Freeze/Thaw-Induced Embolism: Probability of Critical Bubble Formation Depends on Speed of Ice Formation

Sevanto, Sanna; Holbrook, N. Michele; Ball, Marilyn C.

doi:10.3389/fpls.2012.00107

Title: Freeze/Thaw-Induced Embolism: Probability of Critical Bubble Formation Depends on Speed of Ice Formation

Journal Article · Wed Jun 06 00:00:00 EDT 2012 · Frontiers in Plant Science

DOI:https://doi.org/10.3389/fpls.2012.00107· OSTI ID:1396108

Sevanto, Sanna ^[1]; Holbrook, N. Michele ^[1]; Ball, Marilyn C. ^[2]

Harvard Univ., Cambridge, MA (United States)
Australian National Univ., Canberra, ACT (Australia)

Bubble formation in the conduits of woody plants sets a challenge for uninterrupted water transportation from the soil up to the canopy. Freezing and thawing of stems has been shown to increase the number of air-filled (embolized) conduits, especially in trees with large conduit diameters. Despite numerous experimental studies, the mechanisms leading to bubble formation during freezing have not been addressed theoretically. We used classical nucleation theory and fluid mechanics to show which mechanisms are most likely to be responsible for bubble formation during freezing and what parameters determine the likelihood of the process. Our results confirm the common assumption that bubble formation during freezing is most likely due to gas segregation by ice. If xylem conduit walls are not permeable to the salts expelled by ice during the freezing process, osmotic pressures high enough for air seeding could be created. The build-up rate of segregated solutes in front of the ice-water interface depends equally on conduit diameter and freezing velocity. Therefore, bubble formation probability depends on these variables. The dependence of bubble formation probability on freezing velocity means that the experimental results obtained for cavitation threshold conduit diameters during freeze/thaw cycles depend on the experimental setup; namely sample size and cooling rate. The velocity dependence also suggests that to avoid bubble formation during freezing trees should have narrow conduits where freezing is likely to be fast (e.g., branches or outermost layer of the xylem). Avoidance of bubble formation during freezing could thus be one piece of the explanation why xylem conduit size of temperate and boreal zone trees varies quite systematically.

View Accepted Manuscript (DOE)

Cite

Export

Save

Research Organization:: Los Alamos National Laboratory (LANL), Los Alamos, NM (United States)

Sponsoring Organization:: USDOE

Grant/Contract Number:: AC52-06NA25396

OSTI ID:: 1396108

Report Number(s):: LA-UR-12-21317

Journal Information:: Frontiers in Plant Science, Vol. 3; ISSN 1664-462X

Publisher:: Frontiers Research FoundationCopyright Statement

Country of Publication:: United States

Language:: English

Citation Metrics:

Cited by: 53 works

Citation information provided by
Web of Science

References (56)

