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

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

doi:10.1007/s11284-018-1588-y

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

Journal Article · Sat Mar 10 00:00:00 EST 2018 · Ecological Research

DOI:https://doi.org/10.1007/s11284-018-1588-y· OSTI ID:1532338

^[1]; Zeppel, Melanie J. B. ^[2]; Anderegg, William R. L. ^[3]; Bloemen, Jasper ^[4]; De Kauwe, Martin G. ^[5]; Hudson, Patrick ^[6]; Ruehr, Nadine K. ^[7]; Powell, Thomas L. ^[8]; von Arx, Georg ^[9]; Nardini, Andrea ^[10]

Weizmann Inst. of Science, Rehovot (Israel)
Macquarie Univ., NSW (Australia)
Univ. of Utah, Salt Lake City, UT (United States)
Univ. of Innsbruck, Innsbruck (Austria)
Univ. of New South Wales, Sydney, NSW (Australia)
Univ. of New Mexico, Albuquerque, NM (United States)
Karlsruhe Inst. of Technology (KIT), Inst. of Meteorology and Climate Research-Atmospheric Environmental Research, Garmisch-Partenkirchen (Germany)
Harvard Univ., Cambridge, MA (United States)
Swiss Federal Inst. for Forest, Snow and Landscape Research WSL, Birmensdorf (Switzerland)
Univ. di Trieste, Trieste (Italy)

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.

View Accepted Manuscript (DOE)

Research Organization:: Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)

Sponsoring Organization:: USDOE Office of Science (SC)

Grant/Contract Number:: AC02-05CH11231

OSTI ID:: 1532338

Journal Information:: Ecological Research, Journal Name: Ecological Research Journal Issue: 5 Vol. 33; ISSN 0912-3814

Country of Publication:: United States

Language:: English

References (105)

