Visual and hydraulic techniques produce similar estimates of cavitation resistance in woody species.


Journal

The New phytologist
ISSN: 1469-8137
Titre abrégé: New Phytol
Pays: England
ID NLM: 9882884

Informations de publication

Date de publication:
11 2020
Historique:
received: 10 02 2020
accepted: 02 06 2020
pubmed: 17 6 2020
medline: 15 5 2021
entrez: 17 6 2020
Statut: ppublish

Résumé

Hydraulic failure of the plant vascular system is a principal cause of forest die-off under drought. Accurate quantification of this process is essential to our understanding of the physiological mechanisms underpinning plant mortality. Imaging techniques increasingly are applied to estimate xylem cavitation resistance. These techniques allow for in situ measurement of embolism formation in real time, although the benefits and trade-offs associated with different techniques have not been evaluated in detail. Here we compare two imaging methods, microcomputed tomography (microCT) and optical vulnerability (OV), to standard hydraulic methods for measurement of cavitation resistance in seven woody species representing a diversity of major phylogenetic and xylem anatomical groups. Across the seven species, there was strong agreement between cavitation resistance values (P

Identifiants

pubmed: 32542732
doi: 10.1111/nph.16746
doi:

Substances chimiques

Water 059QF0KO0R

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

884-897

Informations de copyright

© 2020 The Authors. New Phytologist © 2020 New Phytologist Trust.