Bubble nucleation in liquids Blander, Milton; Katz, Joseph L. AIChE Journal, Vol. 21, Issue 5 https://doi.org/10.1002/aic.690210502	journal	September 1975
Electroconvective enhancement of mass or heat exchange between a drop or bubble and surroundings in the presence of an interfacial tension gradient Chang, L. S.; Berg, J. C. AIChE Journal, Vol. 31, Issue 1 https://doi.org/10.1002/aic.690310118	journal	January 1985
Freezing, Drying, and/or Vitrification of Membrane– Solute–Water Systems Wolfe, Joe; Bryant, Gary Cryobiology, Vol. 39, Issue 2 https://doi.org/10.1006/cryo.1999.2195	journal	September 1999
Relationships between Embolism, Stem Water Tension, and Diameter Changes HÖLttÄ, T.; Vesala, T.; PerÄMÄKi, M. Journal of Theoretical Biology, Vol. 215, Issue 1 https://doi.org/10.1006/jtbi.2001.2485	journal	March 2002
Changes in hydraulic conductivity upon freezing of the xylem of Populus x canadensis Moench ?robusta? Just, J.; Sauter, J. J. Trees, Vol. 5, Issue 2 https://doi.org/10.1007/bf00227494	journal	June 1991
Mechanism of freeze-induced embolism in Fagus sylvatica L. Lemoine, Damien; Granier, André; Cochard, H. Trees, Vol. 13, Issue 4 https://doi.org/10.1007/pl00009751	journal	June 1999
Stem water transport and freeze-thaw xylem embolism in conifers and angiosperms in a Tasmanian treeline heath Feild, Taylor S.; Brodribb, Tim Oecologia, Vol. 127, Issue 3 https://doi.org/10.1007/s004420000603	journal	May 2001
Freezing-induced xylem cavitation and the northern limit of Larrea tridentata Pockman, W. T.; Sperry, John S. Oecologia, Vol. 109, Issue 1 https://doi.org/10.1007/s004420050053	journal	January 1997
Nucleation rates and bubble stability in water-carbon dioxide solutions Wilt, P. M. Journal of Colloid and Interface Science, Vol. 112, Issue 2 https://doi.org/10.1016/0021-9797(86)90122-0	journal	August 1986
Gas segregation during solidification processes Bianchi, Marcus V. A.; Viskanta, Raymond International Journal of Heat and Mass Transfer, Vol. 40, Issue 9 https://doi.org/10.1016/s0017-9310(96)00283-9	journal	June 1997
Simulation of Osmotic Pressure in Concentrated Aqueous Salt Solutions Luo, Yun; Roux, Benoît The Journal of Physical Chemistry Letters, Vol. 1, Issue 1 https://doi.org/10.1021/jz900079w	journal	November 2009
Xylem dysfunction caused by water stress and freezing in two species of co-occurring chaparral shrubs Langan, S. J.; Ewers, F. W.; Davis, S. D. Plant, Cell and Environment, Vol. 20, Issue 4 https://doi.org/10.1046/j.1365-3040.1997.d01-94.x	journal	April 1997
Hydraulic properties and freezing-induced cavitation in sympatric evergreen and deciduous oaks with contrasting habitats Cavender-Bares, J.; Holbrook, N. M. Plant, Cell and Environment, Vol. 24, Issue 12 https://doi.org/10.1046/j.1365-3040.2001.00797.x	journal	December 2001
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
Xylem sap flow as a major pathway for oxygen supply to the sapwood of birch (Betula pubescens Ehr.) Gansert, D. Plant, Cell & Environment, Vol. 26, Issue 11 https://doi.org/10.1046/j.1365-3040.2003.01097.x	journal	September 2003
Density-functional study of homogeneous bubble nucleation in the stretched Lennard-Jones fluid Shen, Vincent K.; Debenedetti, Pablo G. The Journal of Chemical Physics, Vol. 114, Issue 9 https://doi.org/10.1063/1.1344604	journal	March 2001
Critical state of bubbles in liquid‐gas solutions Tucker, A. S.; Ward, C. A. Journal of Applied Physics, Vol. 46, Issue 11 https://doi.org/10.1063/1.321506	journal	November 1975
A new kinetic model for three-dimensional heterogeneous nucleation Liu, X. Y. The Journal of Chemical Physics, Vol. 111, Issue 4 https://doi.org/10.1063/1.479391	journal	July 1999
Vessel wall vibrations: trigger for embolism repair? Salleo, Sebastiano; Trifilò, Patrizia; Lo Gullo, Maria Assunta Functional Plant Biology, Vol. 35, Issue 4 https://doi.org/10.1071/fp07239	journal	January 2008