Gene expression in vessel-associated cells upon xylem embolism repair in Vitis vinifera L. petioles Chitarra, Walter; Balestrini, Raffaella; Vitali, Marco Planta, Vol. 239, Issue 4 https://doi.org/10.1007/s00425-013-2017-7	journal	January 2014
Trends in wood density and structure are linked to prevention of xylem implosion by negative pressure Hacke, Uwe G.; Sperry, John S.; Pockman, William T. Oecologia, Vol. 126, Issue 4 https://doi.org/10.1007/s004420100628	journal	February 2001
How important is woody tissue photosynthesis in poplar during drought stress? Bloemen, Jasper; Vergeynst, Lidewei L.; Overlaet-Michiels, Lander Trees, Vol. 30, Issue 1 https://doi.org/10.1007/s00468-014-1132-9	journal	December 2014
Variability of ray anatomy of Larix gmelinii along a forest productivity gradient in Siberia Fonti, Patrick; Tabakova, Maria A.; Kirdyanov, Alexander V. Trees, Vol. 29, Issue 4 https://doi.org/10.1007/s00468-015-1197-0	journal	April 2015
Freezing xylem conduits with liquid nitrogen creates artifactual embolisms in water-stressed broadleaf trees Umebayashi, Toshihiro; Ogasa, Mayumi Y.; Miki, Naoko H. Trees, Vol. 30, Issue 1 https://doi.org/10.1007/s00468-015-1302-4	journal	October 2015
Branch sacrifice: cavitation-associated drought adaptation of riparian cottonwoods Rood, S. B.; Patiño, S.; Coombs, K. Trees, Vol. 14, Issue 5 https://doi.org/10.1007/s004680050010	journal	March 2000
Do roots mind the gap? Carminati, A.; Vetterlein, D.; Koebernick, N. Plant and Soil, Vol. 367, Issue 1-2 https://doi.org/10.1007/s11104-012-1496-9	journal	October 2012
Contrasting hydraulic strategies in Salix psammophila and Caragana korshinskii in the southern Mu Us Desert, China Li, Yangyang; Chen, Weiyue; Chen, Jiacun Ecological Research, Vol. 31, Issue 6 https://doi.org/10.1007/s11284-016-1396-1	journal	October 2016
Hydraulic failure and repair are not routine in trees Cochard, Hervé; Delzon, Sylvain Annals of Forest Science, Vol. 70, Issue 7 https://doi.org/10.1007/s13595-013-0317-5	journal	August 2013
Factors determining relations between stand age and catchment water balance in mountain ash forests Vertessy, Robert A.; Watson, Fred G. R.; O′Sullivan, Sharon K. Forest Ecology and Management, Vol. 143, Issue 1-3 https://doi.org/10.1016/S0378-1127(00)00501-6	journal	April 2001
The challenge of the Mediterranean climate to plant hydraulics: Responses and adaptations Nardini, Andrea; Lo Gullo, Maria A.; Trifilò, Patrizia Environmental and Experimental Botany, Vol. 103 https://doi.org/10.1016/j.envexpbot.2013.09.018	journal	July 2014
Relationships between stomatal regulation, water-use, and water-use efficiency of two coexisting key Mediterranean tree species Klein, Tamir; Shpringer, Idan; Fikler, Ben Forest Ecology and Management, Vol. 302 https://doi.org/10.1016/j.foreco.2013.03.044	journal	August 2013
Long term trends of stand transpiration in a remnant forest during wet and dry years Zeppel, Melanie J. B.; Macinnis-Ng, Catriona M. O.; Yunusa, Isa A. M. Journal of Hydrology, Vol. 349, Issue 1-2 https://doi.org/10.1016/j.jhydrol.2007.11.001	journal	January 2008
Is xylem cavitation resistance a relevant criterion for screening drought resistance among Prunus species? Cochard, Hervé; Barigah, S. Tete; Kleinhentz, Marc Journal of Plant Physiology, Vol. 165, Issue 9 https://doi.org/10.1016/j.jplph.2007.07.020	journal	June 2008
The watering of tall trees – Embolization and recovery Gouin, Henri Journal of Theoretical Biology, Vol. 369 https://doi.org/10.1016/j.jtbi.2015.01.009	journal	March 2015
Refilling embolized xylem conduits: Is it a matter of phloem unloading? Nardini, Andrea; Lo Gullo, Maria A.; Salleo, Sebastiano Plant Science, Vol. 180, Issue 4 https://doi.org/10.1016/j.plantsci.2010.12.011	journal	April 2011
Hydraulic safety margins and embolism reversal in stems and leaves: Why are conifers and angiosperms so different? Johnson, Daniel M.; McCulloh, Katherine A.; Woodruff, David R. Plant Science, Vol. 195 https://doi.org/10.1016/j.plantsci.2012.06.010	journal	October 2012
