Visualizing water-filled versus embolized status of xylem conduits by desktop x-ray microtomography

Plant Methods

Ritva Serimaa²  Kurt Fagerstedt³  Marko Peura¹  Jussi-Petteri Suuronen² 

[1] Present address: Central Administration, University of Helsinki, P.O.B. 33, Helsinki, FI-00014, Finland;Department of Physics, University of Helsinki, P.O.B. 64, Helsinki, FI-00014, Finland;Department of Biosciences, University of Helsinki, P.O.B. 65, Helsinki, FI-00014, Finland

关键词: Tomography;    Birch;    Cavitation;    Xylem;   

Others  :  820540
DOI  :  10.1186/1746-4811-9-11

 received in 2013-01-22, accepted in 2013-03-22,  发布年份 2013

【 摘 要 】

Background

The hydraulic conductivity of the stem is a major factor limiting the capability of trees to transport water from the soil to transpiring leaves. During drought conditions, the conducting capacity of xylem can be reduced by some conduits being filled with gas, i.e. embolized. In order to understand the dynamics of embolism formation and repair, considerable attention has been given to developing reliable and accurate methods for quantifying the phenomenon. In the past decade, non-destructive imaging of embolism formation in living plants has become possible. Magnetic resonance imaging has been used to visualize the distribution of water within the stem, but in most cases it is not possible to resolve individual cells. Recently, high-resolution synchrotron x-ray microtomography has been introduced as a tool to visualize the water contents of individual cells in vivo, providing unprecedented insight into the dynamics of embolism repair. We have investigated the potential of an x-ray tube -based microtomography setup to visualize and quantify xylem embolism and embolism repair in water-stressed young saplings and shoot tips of Silver and Curly birch (Betula pendula and B. pendula var. carelica).

Results

From the microtomography images, the water-filled versus gas-filled status of individual xylem conduits can be seen, and the proportion of stem cross-section that consists of embolized tissue can be calculated. Measuring the number of embolized vessels in the imaged area is a simple counting experiment. In the samples investigated, wood fibers were cavitated in a large proportion of the xylem cross-section shortly after watering of the plant was stopped, but the number of embolized vessels remained low several days into a drought period. Under conditions of low evaporative demand, also refilling of previously embolized conduits was observed.

Conclusions

Desktop x-ray microtomography is shown to be an effective method for evaluating the water-filled versus embolized status of the stem xylem in a small living sapling. Due to its non-destructive nature, the risk of inducing embolisms during sampling is greatly reduced. Compared with synchrotron imaging beamlines, desktop microtomography offers easier accessibility, while maintaining sufficient resolution to visualize the water contents of individual cells.