Evolution of Water Transport and Xylem Structure Sperry, John S. International Journal of Plant Sciences, Vol. 164, Issue S3 https://doi.org/10.1086/368398	journal	May 2003
In vivo Visualization of the Water-refilling Process in Xylem Vessels Using X-ray Micro-imaging Lee, S. -J.; Kim, Y. Annals of Botany, Vol. 101, Issue 4 https://doi.org/10.1093/aob/mcm312	journal	January 2008
Freezing in Conifer Xylem Robson, D. J.; Petty, J. A. Journal of Experimental Botany, Vol. 38, Issue 11 https://doi.org/10.1093/jxb/38.11.1901	journal	January 1987
Freezing in Conifer Xylem Robson, D. J.; McHARDY, W. J.; Petty, J. A. Journal of Experimental Botany, Vol. 39, Issue 11 https://doi.org/10.1093/jxb/39.11.1617	journal	January 1988
The effect of aqueous transport of CO2 in xylem sap on gas exchange in woody plants Levy, P. E.; Meir, P.; Allen, S. J. Tree Physiology, Vol. 19, Issue 1 https://doi.org/10.1093/treephys/19.1.53	journal	January 1999
Mechanisms of xylem recovery from winter embolism in Fagus sylvatica Cochard, H.; Lemoine, D.; Ameglio, T. Tree Physiology, Vol. 21, Issue 1 https://doi.org/10.1093/treephys/21.1.27	journal	January 2001
Effects of summer drought and winter freezing on stem hydraulic conductivity of Rhododendron species from contrasting climates Cordero, R. A.; Nilsen, E. T. Tree Physiology, Vol. 22, Issue 13 https://doi.org/10.1093/treephys/22.13.919	journal	September 2002
Winter embolism, mechanisms of xylem hydraulic conductivity recovery and springtime growth patterns in walnut and peach trees Ameglio, T.; Bodet, C.; Lacointe, A. Tree Physiology, Vol. 22, Issue 17 https://doi.org/10.1093/treephys/22.17.1211	journal	December 2002
Tracheid diameter is the key trait determining the extent of freezing-induced embolism in conifers Pittermann, J.; Sperry, J. Tree Physiology, Vol. 23, Issue 13 https://doi.org/10.1093/treephys/23.13.907	journal	September 2003
Ice propagation in plants visualized at the tissue level by infrared differential thermal analysis (IDTA) Hacker, J.; Neuner, G. Tree Physiology, Vol. 27, Issue 12 https://doi.org/10.1093/treephys/27.12.1661	journal	December 2007
Use of Positive Pressures to Establish Vulnerability Curves: Further Support for the Air-Seeding Hypothesis and Implications for Pressure-Volume Analysis Cochard, Hervé; Cruiziat, Pierre; Tyree, Melvin T. Plant Physiology, Vol. 100, Issue 1 https://doi.org/10.1104/pp.100.1.205	journal	September 1992
Analysis of Freeze-Thaw Embolism in Conifers. The Interaction between Cavitation Pressure and Tracheid Size Pittermann, Jarmila; Sperry, John S. Plant Physiology, Vol. 140, Issue 1 https://doi.org/10.1104/pp.105.067900	journal	December 2005
Embolism Formation during Freezing in the Wood of Picea abies Mayr, Stefan; Cochard, Hervé; Améglio, Thierry Plant Physiology, Vol. 143, Issue 1 https://doi.org/10.1104/pp.106.085704	journal	October 2006
Drought-Induced Xylem Dysfunction in Petioles, Branches, and Roots of Populus balsamifera L. and Alnus glutinosa (L.) Gaertn Hacke, U.; Sauter, J. J. Plant Physiology, Vol. 111, Issue 2 https://doi.org/10.1104/pp.111.2.413	journal	June 1996
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
The Progression of Cavitation in Earlywood Vessels ofFraxinus mandshurica var japonicaduring Freezing and Thawing Utsumi, Yasuhiro; Sano, Yuzou; Funada, Ryo Plant Physiology, Vol. 121, Issue 3 https://doi.org/10.1104/pp.121.3.897	journal	November 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
Winter Freezing in Relation to the Rise of Sap in Tall Trees. Lybeck, Berthe Ruud Plant Physiology, Vol. 34, Issue 4 https://doi.org/10.1104/pp.34.4.482	journal	July 1959
Different vulnerabilities of Quercus ilex L. to freeze- and summer drought-induced xylem embolism: an ecological interpretation Gullo, M. A.; Salleo, S. Plant, Cell and Environment, Vol. 16, Issue 5 https://doi.org/10.1111/j.1365-3040.1993.tb00898.x	journal	June 1993
