Home LiteratureArticle Details
PMID: 26527655 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

Noninvasive Measurement of Vulnerability to Drought-Induced Embolism by X-Ray Microtomography.

Plant physiology ·Vol. 170 ·No. 1 ·2016-01-00 ·Pages 273-82

Choat B, Badel E, Burlett R, Delzon S, Cochard H, Jansen S

Abstract

Hydraulic failure induced by xylem embolism is one of the primary mechanisms of plant dieback during drought. However, many of the methods used to evaluate the vulnerability of different species to drought-induced embolism are indirect and invasive, increasing the possibility that measurement artifacts may occur. Here, we utilize x-ray computed microtomography (microCT) to directly visualize embolism formation in the xylem of living, intact plants with contrasting wood anatomy (Quercus robur, Populus tremula × Populus alba, and Pinus pinaster). These observations were compared with widely used centrifuge techniques that require destructive sampling. MicroCT imaging provided detailed spatial information regarding the dimensions and functional status of xylem conduits during dehydration. Vulnerability curves based on microCT observations of intact plants closely matched curves based on the centrifuge technique for species with short vessels (P. tremula × P. alba) or tracheids (P. pinaster). For ring porous Q. robur, the centrifuge technique significantly overestimated vulnerability to embolism, indicating that caution should be used when applying this technique to species with long vessels. These findings confirm that microCT can be used to assess the vulnerability to embolism on intact plants by direct visualization.