Références

Adams HD, Guardiola-Claramonte M, Barron-Gafford GA, Villegas JC, Breshears DD, Zou CB, Troch PA, Huxman TE. 2009. Temperature sensitivity of drought-induced tree mortality portends increased regional die-off under global-change-type drought. Proceedings of the National Academy of Sciences, USA 106: 7063-7066.
Adams HD, Zeppel MJB, Anderegg WRL, Hartmann H, Landhäusser SM, Tissue DT, Huxman TE, Hudson PJ, Franz TE, Allen CD et al. 2017. A multi-species synthesis of physiological mechanisms in drought-induced tree mortality. Nature Ecology & Evolution 1: 1285-1291.
Alder NN, Pockman WT, Sperry JS, Nuismer S. 1997. Use of centrifugal force in the study of xylem cavitation. Journal of Experimental Botany 48: 665-674.
De Baerdemaeker NJF, Arachchige KNR, Zinkernagel J, Van den Bulcke J, Van Acker J, Schenk HJ, Steppe K. 2019. The stability enigma of hydraulic vulnerability curves: addressing the link between hydraulic conductivity and drought-induced embolism. Tree Physiology 39: 1646-1664.
Bouche PS, Delzon S, Choat B, Badel E, Brodribb TJ, Burlett R, Cochard H, Charra-Vaskou K, Lavigne B, Li S et al. 2016. Are needles of Pinus pinaster more vulnerable to xylem embolism than branches? New insights from X-ray computed tomography: embolism resistance of pine needles. Plant, Cell & Environment 39: 860-870.
Bouda M, Windt CW, McElrone AJ, Brodersen CR. 2019. In vivo pressure gradient heterogeneity increases flow contribution of small diameter vessels in grapevine. Nature Communications 10: 1-10.
Bourne AE, Creek D, Peters JMR, Ellsworth DS, Choat B. 2017. Species climate range influences hydraulic and stomatal traits in Eucalyptus species. Annals of Botany 120: 123-133.
Brodersen CR. 2013. Visualizing wood anatomy in three dimensions with high-resolution X-ray micro-tomography (μCT) - a review. IAWA Journal 34: 408-424.
Brodersen CR, McElrone AJ, Choat B, Matthews MA, Shackel KA. 2010. The dynamics of embolism repair in xylem. In vivo visualizations using high-resolution computed tomography. Plant Physiology 154: 1088-1095.
Brodribb TJ, Carriqui M, Delzon S, Lucani C. 2017. Optical measurement of stem xylem vulnerability. Plant Physiology 174: 2054-2061.
Brodribb TJ, Cochard H. 2009. Hydraulic failure defines the recovery and point of death in water-stressed conifers. Plant Physiology 149: 575-584.
Brodribb T, Hill RS. 1999. The importance of xylem constraints in the distribution of conifer species. New Phytologist 143: 365-372.
Brodribb TJ, Skelton RP, McAdam SAM, Bienaimé D, Lucani CJ, Marmottant P. 2016. Visual quantification of embolism reveals leaf vulnerability to hydraulic failure. New Phytologist 209: 1403-1409.
Choat B, Badel E, Burlett R, Delzon S, Cochard H, Jansen S. 2016. Noninvasive measurement of vulnerability to drought-induced embolism by x-ray microtomography. Plant Physiology 170: 273-282.
Choat B, Brodersen CR, McElrone AJ. 2015. Synchrotron X-ray microtomography of xylem embolism in Sequoia sempervirens saplings during cycles of drought and recovery. New Phytologist 205: 1095-1105.
Choat B, Brodribb TJ, Brodersen CR, Duursma RA, López R, Medlyn BE. 2018. Triggers of tree mortality under drought. Nature 558: 531-539.
Choat B, Drayton WM, Brodersen C, Mattthews MA, Shackel KA, Wada H, Mcelrone AJ. 2010. Measurement of vulnerability to water stress-induced cavitation in grapevine: a comparison of four techniques applied to a long-vesseled species: comparison of vulnerability curve technique in grapevine. Plant, Cell & Environment 33: 1502-1512.
Choat B, Jansen S, Brodribb TJ, Cochard H, Delzon S, Bhaskar R, Bucci SJ, Feild TS, Gleason SM, Hacke UG et al. 2012. Global convergence in the vulnerability of forests to drought. Nature 491: 752-755.
Ciais Ph, Reichstein M, Viovy N, Granier A, Ogée J, Allard V, Aubinet M, Buchmann N, Chr Bernhofer, Carrara A et al. 2005. Europe-wide reduction in primary productivity caused by the heat and drought in 2003. Nature 437: 529-533.
Cochard H. 2002. A technique for measuring xylem hydraulic conductance under high negative pressures. Plant, Cell & Environment 25: 815-819.
Cochard H, Badel E, Herbette S, Delzon S, Choat B, Jansen S. 2013. Methods for measuring plant vulnerability to cavitation: a critical review. Journal of Experimental Botany 64: 4779-4791.
Cochard H, Damour G, Bodet C, Tharwat I, Poirier M, Améglio T. 2005. Evaluation of a new centrifuge technique for rapid generation of xylem vulnerability curves. Physiologia Plantarum 124: 410-418.
Cochard H, Delzon S, Badel E. 2015. X-ray microtomography (micro-CT): a reference technology for high-resolution quantification of xylem embolism in trees: A reference method for xylem embolism. Plant, Cell & Environment 38: 201-206.
Cochard H, Herbette S, Barigah T, Badel E, Ennajeh M, Vilagrosa A. 2010. Does sample length influence the shape of xylem embolism vulnerability curves? A test with the Cavitron spinning technique: Shape of xylem embolism vulnerability curves. Plant, Cell & Environment 33: 1543-1552.