Species-specific reversal of stem xylem embolism after a prolonged drought correlates to endpoint concentration of soluble sugars Savi, Tadeja; Casolo, Valentino; Luglio, Jessica Plant Physiology and Biochemistry, Vol. 106 https://doi.org/10.1016/j.plaphy.2016.04.051	journal	September 2016
Drought-induced embolism in stems of sunflower: A comparison of in vivo micro-CT observations and destructive hydraulic measurements Savi, Tadeja; Miotto, Andrea; Petruzzellis, Francesco Plant Physiology and Biochemistry, Vol. 120 https://doi.org/10.1016/j.plaphy.2017.09.017	journal	November 2017
The interdependence of mechanisms underlying climate-driven vegetation mortality McDowell, Nate G.; Beerling, David J.; Breshears, David D. Trends in Ecology & Evolution, Vol. 26, Issue 10 https://doi.org/10.1016/j.tree.2011.06.003	journal	October 2011
Global convergence in the vulnerability of forests to drought Choat, Brendan; Jansen, Steven; Brodribb, Tim J. Nature, Vol. 491, Issue 7426 https://doi.org/10.1038/nature11688	journal	November 2012
Death from drought in tropical forests is triggered by hydraulics not carbon starvation Rowland, L.; da Costa, A. C. L.; Galbraith, D. R. Nature, Vol. 528, Issue 7580 https://doi.org/10.1038/nature15539	journal	November 2015
Limits to xylem refilling under negative pressure in Laurus nobilis and Acer negundo Hacke, U. G.; Sperry, J. S. Plant, Cell and Environment, Vol. 26, Issue 2 https://doi.org/10.1046/j.1365-3040.2003.00962.x	journal	February 2003
The roles of hydraulic and carbon stress in a widespread climate-induced forest die-off Anderegg, W. R. L.; Berry, J. A.; Smith, D. D. Proceedings of the National Academy of Sciences, Vol. 109, Issue 1 https://doi.org/10.1073/pnas.1107891109	journal	December 2011
The Role of Aquaporins in Root Water Uptake Javot, H. Annals of Botany, Vol. 90, Issue 3 https://doi.org/10.1093/aob/mcf199	journal	August 2002
Long-term functional plasticity in plant hydraulic architecture in response to supplemental moisture von Arx, G.; Archer, S. R.; Hughes, M. K. Annals of Botany, Vol. 109, Issue 6 https://doi.org/10.1093/aob/mcs030	journal	March 2012
Visualization of embolism formation in the xylem of liana stems using neutron radiography Tötzke, Christian; Miranda, Tatiana; Konrad, Wilfried Annals of Botany, Vol. 111, Issue 4 https://doi.org/10.1093/aob/mct014	journal	February 2013
Field measurements of xylem cavitation: are acoustic emissions useful? Jackson, G. E.; Grace, J. Journal of Experimental Botany, Vol. 47, Issue 11 https://doi.org/10.1093/jxb/47.11.1643	journal	January 1996
Diurnal cycles of embolism formation and repair in petioles of grapevine (Vitis vinifera cv. Chasselas) Zufferey, V.; Cochard, H.; Ameglio, T. Journal of Experimental Botany, Vol. 62, Issue 11 https://doi.org/10.1093/jxb/err081	journal	March 2011
More than just a vulnerable pipeline: xylem physiology in the light of ion-mediated regulation of plant water transport Nardini, A.; Salleo, S.; Jansen, S. Journal of Experimental Botany, Vol. 62, Issue 14 https://doi.org/10.1093/jxb/err208	journal	July 2011
A broad survey of hydraulic and mechanical safety in the xylem of conifers Bouche, Pauline S.; Larter, Maximilien; Domec, Jean-Christophe Journal of Experimental Botany, Vol. 65, Issue 15 https://doi.org/10.1093/jxb/eru218	journal	June 2014
Structures of Bordered Pits Potentially Contributing to Isolation of a Refilled Vessel from Negative Xylem Pressure in Stems of Morus australis Poir.: Testing of the Pit Membrane Osmosis and Pit Valve Hypotheses Ooeda, Hiroki; Terashima, Ichiro; Taneda, Haruhiko Plant and Cell Physiology https://doi.org/10.1093/pcp/pcw196	journal	December 2016
Xylem dysfunction in Quercus: vessel sizes, tyloses, cavitation and seasonal changes in embolism Cochard, H.; Tyree, M. T. Tree Physiology, Vol. 6, Issue 4 https://doi.org/10.1093/treephys/6.4.393	journal	December 1990