MeSH Terms
Droughts Imaging, Three-Dimensional Pinus/anatomy & histology,physiology Plant Stems/physiology Populus/anatomy & histology,physiology Quercus/anatomy & histology,physiology X-Ray Microtomography/methods Xylem/anatomy & histology,physiology
Authors & Affiliations
6 authors, click to expand affiliations / ORCID
Choat Brendan
Hawkesbury Institute for the Environment, Western Sydney University, Richmond, New South Wales 2753, Australia (B.C.);Institut National de la Recherche Agronomique, Unité Mixte de Recherche 547 PIAF, F-63100 Clermont-Ferrand, France (E.B., H.C.);Université Blaise-Pascal, Unité Mixte de Recherche 547 PIAF, 63000 Clermont-Ferrand, France (E.B., H.C.);Institut National de la Recherche Agronomique, University of Bordeaux, Unité Mixte de Recherche BIOGECO, F-33450 Talence, France (R.B., S.D.); andInstitute for Systematic Botany and Ecology, Ulm University, 89081 Ulm, Germany (S.J.) b.choat@westernsydney.edu.au.
Badel Eric ORCID
Hawkesbury Institute for the Environment, Western Sydney University, Richmond, New South Wales 2753, Australia (B.C.);Institut National de la Recherche Agronomique, Unité Mixte de Recherche 547 PIAF, F-63100 Clermont-Ferrand, France (E.B., H.C.);Université Blaise-Pascal, Unité Mixte de Recherche 547 PIAF, 63000 Clermont-Ferrand, France (E.B., H.C.);Institut National de la Recherche Agronomique, University of Bordeaux, Unité Mixte de Recherche BIOGECO, F-33450 Talence, France (R.B., S.D.); andInstitute for Systematic Botany and Ecology, Ulm University, 89081 Ulm, Germany (S.J.).
Burlett Regis ORCID
Hawkesbury Institute for the Environment, Western Sydney University, Richmond, New South Wales 2753, Australia (B.C.);Institut National de la Recherche Agronomique, Unité Mixte de Recherche 547 PIAF, F-63100 Clermont-Ferrand, France (E.B., H.C.);Université Blaise-Pascal, Unité Mixte de Recherche 547 PIAF, 63000 Clermont-Ferrand, France (E.B., H.C.);Institut National de la Recherche Agronomique, University of Bordeaux, Unité Mixte de Recherche BIOGECO, F-33450 Talence, France (R.B., S.D.); andInstitute for Systematic Botany and Ecology, Ulm University, 89081 Ulm, Germany (S.J.).
Delzon Sylvain ORCID
Hawkesbury Institute for the Environment, Western Sydney University, Richmond, New South Wales 2753, Australia (B.C.);Institut National de la Recherche Agronomique, Unité Mixte de Recherche 547 PIAF, F-63100 Clermont-Ferrand, France (E.B., H.C.);Université Blaise-Pascal, Unité Mixte de Recherche 547 PIAF, 63000 Clermont-Ferrand, France (E.B., H.C.);Institut National de la Recherche Agronomique, University of Bordeaux, Unité Mixte de Recherche BIOGECO, F-33450 Talence, France (R.B., S.D.); andInstitute for Systematic Botany and Ecology, Ulm University, 89081 Ulm, Germany (S.J.).
Cochard Herve
Hawkesbury Institute for the Environment, Western Sydney University, Richmond, New South Wales 2753, Australia (B.C.);Institut National de la Recherche Agronomique, Unité Mixte de Recherche 547 PIAF, F-63100 Clermont-Ferrand, France (E.B., H.C.);Université Blaise-Pascal, Unité Mixte de Recherche 547 PIAF, 63000 Clermont-Ferrand, France (E.B., H.C.);Institut National de la Recherche Agronomique, University of Bordeaux, Unité Mixte de Recherche BIOGECO, F-33450 Talence, France (R.B., S.D.); andInstitute for Systematic Botany and Ecology, Ulm University, 89081 Ulm, Germany (S.J.).
Jansen Steven
Hawkesbury Institute for the Environment, Western Sydney University, Richmond, New South Wales 2753, Australia (B.C.);Institut National de la Recherche Agronomique, Unité Mixte de Recherche 547 PIAF, F-63100 Clermont-Ferrand, France (E.B., H.C.);Université Blaise-Pascal, Unité Mixte de Recherche 547 PIAF, 63000 Clermont-Ferrand, France (E.B., H.C.);Institut National de la Recherche Agronomique, University of Bordeaux, Unité Mixte de Recherche BIOGECO, F-33450 Talence, France (R.B., S.D.); andInstitute for Systematic Botany and Ecology, Ulm University, 89081 Ulm, Germany (S.J.).
References (46)
46 references, click to expand
  1. Diversity of hydraulic traits in nine Cordia species growing in tropical forests with contrasting precipitation.
    New Phytol. 2007;175(4):686-98 PMID: 17688584
  2. The standard centrifuge method accurately measures vulnerability curves of long-vesselled olive stems.
    New Phytol. 2015 Jan;205(1):116-27 PMID: 25229841
  3. Methods for measuring plant vulnerability to cavitation: a critical review.
    J Exp Bot. 2013 Nov;64(15):4779-91 PMID: 23888067
  4. Centrifuge technique consistently overestimates vulnerability to water stress-induced cavitation in grapevines as confirmed with high-resolution computed tomography.
    New Phytol. 2012 Nov;196(3):661-5 PMID: 22803744
  5. Rare pits, large vessels and extreme vulnerability to cavitation in a ring-porous tree species.
    New Phytol. 2012 Feb;193(3):713-20 PMID: 22150784
  6. Shoot dieback during prolonged drought in Ceanothus (Rhamnaceae) chaparral of California: a possible case of hydraulic failure.
    Am J Bot. 2002 May;89(5):820-8 PMID: 21665682
  7. Predicting thresholds of drought-induced mortality in woody plant species.
    Tree Physiol. 2013 Jul;33(7):669-71 PMID: 23878170
  8. Global convergence in the vulnerability of forests to drought.
    Nature. 2012 Nov 29;491(7426):752-5 PMID: 23172141
  9. Cutting xylem under tension or supersaturated with gas can generate PLC and the appearance of rapid recovery from embolism.
    Plant Cell Environ. 2013 Nov;36(11):1938-49 PMID: 23701011
  10. Poplar vulnerability to xylem cavitation acclimates to drier soil conditions.
    Physiol Plant. 2010 Jul 1;139(3):280-8 PMID: 20210873
  11. Plant hydraulics: the ascent of water.
    Nature. 2003 Jun 26;423(6943):923 PMID: 12827177
  12. Use of positive pressures to establish vulnerability curves : further support for the air-seeding hypothesis and implications for pressure-volume analysis.
    Plant Physiol. 1992 Sep;100(1):205-9 PMID: 16652947
  13. Water relations of Robinia pseudoacacia L.: do vessels cavitate and refill diurnally or are R-shaped curves invalid in Robinia?
