Synchrotron X-ray microtomography of xylem embolism in Sequoia sempervirens saplings during cycles of drought and recovery

New Phytologist

Volumn 205, Issue 3, 2015, Pages 1095-1105

  Choat, Brendan ^a   Brodersen, Craig R ^b   Mcelrone, Andrew J ^c,d  

^a WESTERN SYDNEY UNIVERSITY   (Australia)

^b Yale University   (United States)

^c AGRICULTURAL RESEARCH SERVICE   (United States)

^d UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Cavitation; Embolism; MicroCT; Redwood; Refilling; Sequoia; Xylem

Indexed keywords

DROUGHT RESISTANCE; FUNCTIONAL GROUP; PHOTOSYNTHESIS; SAPLING; TREE; WOODY PLANT; XYLEM;

SEQUOIA SEMPERVIRENS;

GAS; WATER;

AIR; DROUGHT; EVAPOTRANSPIRATION; GAS; MICRO-COMPUTED TOMOGRAPHY; PHYSIOLOGICAL STRESS; PHYSIOLOGY; PLANT STEM; SEQUOIA; SYNCHROTRON; TREE; XYLEM;

AIR; DROUGHTS; GASES; PLANT STEMS; PLANT TRANSPIRATION; SEQUOIA; STRESS, PHYSIOLOGICAL; SYNCHROTRONS; TREES; WATER; X-RAY MICROTOMOGRAPHY; XYLEM;

EID: 84920982428     PISSN: 0028646X     EISSN: 14698137     Source Type: Journal    
DOI: 10.1111/nph.13110     Document Type: Article

References (79)