Changes of hydraulic conductivity during dehydration and rehydration in Quercus serrata Thunb. and Betula platyphylla var. japonica Hara: the effect of xylem structures Ogasa, M.; Miki, N.; Yoshikawa, K. Tree Physiology, Vol. 30, Issue 5 https://doi.org/10.1093/treephys/tpq011	journal	April 2010
Hydraulic adjustments underlying drought resistance of Pinus halepensis Klein, T.; Cohen, S.; Yakir, D. Tree Physiology, Vol. 31, Issue 6 https://doi.org/10.1093/treephys/tpr047	journal	June 2011
Recovery performance in xylem hydraulic conductivity is correlated with cavitation resistance for temperate deciduous tree species Ogasa, M.; Miki, N. H.; Murakami, Y. Tree Physiology, Vol. 33, Issue 4 https://doi.org/10.1093/treephys/tpt010	journal	March 2013
Coping with drought-induced xylem cavitation: coordination of embolism repair and ionic effects in three Mediterranean evergreens Trifilo, P.; Barbera, P. M.; Raimondo, F. Tree Physiology, Vol. 34, Issue 2 https://doi.org/10.1093/treephys/tpt119	journal	January 2014
Variation in photosynthetic performance and hydraulic architecture across European beech (Fagus sylvatica L.) populations supports the case for local adaptation to water stress Aranda, I.; Cano, F. J.; Gasco, A. Tree Physiology, Vol. 35, Issue 1 https://doi.org/10.1093/treephys/tpu101	journal	December 2014
Diurnal changes in embolism rate in nine dry forest trees: relationships with species-specific xylem vulnerability, hydraulic strategy and wood traits Trifilò, Patrizia; Nardini, Andrea; Gullo, Maria A. Lo Tree Physiology, Vol. 35, Issue 7 https://doi.org/10.1093/treephys/tpv049	journal	June 2015
Hydraulic Failure Defines the Recovery and Point of Death in Water-Stressed Conifers Brodribb, Tim J.; Cochard, Hervé Plant Physiology, Vol. 149, Issue 1 https://doi.org/10.1104/pp.108.129783	journal	November 2008
Analysis of Xylem Sap from Functional (Nonembolized) and Nonfunctional (Embolized) Vessels of Populus nigra : Chemistry of Refilling Secchi, Francesca; Zwieniecki, Maciej A. Plant Physiology, Vol. 160, Issue 2 https://doi.org/10.1104/pp.112.200824	journal	July 2012
Cavitation and Its Discontents: Opportunities for Resolving Current Controversies Rockwell, Fulton E.; Wheeler, James K.; Holbrook, N. Michele Plant Physiology, Vol. 164, Issue 4 https://doi.org/10.1104/pp.113.233817	journal	February 2014
Uptake of Water via Branches Helps Timberline Conifers Refill Embolized Xylem in Late Winter Mayr, Stefan; Schmid, Peter; Laur, Joan Plant Physiology, Vol. 164, Issue 4 https://doi.org/10.1104/pp.114.236646	journal	February 2014
Down-Regulation of Plasma Intrinsic Protein1 Aquaporin in Poplar Trees Is Detrimental to Recovery from Embolism Secchi, Francesca; Zwieniecki, Maciej A. Plant Physiology, Vol. 164, Issue 4 https://doi.org/10.1104/pp.114.237511	journal	February 2014
Direct X-Ray Microtomography Observation Confirms the Induction of Embolism upon Xylem Cutting under Tension Torres-Ruiz, José M.; Jansen, Steven; Choat, Brendan Plant Physiology, Vol. 167, Issue 1 https://doi.org/10.1104/pp.114.249706	journal	November 2014
Visualization of Cavitated Vessels in Winter and Refilled Vessels in Spring in Diffuse-Porous Trees by Cryo-Scanning Electron Microscopy Utsumi, Yasuhiro; Sano, Yuzou; Fujikawa, Seizo Plant Physiology, Vol. 117, Issue 4 https://doi.org/10.1104/pp.117.4.1463	journal	August 1998
Refilling of Embolized Vessels in Young Stems of Laurel. Do We Need a New Paradigm? Tyree, Melvin Thomas; Salleo, Sebastiano; Nardini, Andrea Plant Physiology, Vol. 120, Issue 1 https://doi.org/10.1104/pp.120.1.11	journal	May 1999
Bordered Pit Structure and Vessel Wall Surface Properties. Implications for Embolism Repair Zwieniecki, Maciej Andrzej; Holbrook, Noel Michele Plant Physiology, Vol. 123, Issue 3 https://doi.org/10.1104/pp.123.3.1015	journal	July 2000
Cryo-Scanning Electron Microscopy Observations of Vessel Content during Transpiration in Walnut Petioles. Facts or Artifacts? Cochard, Hervé; Bodet, Christian; Améglio, Thierry Plant Physiology, Vol. 124, Issue 3 https://doi.org/10.1104/pp.124.3.1191	journal	November 2000