    Plant Cell Environ. 2014 Dec;37(12):2667-78 PMID: 24588635
  14. No evidence for an open vessel effect in centrifuge-based vulnerability curves of a long-vesselled liana (Vitis vinifera).
    New Phytol. 2012 Jun;194(4):982-90 PMID: 22448870
  15. Functional repair of embolized vessels in maize roots after temporal drought stress, as demonstrated by magnetic resonance imaging.
    New Phytol. 2009;184(1):245-56 PMID: 19563443
  16. Vulnerability to cavitation in Olea europaea current-year shoots: further evidence of an open-vessel artifact associated with centrifuge and air-injection techniques.
    Physiol Plant. 2014 Nov;152(3):465-74 PMID: 24611594
  17. Measurement of vulnerability to water stress-induced cavitation in grapevine: a comparison of four techniques applied to a long-vesseled species.
    Plant Cell Environ. 2010 Sep;33(9):1502-12 PMID: 20444217
  18. How reliable is the double-ended pressure sleeve technique for assessing xylem vulnerability to cavitation in woody angiosperms?
    Physiol Plant. 2011 Jul;142(3):205-10 PMID: 21401617
  19. In vivo visualizations of drought-induced embolism spread in Vitis vinifera.
    Plant Physiol. 2013 Apr;161(4):1820-9 PMID: 23463781
  20. Spatial and temporal variation in plant hydraulic traits and their relevance for climate change impacts on vegetation.
    New Phytol. 2015 Feb;205(3):1008-14 PMID: 25729797
  21. Using high resolution computed tomography to visualize the three dimensional structure and function of plant vasculature.
    J Vis Exp. 2013;(74). doi: 10.3791/50162 PMID: 23609036
  22. Improving xylem hydraulic conductivity measurements by correcting the error caused by passive water uptake.
    Physiol Plant. 2012 Oct;146(2):129-35 PMID: 22443461
  23. Hydraulic failure defines the recovery and point of death in water-stressed conifers.
    Plant Physiol. 2009 Jan;149(1):575-84 PMID: 19011001
  24. Structure and function of bordered pits: new discoveries and impacts on whole-plant hydraulic function.
    New Phytol. 2008;177(3):608-25 PMID: 18086228
  25. Direct measurement of xylem pressure in leaves of intact maize plants. A test of the cohesion-tension theory taking hydraulic architecture into consideration
    Plant Physiol. 1999 Dec;121(4):1191-206 PMID: 10594106
  26. Hydraulic efficiency and safety of vascular and non-vascular components in Pinus pinaster leaves.
    Tree Physiol. 2012 Sep;32(9):1161-70 PMID: 22907978
  27. Evaluation of centrifugal methods for measuring xylem cavitation in conifers, diffuse- and ring-porous angiosperms.
    New Phytol. 2008;177(2):558-68 PMID: 18028295
  28. Xylem embolism threshold for catastrophic hydraulic failure in angiosperm trees.
    Tree Physiol. 2013 Jul;33(7):672-83 PMID: 23658197
  29. Xylem vulnerability to cavitation can be accurately characterised in species with long vessels using a centrifuge method.
    Plant Biol (Stuttg). 2013 May;15(3):496-504 PMID: 23127246
  30. In vivo observation of cavitation and embolism repair using magnetic resonance imaging.
    Plant Physiol. 2001 May;126(1):27-31 PMID: 11351066
  31. Mechanism of water stress-induced xylem embolism.
    Plant Physiol. 1988 Nov;88(3):581-7 PMID: 16666352
  32. Bordered pit structure and function determine spatial patterns of air-seeding thresholds in xylem of Douglas-fir (Pseudotsuga menziesii; Pinaceae) trees.
    Am J Bot. 2006 Nov;93(11):1588-600 PMID: 21642104
  33. Hierarchical statistical modeling of xylem vulnerability to cavitation.
    New Phytol. 2009;182(2):541-54 PMID: 19210723
  34. Does sample length influence the shape of xylem embolism vulnerability curves? A test with the Cavitron spinning technique.
    Plant Cell Environ. 2010 Sep;33(9):1543-52 PMID: 20444214
  35. Direct x-ray microtomography observation confirms the induction of embolism upon xylem cutting under tension.
    Plant Physiol. 2015 Jan;167(1):40-3 PMID: 25378693
  36. Nanobubbles: a new paradigm for air-seeding in xylem.
    Trends Plant Sci. 2015 Apr;20(4):199-205 PMID: 25680733
  37. Visualization of cavitated vessels in winter and refilled vessels in spring in diffuse-porous trees by cryo-scanning electron microscopy
    Plant Physiol. 1998 Aug;117(4):1463-71 PMID: 9701601
  38. Recalcitrant vulnerability curves: methods of analysis and the concept of fibre bridges for enhanced cavitation resistance.
    Plant Cell Environ. 2014 Jan;37(1):35-44 PMID: 23600520
  39. The dynamics of embolism repair in xylem: in vivo visualizations using high-resolution computed tomography.
    Plant Physiol. 2010 Nov;154(3):1088-95 PMID: 20841451
  40. How reliable are methods to assess xylem vulnerability to cavitation? The issue of 'open vessel' artifact in oaks.
    Tree Physiol. 2014 Aug;34(8):894-905 PMID: 25074860
  41. Vulnerability curves by centrifugation: is there an open vessel artefact, and are 'r' shaped curves necessarily invalid?
    Plant Cell Environ. 2012 Mar;35(3):601-10 PMID: 21988455
  42. Testing hypotheses that link wood anatomy to cavitation resistance and hydraulic conductivity in the genus Acer.
    New Phytol. 2011 May;190(3):709-23 PMID: 21054413
  43. Size and function in conifer tracheids and angiosperm vessels.
    Am J Bot. 2006 Oct;93(10):1490-500 PMID: 21642096
  44. X-ray microtomography (micro-CT): a reference technology for high-resolution quantification of xylem embolism in trees.
    Plant Cell Environ. 2015 Jan;38(1):201-6 PMID: 24942003
  45. The relationships between xylem safety and hydraulic efficiency in the Cupressaceae: the evolution of pit membrane form and function.
    Plant Physiol. 2010 Aug;153(4):1919-31 PMID: 20551212
  46. Synchrotron X-ray microtomography of xylem embolism in Sequoia sempervirens saplings during cycles of drought and recovery.
    New Phytol. 2015 Feb;205(3):1095-105 PMID: 25385085
Article Info
Journal
Plant physiology
Abbr.
Plant Physiol
ISSN
1532-2548
Published
2016-01-00
Epub
2015-00-02
Pages
273-82
Language
English
Region
United States
NLM ID
0401224
PMCID
PMC4704566
Subset
IM
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: product@genelibs.com