Cumming G, Fidler F, Vaux DL. 2007. Error bars in experimental biology. Journal of Cell Biology 177: 7-11.
Dixon HH, Joly J. 1894. On the ascent of sap. Proceedings of the Royal Society of London 57: 3-5.
Duke NC, Kovacs JM, Griffiths AD, Preece L, Hill DJE, van Oosterzee P, Mackenzie J, Morning HS, Burrows D. 2017. Large-scale dieback of mangroves in Australia. Marine and Freshwater Research 68: 1816.
Duursma RA, Choat B. 2017. fitplc - an R package to fit hydraulic vulnerability curves. Journal of Plant Hydraulics 4: 002
Ennajeh M, Nouiri M, Khemira H, Cochard H. 2011. Improvement to the air-injection technique to estimate xylem vulnerability to cavitation. Trees 25: 705-710.
Espino S, Schenk HJ. 2011. Mind the bubbles: achieving stable measurements of maximum hydraulic conductivity through woody plant samples. Journal of Experimental Botany 62: 1119-1132.
Hammond WM, Adams HD. 2019. Dying on time: traits influencing the dynamics of tree mortality risk from drought. Tree Physiology 39: 906-909.
Jacobsen AL, Rodriguez-Zaccaro FD, Lee TF, Valdovinos J, Toschi HS, Martinez JA, Pratt RB. 2015. Grapevine xylem development, architecture, and function. In: Hacke U, ed. Functional and ecological xylem anatomy. Cham, Switzerland: Springer International, 133-162.
Kim HK, Lee SJ. 2010. Synchrotron X-ray imaging for nondestructive monitoring of sap flow dynamics through xylem vessel elements in rice leaves. New Phytologist 188: 1085-1098.
Larter M, Pfautsch S, Domec J-C, Trueba S, Nagalingum N, Delzon S. 2017. Aridity drove the evolution of extreme embolism resistance and the radiation of conifer genus Callitris. New Phytologist 215: 97-112.
Ledger ME, Edwards FK, Brown LE, Milner AM, Woodward G. 2011. Impact of simulated drought on ecosystem biomass production: an experimental test in stream mesocosms. Global Change Biology 17: 2288-2297.
Li X, Blackman CJ, Choat B, Duursma RA, Rymer PD, Medlyn BE, Tissue DT. 2018. Tree hydraulic traits are coordinated and strongly linked to climate-of-origin across a rainfall gradient: Hydraulic traits coordination and link to climate. Plant, Cell & Environment 41: 646-660.
Li X, Delzon S, Torres-Ruiz J, Badel E, Burlett R, Cochard H, Jansen S, King A, Lamarque LJ, Lenoir N et al. 2020. Lack of vulnerability segmentation in four angiosperm tree species: evidence from direct X-ray microtomography observation. Annals of Forest Science 77: 1-12.
Li Y, Sperry JS, Taneda H, Bush SE, Hacke UG. 2007. Evaluation of centrifugal methods for measuring xylem cavitation in conifers, diffuse- and ring-porous angiosperms. New Phytologist 177: 558-568.
López R, Nolf M, Duursma RA, Badel E, Flavel RJ, Cochard H, Choat B. 2019. Mitigating the open vessel artefact in centrifuge-based measurement of embolism resistance. Tree Physiology 39: 143-155.
Losso A, Bär A, Dämon B, Dullin C, Ganthaler A, Petruzzellis F, Savi T, Tromba G, Nardini A, Mayr S et al. 2019. Insights from in vivo micro-CT analysis: testing the hydraulic vulnerability segmentation in Acer pseudoplatanus and Fagus sylvatica seedlings. New Phytologist 221: 1831-1842.
McCutchan H, Shackel KA. 1992. Stem-water potential as a sensitive indicator of water stress in prune trees (Prunus domestica L. cv. French). Journal of the American Society for Horticultural Science 117: 607-611.
McDowell N, Pockman WT, Allen CD, Breshears DD, Cobb N, Kolb T, Plaut J, Sperry J, West A, Williams DG et al. 2008. Mechanisms of plant survival and mortality during drought: why do some plants survive while others succumb to drought? New Phytologist 178: 719-739.
McElrone AJ, Choat B, Parkinson DY, MacDowell AA, Brodersen CR. 2013. Using high resolution computed tomography to visualize the three dimensional structure and function of plant vasculature. JoVE (Journal of Visualized Experiments) 74: e50162.
Michaelian M, Hogg EH, Hall RJ, Arsenault E. 2011. Massive mortality of aspen following severe drought along the southern edge of the Canadian boreal forest. Global Change Biology. 17: 2084-2094.
Mirone A, Brun E, Gouillart E, Tafforeau P, Kieffer J. 2014. The PyHST2 hybrid distributed code for high speed tomographic reconstruction with iterative reconstruction and a priori knowledge capabilities. Nuclear Instruments and Methods in Physics Research Section B: Beam Interactions with Materials and Atoms 324: 41-48.
Nardini A, Savi T, Trifilò P, Lo Gullo MA. 2017. Drought stress and the recovery from xylem embolism in woody plants. In: Cánovas FM, Lüttge U, Matyssek R, eds. Progress in botany, vol. 79. Cham, Switzerland: Springer International, 197-231.
Nolf M, Lopez R, Peters JMR, Flavel RJ, Koloadin LS, Young IM, Choat B. 2017. Visualization of xylem embolism by X-ray microtomography: a direct test against hydraulic measurements. New Phytologist 214: 890-898.