In Vivo Observation of Cavitation and Embolism Repair Using Magnetic Resonance Imaging Holbrook, N. Michele; Ahrens, Eric T.; Burns, Michael J. Plant Physiology, Vol. 126, Issue 1 https://doi.org/10.1104/pp.126.1.27	journal	May 2001
Easy Come, Easy Go: Capillary Forces Enable Rapid Refilling of Embolized Primary Xylem Vessels Rolland, Vivien; Bergstrom, Dana M.; Lenné, Thomas Plant Physiology, Vol. 168, Issue 4 https://doi.org/10.1104/pp.15.00333	journal	June 2015
Evidence for Hydraulic Vulnerability Segmentation and Lack of Xylem Refilling under Tension Charrier, Guillaume; Torres-Ruiz, José M.; Badel, Eric Plant Physiology, Vol. 172, Issue 3 https://doi.org/10.1104/pp.16.01079	journal	September 2016
Physiological regulation and efficient xylem water transport regulate diurnal water and carbon balances of tropical lianas Chen, Ya-Jun; Schnitzer, Stefan A.; Zhang, Yong-Jiang Functional Ecology, Vol. 31, Issue 2 https://doi.org/10.1111/1365-2435.12724	journal	September 2016
Drought-induced leaf shedding in walnut: evidence for vulnerability segmentation Tyree, M. T.; Cochard, H.; Cruiziat, P. Plant, Cell and Environment, Vol. 16, Issue 7 https://doi.org/10.1111/j.1365-3040.1993.tb00511.x	journal	September 1993
Modelling the soil-plant-atmosphere continuum in a Quercus-Acer stand at Harvard Forest: the regulation of stomatal conductance by light, nitrogen and soil/plant hydraulic properties Williams, M.; Rastetter, E. B.; Fernandes, D. N. Plant, Cell and Environment, Vol. 19, Issue 8 https://doi.org/10.1111/j.1365-3040.1996.tb00456.x	journal	August 1996
New evidence for a role of vessel-associated cells and phloem in the rapid xylem refilling of cavitated stems of Laurus nobilis L. Salleo, S.; Lo Gullo, M. A.; Trifilo, P. Plant, Cell and Environment, Vol. 27, Issue 8 https://doi.org/10.1111/j.1365-3040.2004.01211.x	journal	August 2004
Patterns of PIP gene expression in Populus trichocarpa during recovery from xylem embolism suggest a major role for the PIP1 aquaporin subfamily as moderators of refilling process: Xylem embolism refilling in poplar: the role of aquaporins Secchi, Francesca; Zwieniecki, Maciej A. Plant, Cell & Environment, Vol. 33, Issue 8 https://doi.org/10.1111/j.1365-3040.2010.02147.x	journal	March 2010
Mechanism of water-stress induced cavitation in conifers: bordered pit structure and function support the hypothesis of seal capillary-seeding: Cavitation in conifers Delzon, Sylvain; Douthe, Cyril; Sala, Anna Plant, Cell & Environment, Vol. 33, Issue 12 https://doi.org/10.1111/j.1365-3040.2010.02208.x	journal	November 2010
Sensing embolism in xylem vessels: the role of sucrose as a trigger for refilling: Sensing embolism in poplar vessels Secchi, Francesca; Zwieniecki, Maciej A. Plant, Cell & Environment, Vol. 34, Issue 3 https://doi.org/10.1111/j.1365-3040.2010.02259.x	journal	January 2011
Vulnerability curves by centrifugation: is there an open vessel artefact, and are ‘r’ shaped curves necessarily invalid?: Vulnerability curves by centrifugation Sperry, John S.; Christman, Mairgareth A.; Torres-Ruiz, Jose M. Plant, Cell & Environment, Vol. 35, Issue 3 https://doi.org/10.1111/j.1365-3040.2011.02439.x	journal	November 2011
Variation in embolism occurrence and repair along the stem in drought-stressed and re-watered seedlings of a poplar clone Leng, Huani; Lu, Mengzhu; Wan, Xianchong Physiologia Plantarum, Vol. 147, Issue 3 https://doi.org/10.1111/j.1399-3054.2012.01665.x	journal	July 2012
Water Relations and Ultrasound Emissions of Pinus Sylvestris l. Before, During and After a Period of Water Stress Pena, Jose; Grace, John New Phytologist, Vol. 103, Issue 3 https://doi.org/10.1111/j.1469-8137.1986.tb02889.x	journal	July 1986
