hydraulic information as a proxy for entire plants, much research has potentially overestimated embolism resistance, and possibly drought tolerance, for many species. This study highlights the necessity to reconsider past conclusions made about plant resistance to drought based on branch xylem only. As a result, this study also highlights the necessity for more research of whole-plant hydraulic physiology to better understand strategies of plant drought tolerance and the critical control points within the hydraulic pathway.« less

Authors:
 [1];  [2];  [3];  [4];  [5];  [6];  [2];  [7]
  1. Univ. of Idaho, Moscow, ID (United States)
  2. Duke Univ., Durham, NC (United States)
  3. Univ. of Wisconsin, Madison, WI (United States)
  4. Bordeaux Sciences Agro, UMR INRA-ISPA 1391, Gradignan (France)
  5. North Carolina State Univ., Raleigh, NC (United States)
  6. Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States)
  7. Duke Univ., Durham, NC (United States); Bordeaux Sciences Agro, UMR INRA-ISPA 1391, Gradignan (France)
Publication Date:
Research Org.:
Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States)
Sponsoring Org.:
USDOE Office of Science (SC)
OSTI Identifier:
1325499
Grant/Contract Number:  
AC05-00OR22725
Resource Type:
Accepted Manuscript
Journal Name:
Tree Physiology
Additional Journal Information:
Journal Volume: 36; Journal Issue: 8; Journal ID: ISSN 0829-318X
Publisher:
Oxford University Press
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; cavitation; drought; embolism; transpiration; water relations

Citation Formats

Johnson, Daniel M., Wortemann, Remi, McCulloh, Katherine A., Jordan-Meille, Lionel, Ward, Eric, Warren, Jeffrey M., Palmroth, Sari, and Domec, Jean -Christophe. A test of the hydraulic vulnerability segmentation hypothesis in angiosperm and conifer tree species. United States: N. p., 2016. Web. doi:10.1093/treephys/tpw031.
Johnson, Daniel M., Wortemann, Remi, McCulloh, Katherine A., Jordan-Meille, Lionel, Ward, Eric, Warren, Jeffrey M., Palmroth, Sari, & Domec, Jean -Christophe. A test of the hydraulic vulnerability segmentation hypothesis in angiosperm and conifer tree species. United States. doi:10.1093/treephys/tpw031.
Johnson, Daniel M., Wortemann, Remi, McCulloh, Katherine A., Jordan-Meille, Lionel, Ward, Eric, Warren, Jeffrey M., Palmroth, Sari, and Domec, Jean -Christophe. Wed . "A test of the hydraulic vulnerability segmentation hypothesis in angiosperm and conifer tree species". United States. doi:10.1093/treephys/tpw031. https://www.osti.gov/servlets/purl/1325499.
@article{osti_1325499,
title = {A test of the hydraulic vulnerability segmentation hypothesis in angiosperm and conifer tree species},
author = {Johnson, Daniel M. and Wortemann, Remi and McCulloh, Katherine A. and Jordan-Meille, Lionel and Ward, Eric and Warren, Jeffrey M. and Palmroth, Sari and Domec, Jean -Christophe},
abstractNote = {Water transport from soils to the atmosphere is critical for plant growth and survival. However, we have a limited understanding about many portions of the whole-tree hydraulic pathway, because the vast majority of published information is on terminal branches. Our understanding of mature tree trunk hydraulic physiology, in particular, is limited. The hydraulic vulnerability segmentation hypothesis (HVSH) stipulates that distal portions of the plant (leaves, branches and roots) should be more vulnerable to embolism than trunks, which are non-redundant organs that require a massive carbon investment. In the current study, we compared vulnerability to loss of hydraulic function, leaf and xylem water potentials and the resulting hydraulic safety margins (in relation to the water potential causing 50% loss of hydraulic conductivity) in leaves, branches, trunks and roots of four angiosperms and four conifer tree species. Across all species, our results supported strongly the HVSH as leaves and roots were less resistant to embolism than branches or trunks. However, branches were consistently more resistant to embolism than any other portion of the plant, including trunks. Also, calculated whole-tree vulnerability to hydraulic dysfunction was much greater than vulnerability in branches. This was due to hydraulic dysfunction in roots and leaves at less negative water potentials than those causing branch or trunk dysfunction. Leaves and roots had narrow or negative hydraulic safety margins, but trunks and branches maintained positive safety margins. By using branch-based hydraulic information as a proxy for entire plants, much research has potentially overestimated embolism resistance, and possibly drought tolerance, for many species. This study highlights the necessity to reconsider past conclusions made about plant resistance to drought based on branch xylem only. As a result, this study also highlights the necessity for more research of whole-plant hydraulic physiology to better understand strategies of plant drought tolerance and the critical control points within the hydraulic pathway.},
doi = {10.1093/treephys/tpw031},
journal = {Tree Physiology},
number = 8,
volume = 36,
place = {United States},
year = {2016},
month = {5}
}

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    Works referencing / citing this record:

    Leaf hydraulic parameters are more plastic in species that experience a wider range of leaf water potentials
    journal, February 2018

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    Acclimation of branch and leaf hydraulics in adult Fagus sylvatica and Picea abies in a forest through-fall exclusion experiment
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