Within-stem oxygen concentration and sap flow in four temperate tree species: does long-lived xylem parenchyma experience hypoxia? Spicer, R.; Holbrook, N. M. Plant, Cell and Environment, Vol. 28, Issue 2 https://doi.org/10.1111/j.1365-3040.2004.01262.x	journal	February 2005
The spatial pattern of air seeding thresholds in mature sugar maple trees Choat, Brendan; Lahr, Eleanor C.; Melcher, Peter J. Plant, Cell and Environment, Vol. 28, Issue 9 https://doi.org/10.1111/j.1365-3040.2005.01336.x	journal	September 2005
Freeze/thaw-induced embolism depends on nadir temperature: the heterogeneous hydration hypothesis Ball, M. C.; Canny, M. J.; Huang, C. X. Plant, Cell and Environment, Vol. 29, Issue 5 https://doi.org/10.1111/j.1365-3040.2005.01426.x	journal	May 2006
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
Freezing of Conifer Xylem and the Cohesion-Tension Theory Sucoff, Edward Physiologia Plantarum, Vol. 22, Issue 2 https://doi.org/10.1111/j.1399-3054.1969.tb07394.x	journal	February 1969
Rates of apoplastic diffusion in wheat leaves Canny, M. J. New Phytologist, Vol. 116, Issue 2 https://doi.org/10.1111/j.1469-8137.1990.tb04713.x	journal	October 1990
High‐resolution time series of vessel density in Kenyan mangrove trees reveal a link with climate Verheyden, Anouk; De Ridder, Fjo; Schmitz, Nele New Phytologist, Vol. 167, Issue 2 https://doi.org/10.1111/j.1469-8137.2005.01415.x	journal	March 2005
The role of freezing in setting the latitudinal limits of mangrove forests Stuart, S. A.; Choat, B.; Martin, K. C. New Phytologist, Vol. 173, Issue 3 https://doi.org/10.1111/j.1469-8137.2006.01938.x	journal	November 2006
Testing the ‘rare pit’ hypothesis for xylem cavitation resistance in three species of Acer Christman, Mairgareth A.; Sperry, John S.; Adler, Frederick R. New Phytologist, Vol. 182, Issue 3 https://doi.org/10.1111/j.1469-8137.2009.02776.x	journal	April 2009
Freeze–thaw‐induced embolism in Pinus contorta : centrifuge experiments validate the ‘thaw‐expansion hypothesis’ but conflict with ultrasonic emission data Mayr, Stefan; Sperry, John S. New Phytologist, Vol. 185, Issue 4 https://doi.org/10.1111/j.1469-8137.2009.03133.x	journal	December 2009
Xylem traits mediate a trade‐off between resistance to freeze–thaw‐induced embolism and photosynthetic capacity in overwintering evergreens Choat, Brendan; Medek, Danielle E.; Stuart, Stephanie A. New Phytologist, Vol. 191, Issue 4 https://doi.org/10.1111/j.1469-8137.2011.03772.x	journal	May 2011
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
Toward Direct Measurement of Atmospheric Nucleation Kulmala, M.; Riipinen, I.; Sipila, M. Science, Vol. 318, Issue 5847 https://doi.org/10.1126/science.1144124	journal	August 2007
Vulnerability of Xylem to Cavitation and Embolism Tyree, M. T.; Sperry, J. S. Annual Review of Plant Physiology and Plant Molecular Biology, Vol. 40, Issue 1 https://doi.org/10.1146/annurev.pp.40.060189.000315	journal	June 1989
Apoplastic Water and Solute Movement: New Rules for an Old Space Canny, M. J. Annual Review of Plant Physiology and Plant Molecular Biology, Vol. 46, Issue 1 https://doi.org/10.1146/annurev.pp.46.060195.001243	journal	June 1995
The relationship between xylem conduit diameter and cavitation caused by freezing Davis, Stephen D.; Sperry, John S.; Hacke, Uwe G. American Journal of Botany, Vol. 86, Issue 10 https://doi.org/10.2307/2656919	journal	October 1999
The vulnerability to freezing-induced xylem cavitation of Larrea tridentata (Zygophyllaceae) in the Chihuahuan desert Martinez-Vilalta, J.; Pockman, W. T. American Journal of Botany, Vol. 89, Issue 12 https://doi.org/10.3732/ajb.89.12.1916	journal	December 2002
Embolized conduits of rice (Oryza sativa, Poaceae) refill despite negative xylem pressure Stiller, V.; Sperry, J. S.; Lafitte, R. American Journal of Botany, Vol. 92, Issue 12 https://doi.org/10.3732/ajb.92.12.1970	journal	December 2005