Xylem recovery from cavitation-induced embolism in young plants of Laurus nobilis: a possible mechanism Salleo, Sebastiano; Gullo, M. Assukta Lo; Paoli, Dorotea New Phytologist, Vol. 132, Issue 1 https://doi.org/10.1111/j.1469-8137.1996.tb04507.x	journal	January 1996
Stomatal protection against hydraulic failure: a comparison of coexisting ferns and angiosperms Brodribb, Tim J.; Holbrook, N. Michele New Phytologist, Vol. 162, Issue 3 https://doi.org/10.1111/j.1469-8137.2004.01060.x	journal	June 2004
Xylem function and growth rate interact to determine recovery rates after exposure to extreme water deficit Brodribb, Tim J.; Bowman, David J. M. S.; Nichols, Scott New Phytologist, Vol. 188, Issue 2 https://doi.org/10.1111/j.1469-8137.2010.03393.x	journal	July 2010
Do quantitative vessel and pit characters account for ion-mediated changes in the hydraulic conductance of angiosperm xylem? Jansen, Steven; Gortan, Emmanuelle; Lens, Frederic New Phytologist, Vol. 189, Issue 1 https://doi.org/10.1111/j.1469-8137.2010.03448.x	journal	September 2010
Testing hypotheses that link wood anatomy to cavitation resistance and hydraulic conductivity in the genus Acer Lens, Frederic; Sperry, John S.; Christman, Mairgareth A. New Phytologist, Vol. 190, Issue 3 https://doi.org/10.1111/j.1469-8137.2010.03518.x	journal	November 2010
Rare pits, large vessels and extreme vulnerability to cavitation in a ring-porous tree species Christman, Mairgareth A.; Sperry, John S.; Smith, Duncan D. New Phytologist, Vol. 193, Issue 3 https://doi.org/10.1111/j.1469-8137.2011.03984.x	journal	December 2011
Light-dependent maintenance of hydraulic function in mangrove branches: do xylary chloroplasts play a role in embolism repair?: Rapid report Schmitz, N.; Egerton, J. J. G.; Lovelock, C. E. New Phytologist, Vol. 195, Issue 1 https://doi.org/10.1111/j.1469-8137.2012.04187.x	journal	May 2012
Foliar uptake of fog water and transport belowground alleviates drought effects in the cloud forest tree species, Drimys brasiliensis (Winteraceae) Eller, Cleiton B.; Lima, Aline L.; Oliveira, Rafael S. New Phytologist, Vol. 199, Issue 1 https://doi.org/10.1111/nph.12248	journal	March 2013
Feature: Improving our knowledge of drought-induced forest mortality through experiments, observations, and modeling McDowell, Nate G.; Ryan, Michael G.; Zeppel, Melanie J. B. New Phytologist, Vol. 200, Issue 2 https://doi.org/10.1111/nph.12502	journal	September 2013
Towards an advanced assessment of the hydrological vulnerability of forests to climate change-induced drought Klein, Tamir; Yakir, Dan; Buchmann, Nina New Phytologist, Vol. 201, Issue 3 https://doi.org/10.1111/nph.12548	journal	October 2013
Exploring Picea glauca aquaporins in the context of needle water uptake and xylem refilling Laur, Joan; Hacke, Uwe G. New Phytologist, Vol. 203, Issue 2 https://doi.org/10.1111/nph.12806	journal	April 2014
Spatial and temporal variation in plant hydraulic traits and their relevance for climate change impacts on vegetation Anderegg, William R. L. New Phytologist, Vol. 205, Issue 3 https://doi.org/10.1111/nph.12907	journal	July 2014
The standard centrifuge method accurately measures vulnerability curves of long-vesselled olive stems Hacke, Uwe G.; Venturas, Martin D.; MacKinnon, Evan D. New Phytologist, Vol. 205, Issue 1 https://doi.org/10.1111/nph.13017	journal	September 2014
Synchrotron X-ray microtomography of xylem embolism in Sequoia sempervirens saplings during cycles of drought and recovery Choat, Brendan; Brodersen, Craig R.; McElrone, Andrew J. New Phytologist, Vol. 205, Issue 3 https://doi.org/10.1111/nph.13110	journal	November 2014
Drought and resprouting plants Zeppel, Melanie J. B.; Harrison, Sandy P.; Adams, Henry D. New Phytologist, Vol. 206, Issue 2 https://doi.org/10.1111/nph.13205	journal	December 2014
What plant hydraulics can tell us about responses to climate-change droughts Sperry, John S.; Love, David M. New Phytologist, Vol. 207, Issue 1 https://doi.org/10.1111/nph.13354	journal	March 2015