Paganin D, Mayo SC, Gureyev TE, Miller PR, Wilkins SW. 2002. Simultaneous phase and amplitude extraction from a single defocused image of a homogeneous object. Journal of Microscopy 206: 33-40.
Petruzzellis F, Pagliarani C, Savi T, Losso A, Cavalletto S, Tromba G, Dullin C, Bär A, Ganthaler A, Miotto A et al. 2018. The pitfalls of in vivo imaging techniques: evidence for cellular damage caused by synchrotron X-ray computed micro-tomography. New Phytologist 220: 104-110.
Pittermann J. 2010. The evolution of water transport in plants: an integrated approach. Geobiology 8: 112-139.
Pockman WT, Sperry JS. 2000. Vulnerability to xylem cavitation and the distribution of Sonoran Desert vegetation. American Journal of Botany 87: 1287-1299.
Pratt RB, Castro V, Fickle JC, Jacobsen AL. 2020. Embolism resistance of different aged stems of a California oak species (Quercus douglasii): optical and microCT methods differ from the benchtop-dehydration standard. Tree Physiology 40: 5-18.
Pratt RB, Jacobsen AL. 2018. Identifying which conduits are moving water in woody plants: a new HRCT-based method. Tree Physiology 38: 1200-1212.
R Core Team. 2017. R: A language and environment for statistical computing. R v.3.5.2 GUI 1.70 El Capitan build. Vienna, Austria: R Foundation for Statistical Computing. [WWW document] URL https://www.R-project.org/.
Rockwell FE, Wheeler JK, Holbrook NM. 2014. Cavitation and its discontents: opportunities for resolving current controversies. Plant Physiology 164: 1649-1660.
Rodriguez-Dominguez CM, Carins Murphy MR, Lucani C, Brodribb TJ. 2018. Mapping xylem failure in disparate organs of whole plants reveals extreme resistance in olive roots. New Phytologist 218: 1025-1035.
RStudio Team. 2015. RStudio: Integrated development for R. RStudio v.1.1.463. Boston, MA, USA: RStudio Inc. [WWW document] URL http://www.rstudio.com/.
Savi T, Miotto A, Petruzzellis F, Losso A, Pacilè S, Tromba G, Mayr S, Nardini A. 2017. Drought-induced embolism in stems of sunflower: a comparison of in vivo micro-CT observations and destructive hydraulic measurements. Plant Physiology and Biochemistry 120: 24-29.
Schneider CA, Rasband WS, Eliceiri KW. 2012. NIH Image to ImageJ: 25 years of Image Analysis. Nature Methods 9: 671-675.
Scholander PF, Hammel HT, Bradstreet ED, Hemmingsen EA. 1965. Sap pressure in vascular plants. Science 148: 339-346.
Skelton RP, Dawson TE, Thompson SE, Shen Y, Weitz AP, Ackerly D. 2018. Low vulnerability to xylem embolism in leaves and stems of North American Oaks. Plant Physiology 177: 1066-1077.
Sperry JS, Tyree MT. 1988. Mechanism of water stress-induced xylem embolism. Plant Physiology 88: 581-587.
Torres-Ruiz JM, Cochard H, Choat B, Jansen S, López R, Tomášková I, Padilla-Díaz CM, Badel E, Burlett R, King A et al. 2017. Xylem resistance to embolism: presenting a simple diagnostic test for the open vessel artefact. New Phytologist 215: 489-499.
Torres-Ruiz JM, Cochard H, Mayr S, Beikircher B, Diaz-Espejo A, Rodriguez-Dominguez CM, Badel E, Fernández JE. 2014. Vulnerability to cavitation in Olea europaea current-year shoots: further evidence of an open-vessel artifact associated with centrifuge and air-injection techniques. Physiologia Plantarum 152: 465-474.
Trenberth KE, Dai A, van der Schrier G, Jones PD, Barichivich J, Briffa KR, Sheffield J. 2014. Global warming and changes in drought. Nature Climate Change 4: 17-22.
Tyree MT, Ewers FW. 1991. The hydraulic architecture of trees and other woody plants. New Phytologist 119: 345-360.
Tyree MT, Sperry JS. 1989. Vulnerability of xylem to cavitation and embolism. Annual Review of Plant Physiology and Plant Molecular Biology 40: 19-36.
Urli M, Porté AJ, Cochard H, Guengant Y, Burlett R, Delzon S. 2013. Xylem embolism threshold for catastrophic hydraulic failure in angiosperm trees. Tree Physiology 33: 672-683.
Venturas MD, Pratt RB, Jacobsen AL, Castro V, Fickle JC, Hacke UG. 2019. Direct comparison of four methods to construct xylem vulnerability curves: differences among techniques are linked to vessel network characteristics. Plant, Cell & Environment 42: 2422-2436.
Warton DI, Duursma RA, Falster DS, Taskinen S. 2012. smatr 3- an R package for estimation and inference about allometric lines. Methods in Ecology and Evolution 3: 257-259.
Wheeler JK, Huggett BA, Tofte AN, Rockwell FE, Holbrook NM. 2013. Cutting xylem under tension or supersaturated with gas can generate PLC and the appearance of rapid recovery from embolism: sampling induced embolism. Plant, Cell & Environment 36: 1938-1949.
Williams AP, Allen CD, Macalady AK, Griffin D, Woodhouse CA, Meko DM, Swetnam TW, Rauscher SA, Seager R, Grissino-Mayer HD et al. 2013. Temperature as a potent driver of regional forest drought stress and tree mortality. Nature Climate Change 3: 292-297.
Zhang F-P, Brodribb TJ. 2017. Are flowers vulnerable to xylem cavitation during drought? Proceedings of the Royal Society of London. Series B: Biological Sciences 284: 20162642.