【 授权许可】

   
2013 Suuronen et al.; licensee BioMed Central Ltd.

【 图 表 】

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【 参考文献 】

• [1]Pallardy SG: Physiology of woody plants. 3rd edition. New York: Academic; 2008.
• [2]Taiz L, Zeiger E: Plant Physiology. 3rd edition. Sunderland, Mass: Sinauer Associates Inc; 2002.
• [3]Holbrook NM, Zwieniecki MA: The Dynamics of “Dead Wood”: Maintenance of Water Transport Through Plant Stems. Integr Comp Biol 2002, 42:492-496.
• [4]Sperry JS, Nichols KL, Sullivan JEM, Eastlack SE: Xylem embolism in ring-porous, diffuse-porous, and coniferous trees of northern Utah and interior Alaska. Ecology 1994, 75(6):1736-1752.
• [5]Holbrook NM, Zwieniecki MA: Embolism Repair and Xylem Tension: Do We Need a Miracle? Plant Physiol 1999, 120:7-10.
• [6]Salleo S, Lo Gullo MA, Trifilò P, Nardini A: New evidence for a role of vessel-associated cells and phloem in the rapid xylem refilling of cavitated stems of Laurus nobilis L. Plant Cell Environ 2004, 27:1065-1076.
• [7]Nardini A, Lo Gullo MA, Salleo S: Refilling embolized xylem conduits: Is it a matter of phloem unloading? Plant Sci 2011, 180:604-611.
• [8]Canny MJ: Vessel contents during transpiration — embolisms and refilling. Am J Bot 1997, 84(9):1223-1230.
• [9]Pate JS, Canny MJ: Quantification of vessel embolisms by direct observation: a comparison of two methods. New Phytol 1999, 141:33-44.
• [10]Ogasa M, Miki N, Yoshikawa K: Changes of hydraulic conductivity during dehydration and rehydration in Quercus serrata thunb. and Betula platyphylla var. japonica hara: the effect of xylem structures. Tree Physiol 2010, 30:608-617.
• [11]Mayr S, Zublasing V: Ultrasonic emissions from conifer xylem exposed to repeated freezing. J Plant Physiol 2010, 167:34-40.
• [12]Johnson DM, McCulloh KA, Woodruff DR, Meinzer FC: Evidence for xylem embolism as a primary factor in dehydration-induced declines in leaf hydraulic conductance. Plant Cell Environ 2012, 35:760-769.
• [13]Sano Y, Okamura Y, Utsumi Y: Visualizing water-conducting pathways of living trees: selection of dyes and tissue preparation methods. Tree Physiol 2005, 25:269-275.
• [14]Canny MJ, Huang CX, McCully ME: The cohesion theory debate continues. Trends Plant Sci 2001, 6(10):454-455.
• [15]Cochard H, Ameglio T, Cruiziat P: The cohesion theory debate continues. Trends Plant Sci 2001, 6(10):456.
• [16]Richter H: The cohesion theory debate continues: the pitfalls of cryobiology. Trends Plant Sci 2001, 6(10):456-457.
• [17]Holbrook NM, Ahrens ET, Burns MJ, Zwieniecki MA: In Vivo Observation of Cavitation and Embolism Repair Using Magnetic Resonance Imaging. Plant Physiol 2001, 126:27-31.
• [18]Clearwater MJ, Clark CJ: In vivo magnetic resonance imaging of xylem vessel contents in woody lianas. Plant Cell Environ 2003, 26:1205-1214.
• [19]Scheenen TWJ, Vergeld FJ, Heemskerk AM, Van As H: Intact plant magnetic resonance imaging to study dynamics in long-distance sap flow and flow-conducting surface area. Plant Physiol 2007, 144:1157-1165.
• [20]Lee S, Kim Y: In vivo visualization of the water-refilling process in xylem vessels using x-ray micro-imaging. Ann Bot 2008, 101(4):595-602.
• [21]Brodersen CR, McElrone AJ, Choat B, Matthews MA, Shackel KA: The dynamics of embolism repair in xylem: In vivo visualizations using high-resolution computed tomography. Plant Physiol 2010, 154:1088-1095.
• [22]Steppe K, Cnudde V, Girard C, Lemeur R, Cnudde J-P, Jacobs P: Use of X-ray computed microtomography for non-invasive determination of wood anatomical characteristics. J Struct Biol 2004, 148:11-21.
• [23]Van den Bulcke J, Boone M, Van Acker J, Stevens M, Van Hoorebecke L: X-ray tomography as a tool for detailed anatomical analysis. Ann For Sci 2009, 66:508.
• [24]Jenneson PM, Gilboy WB, Morton EJ, Gregory PJ: An X-ray micro-tomography system optimised for the low-dose study of living organisms. Appl Radiat Isot 2003, 58:177-181.
• [25]Dhondt S, Vanhaeren H, Van Loo D, Cnudde V, Inzé D: Plant structure visualization by high-resolution X-ray computed tomography. Trends Plant Sci 2010, 15(8):419-422.
• [26]Tyree MT, Ewers FW: The hydraulic architecture of trees and other woody plants. New Phytol 1991, 119:345-360.
• [27]Meinzer FC, Johnson DM, Lachenbruch B, McCulloh KA, Woodruff DR: Xylem hydraulic safety margins in woody plants: coordination of stomatal control of xylem tension with hydraulic capacitance. Funct Ecol 2009, 23:922-930.
• [28]Scholz FG, Phillips NG, Bucci SJ, Meinzer FC, Goldstein G: Hydraulic capacitance: biophysics and functional significance of internal water sources in relation to tree size. In Size- and Age-Related Changes in Tree Structure and Function. Edited by Meinzer FC, Lachenbruch B, Dawson TE. Dordrecht: Springer; 2011:341-361.
• [29]Alexakhin RM, Karaban RT, Prister BS, Spirin DA, Romanov GN, Mishenkov MN, Spiridinov SI, Fesenko SV, Fyodorov Ye A, Tikhomirov FA: The effects of acute irradiation on the forest biogeocenosis; experimental data, model and practical applications for accidental cases. Sci Total Environ 1994, 157:357-369.
• [30]United Nations Scientific Committee on the Effects of Atomic Radiation (UNSCEAR): Sources and effects of ionizing radiation, scientific annex to the 1996 report to the General Assembly . New York: ; 1996:20-25.
• [31]Feldkamp LA, Davis LC, Kress JW: Practical cone-beam algorithm. J Opt Soc Am 1984, 1(6):612-619.
• [32]Stock SR: Microcomputed Tomography: Methodology and Applications. Boca Raton, FL: CRC Press; 2009.
• [33]Gonzalez RC, Woods RE: Digital Image Processing. 3rd edition. New Jersey: Pearson Education Inc.; 2008.
• [34]Tomasi C, Manduchi R: Bilateral filtering for gray and color images. In Proceedings of the 6th International Conference on Computer Vision: 4-7 January 1998; Bombay. Edited by IEEE. : ; 1998:839-846.