Xylem cavitation resistance can be estimated based on time-dependent rate of acoustic emissions Nolf, Markus; Beikircher, Barbara; Rosner, Sabine New Phytologist, Vol. 208, Issue 2 https://doi.org/10.1111/nph.13476	journal	May 2015
Weak tradeoff between xylem safety and xylem-specific hydraulic efficiency across the world's woody plant species Gleason, Sean M.; Westoby, Mark; Jansen, Steven New Phytologist, Vol. 209, Issue 1 https://doi.org/10.1111/nph.13646	journal	September 2015
Diversity in plant hydraulic traits explains seasonal and inter-annual variations of vegetation dynamics in seasonally dry tropical forests Xu, Xiangtao; Medvigy, David; Powers, Jennifer S. New Phytologist, Vol. 212, Issue 1 https://doi.org/10.1111/nph.14009	journal	May 2016
X-ray microtomography observations of xylem embolism in stems of Laurus nobilis are consistent with hydraulic measurements of percentage loss of conductance Nardini, Andrea; Savi, Tadeja; Losso, Adriano New Phytologist, Vol. 213, Issue 3 https://doi.org/10.1111/nph.14245	journal	October 2016
Visualization of xylem embolism by X-ray microtomography: a direct test against hydraulic measurements Nolf, Markus; Lopez, Rosana; Peters, Jennifer M. R. New Phytologist, Vol. 214, Issue 2 https://doi.org/10.1111/nph.14462	journal	February 2017
Foggy days and dry nights determine crown-level water balance in a seasonal tropical montane cloud forest: Foliar uptake and night-time transpiration determine crown-level water balance Gotsch, Sybil G.; Asbjornsen, Heidi; Holwerda, Friso Plant, Cell & Environment, Vol. 37, Issue 1 https://doi.org/10.1111/pce.12151	journal	July 2013
Rapid hydraulic recovery in Eucalyptus pauciflora after drought: linkages between stem hydraulics and leaf gas exchange : Rapid hydraulic recovery in Eucalyptus Martorell, SebastiÀ; Diaz-Espejo, Antonio; Medrano, HipÓLito Plant, Cell & Environment, Vol. 37, Issue 3 https://doi.org/10.1111/pce.12182	journal	September 2013
Frost fatigue and spring recovery of xylem vessels in three diffuse-porous trees in situ : Frost fatigue in diffuse-porous trees Christensen-Dalsgaard, Karen K.; Tyree, Melvin T. Plant, Cell & Environment, Vol. 37, Issue 5 https://doi.org/10.1111/pce.12216	journal	November 2013
The dynamic pipeline: hydraulic capacitance and xylem hydraulic safety in four tall conifer species: The dynamic pipeline Mcculloh, Katherine A.; Johnson, Daniel M.; Meinzer, Frederick C. Plant, Cell & Environment, Vol. 37, Issue 5 https://doi.org/10.1111/pce.12225	journal	December 2013
Relax and refill: xylem rehydration prior to hydraulic measurements favours embolism repair in stems and generates artificially low PLC values: Xylem rehydration and embolism repair TrifilÒ, Patrizia; Raimondo, Fabio; Lo Gullo, Maria A. Plant, Cell & Environment, Vol. 37, Issue 11 https://doi.org/10.1111/pce.12313	journal	April 2014
X-ray microtomography (micro-CT): a reference technology for high-resolution quantification of xylem embolism in trees: A reference method for xylem embolism Cochard, H.; Delzon, S.; Badel, E. Plant, Cell & Environment, Vol. 38, Issue 1 https://doi.org/10.1111/pce.12391	journal	July 2014
Excising stem samples underwater at native tension does not induce xylem cavitation: No evidence for a tension-cutting artefact Venturas, Martin D.; Mackinnon, Evan D.; Jacobsen, Anna L. Plant, Cell & Environment, Vol. 38, Issue 6 https://doi.org/10.1111/pce.12461	journal	November 2014
Vulnerability to drought-induced cavitation in poplars: synthesis and future opportunities: Drought-induced cavitation in poplars: a review Fichot, RÉGis; Brignolas, Franck; Cochard, HervÉ Plant, Cell & Environment, Vol. 38, Issue 7 https://doi.org/10.1111/pce.12491	journal	January 2015
Vulnerability to cavitation differs between current-year and older xylem: non-destructive observation with a compact magnetic resonance imaging system of two deciduous diffuse-porous species: Cavitation in current-year and older xylem Fukuda, Kenji; Kawaguchi, Daichi; Aihara, Tomo Plant, Cell & Environment, Vol. 38, Issue 12 https://doi.org/10.1111/pce.12510	journal	March 2015