Auteurs

Alice Gauthey (A)

Hawkesbury Institute for the Environment, Western Sydney University, Richmond, NSW, 2753, Australia.

Jennifer M R Peters (JMR)

Hawkesbury Institute for the Environment, Western Sydney University, Richmond, NSW, 2753, Australia.

Madeline R Carins-Murphy (MR)

School of Biological Sciences, University of Tasmania, Private Bag 55, Hobart, Tas, 7001, Australia.

Celia M Rodriguez-Dominguez (CM)

School of Biological Sciences, University of Tasmania, Private Bag 55, Hobart, Tas, 7001, Australia.
Irrigation and Crop Ecophysiology Group, Instituto de Recursos Naturales y Agrobiología de Sevilla (IRNAS, CSIC), Avenida Reina Mercedes, 10, Sevilla, 41012, Spain.

Ximeng Li (X)

Hawkesbury Institute for the Environment, Western Sydney University, Richmond, NSW, 2753, Australia.

Sylvain Delzon (S)

UMR BIOGECO, INRA, Univ Bordeaux, Talence, 33450, France.

Andrew King (A)

L'Orme de Merisiers, Synchrotron SOLEIL, 91190 Saint-Aubin-BP48, Gif-sur-Yvette Cedex, France.

Rosana López (R)

Hawkesbury Institute for the Environment, Western Sydney University, Richmond, NSW, 2753, Australia.
Departamento de Sistemas y Recursos Naturales, Universidad Politécnica de Madrid, Madrid, Spain.
PIAF, INRA, University of Clermont-Auvergne, 63100, Clermont-Ferrand, France.

Belinda E Medlyn (BE)

Hawkesbury Institute for the Environment, Western Sydney University, Richmond, NSW, 2753, Australia.

David T Tissue (DT)

Hawkesbury Institute for the Environment, Western Sydney University, Richmond, NSW, 2753, Australia.

Tim J Brodribb (TJ)

School of Biological Sciences, University of Tasmania, Private Bag 55, Hobart, Tas, 7001, Australia.

Brendan Choat (B)

Hawkesbury Institute for the Environment, Western Sydney University, Richmond, NSW, 2753, Australia.

Articles similaires

Genome, Chloroplast Phylogeny Genetic Markers Base Composition High-Throughput Nucleotide Sequencing
Animals Hemiptera Insect Proteins Phylogeny Insecticides
Amaryllidaceae Alkaloids Lycoris NADPH-Ferrihemoprotein Reductase Gene Expression Regulation, Plant Plant Proteins
Drought Resistance Gene Expression Profiling Gene Expression Regulation, Plant Gossypium Multigene Family

Classifications MeSH