Cited By (12)

Elevational adaptation of morphological and anatomical traits by Sakhalin fir (Abies sachalinensis) Taneda, Haruhiko; Funayama-Noguchi, Sachiko; Mayr, Stefan Trees, Vol. 34, Issue 2 https://doi.org/10.1007/s00468-019-01932-4	journal	November 2019
Annual patterns of xylem embolism in high-yield apple cultivars Beikircher, Barbara; Mayr, Stefan Functional Plant Biology, Vol. 44, Issue 6 https://doi.org/10.1071/fp16048	journal	January 2017
Short-time xylem tension relaxation prevents vessel refilling and alleviates cryo-fixation artifacts in diffuse-porous Carpinus tschonoskii and Cercidiphyllum japonicum Ogasa, Mayumi Y.; Yazaki, Kenichi; Utsumi, Yasuhiro Tree Physiology, Vol. 39, Issue 10 https://doi.org/10.1093/treephys/tpz072	journal	June 2019
Variation of xylem vessel diameters across a climate gradient: insight from a reciprocal transplant experiment with a widespread boreal tree Schreiber, Stefan G.; Hacke, Uwe G.; Hamann, Andreas Functional Ecology, Vol. 29, Issue 11 https://doi.org/10.1111/1365-2435.12455	journal	April 2015
Plant xylem hydraulics: What we understand, current research, and future challenges: Plant xylem hydraulics Venturas, Martin D.; Sperry, John S.; Hacke, Uwe G. Journal of Integrative Plant Biology, Vol. 59, Issue 6 https://doi.org/10.1111/jipb.12534	journal	June 2017
Long-term stem CO ₂ concentration measurements in Norway spruce in relation to biotic and abiotic factors Etzold, Sophia; Zweifel, Roman; Ruehr, Nadine K. New Phytologist, Vol. 197, Issue 4 https://doi.org/10.1111/nph.12115	journal	January 2013
Moisture rivals temperature in limiting photosynthesis by trees establishing beyond their cold-edge range limit under ambient and warmed conditions Moyes, Andrew B.; Germino, Matthew J.; Kueppers, Lara M. New Phytologist, Vol. 207, Issue 4 https://doi.org/10.1111/nph.13422	journal	April 2015
Die hard: timberline conifers survive annual winter embolism Mayr, Stefan; Schmid, Peter; Beikircher, Barbara New Phytologist, Vol. 226, Issue 1 https://doi.org/10.1111/nph.16304	journal	November 2019
Anatomical regulation of ice nucleation and cavitation helps trees to survive freezing and drought stress Lintunen, A.; Hölttä, T.; Kulmala, M. Scientific Reports, Vol. 3, Issue 1 https://doi.org/10.1038/srep02031	journal	June 2013
The Widened Pipe Model of plant hydraulic evolution Koçillari, Loren; Olson, Mark E.; Suweis, Samir Proceedings of the National Academy of Sciences, Vol. 118, Issue 22 https://doi.org/10.1073/pnas.2100314118	journal	May 2021
Bursts of CO2 released during freezing offer a new perspective on avoidance of winter embolism in trees Lintunen, A.; Lindfors, L.; Kolari, P. Annals of Botany, Vol. 114, Issue 8 https://doi.org/10.1093/aob/mcu190	journal	September 2014
Cavitation and water fluxes driven by ice water potential inJuglans regiaduring freeze–thaw cycles Charra-Vaskou, Katline; Badel, Eric; Charrier, Guillaume Journal of Experimental Botany, Vol. 67, Issue 3 https://doi.org/10.1093/jxb/erv486	journal	November 2015

Similar Records

Electrical and seismic response of saline permafrost soil during freeze - Thaw transition

Journal Article · Wed Nov 01 00:00:00 EDT 2017 · Journal of Applied Geophysics · OSTI ID:1396108

Wu, Yuxin; Nakagawa, Seiji; Kneafsey, Timothy J.; +2 more

Numerical Study of Coupled Water and Vapor Flow, Heat Transfer, and Solute Transport in Variably-Saturated Deformable Soil During Freeze-Thaw Cycles

Journal Article · Thu Jul 27 00:00:00 EDT 2023 · Water Resources Research · OSTI ID:1396108

Huang, Xiang; Rudolph, David L.

Freeze-thaw durability of concrete: Ice formation process in pores

Journal Article · Tue Sep 01 00:00:00 EDT 1998 · Cement and Concrete Research · OSTI ID:1396108

Cai, H; Liu, X

Related Subjects

59 BASIC BIOLOGICAL SCIENCES
Biological Science

Title: Freeze/Thaw-Induced Embolism: Probability of Critical Bubble Formation Depends on Speed of Ice Formation

Citation Formats

References (56)

Cited By (12)

Similar Records

Related Subjects