Vulnerability to cavitation in Olea europaea current-year shoots: further evidence of an open-vessel artifact associated with centrifuge and air-injection techniques Torres-Ruiz, José M.; Cochard, Hervé; Mayr, Stefan Physiologia Plantarum, Vol. 152, Issue 3 https://doi.org/10.1111/ppl.12185	journal	April 2014
Dwarf shrub hydraulics: two Vaccinium species ( Vaccinium myrtillus, Vaccinium vitis-idaea ) of the European Alps compared Ganthaler, Andrea; Mayr, Stefan Physiologia Plantarum, Vol. 155, Issue 4 https://doi.org/10.1111/ppl.12333	journal	March 2015
Visualizing wood anatomy in three dimensions with high-resolution X-ray micro-tomography (μCT ) – a review – Brodersen, Craig R. IAWA Journal, Vol. 34, Issue 4 https://doi.org/10.1163/22941932-00000033	journal	January 2013
Formation and Repair of Xylem Embolisms: Current State of Knowledge and Implications for Irrigation of Horticultural Crops Schenk, H. J. Acta Horticulturae, Issue 1038 https://doi.org/10.17660/ActaHortic.2014.1038.37	journal	June 2014
Mortality of Large Trees and Lianas Following Experimental Drought in an Amazon Forest Nepstad, Daniel C.; Tohver, Ingrid Marisa; Ray, David Ecology, Vol. 88, Issue 9 https://doi.org/10.1890/06-1046.1	journal	September 2007
Maintenance of xylem Network Transport Capacity: A Review of Embolism Repair in Vascular Plants Brodersen, Craig R.; McElrone, Andrew J. Frontiers in Plant Science, Vol. 4 https://doi.org/10.3389/fpls.2013.00108	journal	January 2013
The physiological resilience of fern sporophytes and gametophytes: advances in water relations offer new insights into an old lineage Pittermann, Jarmila; Brodersen, Craig; Watkins, James E. Frontiers in Plant Science, Vol. 4 https://doi.org/10.3389/fpls.2013.00285	journal	January 2013
Diurnal dynamics of water transport, storage and hydraulic conductivity in pine trees under seasonal drought Klein, T.; Cohen, S.; Paudel, I. iForest - Biogeosciences and Forestry, Vol. 9, Issue 5 https://doi.org/10.3832/ifor2046-009	journal	January 2016
Magnetic resonance imaging of water ascent in embolized xylem vessels of grapevine stem segments Wang, Mingtao; Tyree, Melvin T.; Wasylishen, Roderick E. Canadian Journal of Plant Science, Vol. 93, Issue 5 https://doi.org/10.4141/cjps2013-025	journal	September 2013
MAESPA: a model to study interactions between water limitation, environmental drivers and vegetation function at tree and stand levels, with an example application to [CO ₂ ] × drought interactions Duursma, R. A.; Medlyn, B. E. Geoscientific Model Development, Vol. 5, Issue 4 https://doi.org/10.5194/gmd-5-919-2012	journal	January 2012
Improved simulation of fire–vegetation interactions in the Land surface Processes and eXchanges dynamic global vegetation model (LPX-Mv1) Kelley, D. I.; Harrison, S. P.; Prentice, I. C. Geoscientific Model Development, Vol. 7, Issue 5 https://doi.org/10.5194/gmd-7-2411-2014	journal	January 2014
Linking hydraulic traits to tropical forest function in a size-structured and trait-driven model (TFS v.1-Hydro) Christoffersen, Bradley O.; Gloor, Manuel; Fauset, Sophie Geoscientific Model Development, Vol. 9, Issue 11 https://doi.org/10.5194/gmd-9-4227-2016	journal	January 2016
Improved simulation of fire-vegetation interactions in the Land surface Processes and eXchanges dynamic global vegetation model (LPX-Mv1) Kelley, D. I.; Harrison, S. P.; Prentice, I. C. Geoscientific Model Development Discussions, Vol. 7, Issue 1 https://doi.org/10.5194/gmdd-7-931-2014	journal	January 2014

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Anisohydric behavior linked to persistent hydraulic damage and delayed drought recovery across seven North American tree species Kannenberg, Steven A.; Novick, Kimberly A.; Phillips, Richard P. New Phytologist, Vol. 222, Issue 4 https://doi.org/10.1111/nph.15699	journal	February 2019
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