1. Ameglio T, Ewers FW, Cochard H, Martignac M, Vandame M, Bodet C, Cruiziat P. 2001. Winter stem xylem pressure in walnut trees: effects of carbohydrates, cooling and freezing. Tree Physiology 21: 387-394.
2. Bailey IW. 1913. The preservative treatment of wood - II. The structure of the pit membranes in the tracheids of Cconifers and their relation to the penetration of Ggases, liquids, and finely divided solids into green and seasoned wood. Journal of Forestry 11: 12-20.
3. Briggs LJ. 1950. Limiting negative pressure of water. Journal of Applied Physics 21: 721-722.
4. Brodersen CR. 2013. Using high resolution computed tomography to visualize the three dimensional structure and function of plant vasculature. IAWA Journal 34: 408-424.
5. Brodersen CR, Choat B, Chatelet DS, Shackel KA, Matthews MA, McElrone AJ. 2013a. Xylem vessel relays contribute to radial connectivity in grapevine stems (Vitis vinifera and V. arizonica; Vitaceae). American Journal of Botany 100: 314-321.
6. Brodersen CR, McElrone AJ. 2013. Maintenance of xylem network transport capacity: a review of embolism repair in vascular plants. Frontiers in Plant Science 4: 108.
7. Brodersen CR, McElrone AJ, Choat B, Lee EF, Shackel KA, Matthews MA. 2013b. In vivo visualizations of drought-induced embolism spread in Vitis vinifera. Plant Physiology 161: 1820-1829.
8. 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.
9. Brodribb TJ, Bowman DMJS, Nichols S, Delzon S, Burlett R. 2010. Xylem function and growth rate interact to determine recovery rates after exposure to extreme water deficit. New Phytologist 188: 533-542.
10. Brodribb TJ, Cochard H. 2009. Hydraulic failure defines the recovery and point of death in water-stressed conifers. Plant Physiology 149: 575-584.
11. Burgess SSO, Dawson TE. 2004. The contribution of fog to the water relations of Sequoia sempervirens (D. Don): foliar uptake and prevention of dehydration. Plant, Cell & Environment 27: 1023-1034.
12. Burgess SSO, Pittermann J, Dawson TE. 2006. Hydraulic efficiency and safety of branch xylem increases with height in Sequoia sempervirens (D. Don) crowns. Plant, Cell & Environment 29: 229-239.
13. Canny MJ. 1997. Vessel contents during transpiration - embolisms and refilling. American Journal of Botany 84: 1223-1230.
14. Choat B. 2013. Predicting thresholds of drought-induced mortality in woody plant species. Tree Physiology 33: 669-671.
15. Choat B, Cobb AR, Jansen S. 2008. Structure and function of bordered pits: new discoveries and impacts on whole-plant hydraulic function. New Phytologist 177: 608-625.
16. Choat B, Drayton WM, Brodersen C, Matthews 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. Plant, Cell & Environment 33: 1502-1512.
17. 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.
18. Choat B, Jansen S, Zwieniecki MA, Smets E, Holbrook NM. 2004. Changes in pit membrane porosity due to deflection and stretching: the role of vestured pits. Journal of Experimental Botany 55: 1569-1575.
19. Choat B, Pittermann J. 2009. New insights into bordered pit structure and cavitation resistance in angiosperms and conifers. New Phytologist 182: 557-560.
20. Cobb AR, Choat B, Holbrook NM. 2007. Dynamics of freeze-thaw embolism in Smilax rotundifolia (Smilacaceae). American Journal of Botany 94: 640-649.
21. Debenedetti PG. 2013. Physics of water stretched to the limit. Nature Physics 9: 7-8.
22. Delzon S, Douthe C, Sala A, Cochard H. 2010. Mechanism of water-stress induced cavitation in conifers: bordered pit structure and function support the hypothesis of seal capillary-seeding. Plant, Cell & Environment 33: 2101-2111.
23. Dixon HH, Joly J. 1895. On the ascent of sap. Philosophical Transactions of the Royal Society of London B 186: 563-576.
24. Domec JC, Gartner BL. 2002. Age- and position-related changes in hydraulic versus mechanical dysfunction of xylem: inferring the design criteria for Douglas-fir wood structure. Tree Physiology 22: 91-104.
25. Domec JC, Lachenbruch B, Meinzer FC. 2006. Bordered pit structure and function determine spatial patterns of air-seeding thresholds in xylem of Douglas fir (Pseudotsuga menziesii; Pinaceae) trees. American Journal of Botany 93: 1588-1600.
26. Gregory SC, Petty JA. 1973. Valve action of bordered pits in conifers. Journal of Experimental Botany 24: 763-767.
27. Hacke UG, Sperry JS. 2003. Limits to xylem refilling under negative pressure in Laurus nobilis and Acer negundo. Plant, Cell & Environment 26: 303-311.
28. Hacke UG, Sperry JS, Pittermann J. 2004. Analysis of circular bordered pit function - II. Gymnosperm tracheids with torus-margo pit membranes. American Journal of Botany 91: 386-400.
29. Holbrook NM, Zwieniecki MA. 1999. Embolism repair and xylem tension: do we need a miracle? Plant Physiology 120: 7-10.
30. Jansen S, Lamy JB, Burlett R, Cochard H, Gasson P, Delzon S. 2012. Plasmodesmatal pores in the torus of bordered pit membranes affect cavitation resistance of conifer xylem. Plant, Cell & Environment 35: 1109-1120.
31. Johnson DM, McCulloh KA, Woodruff DR, Meinzer FC. 2012. Hydraulic safety margins and embolism reversal in stems and leaves: why are conifers and angiosperms so different? Plant Science 195: 48-53.
32. Johnstone JA, Dawson TE. 2010. Climatic context and ecological implications of summer fog decline in the coast redwood region. Proceedings of the National Academy of Sciences, USA 107: 4533-4538.
33. Kitin P, Fujii T, Abe H, Takata K. 2009. Anatomical features that facilitate radial flow across growth rings and from xylem to cambium in Cryptomeria japonica. Annals of Botany 103: 1145-1157.
34. Koran Z. 1977. Tangential pitting in black spruce tracheids. Wood Science and Technology 11: 115-123.
35. Laur J, Hacke UG. 2014. Exploring Picea glauca aquaporins in the context of needle water uptake and xylem refilling. New Phytologist 203: 388-400.
36. Limm EB, Simonin KA, Bothman AG, Dawson TE. 2009. Foliar water uptake: a common water acquisition strategy for plants of the redwood forest. Oecologia 161: 449-459.
37. Martorell S, Diaz-Espejo A, Medrano H, Ball MC, Choat B. 2014. Rapid hydraulic recovery in Eucalyptus pauciflora after drought: linkages between stem hydraulics and leaf gas exchange. Plant, Cell & Environment 37: 617-626.
38. Mauseth JD. 1988. Plant anatomy. California, CA, USA: Benjamin/Cummings Publishing Company.
39. Mayr S, Schmid P, Laur J, Rosner S, Charra-Vaskou K, Dämon B, Hacke UG. 2014. Uptake of water via branches helps timberline conifers refill embolized xylem in late winter. Plant Physiology 164: 1731-1740.
40. McCulloh KA, Johnson DM, Meinzer FC, Lachenbruch B. 2011. An annual pattern of native embolism in upper branches of four tall conifer species. American Journal of Botany 98: 1007-1015.
41. McCully ME. 1999. Root xylem embolisms and refilling. Relation to water potentials of soil, roots, and leaves, and osmotic potentials of root xylem sap. Plant Physiology 119: 1001-1008.
42. 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.
43. McElrone AJ, Brodersen CR, Alsina MM, Drayton WM, Matthews MA, Shackel KA, Wada H, Zufferey V, Choat B. 2012. Centrifuge technique consistently overestimates vulnerability to water stress-induced cavitation in grapevines as confirmed with high-resolution computed tomography. New Phytologist 196: 661-665.
44. 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. Journal of Visualized Experiments 74: doi: 10.3791/50162.
45. Melcher PJ, Meinzer FC, Yount DE, Goldstein G, Zimmermann U. 1998. Comparative measurements of xylem pressure in transpiring and non-transpiring leaves by means of the pressure chamber and the xylem pressure probe. Journal of Experimental Botany 49: 1757-1760.
46. Milburn JA. 1973. Cavitation studies on whole ricinus plants by acoustic detection. Planta 112: 333-342.
47. Nardini A, Lo Gullo MA, Salleo S. 2011. Refilling embolized xylem conduits: is it a matter of phloem unloading? Plant Science 180: 604-611.
48. Oertli JJ. 1971. Stability of water under tension in xylem. Zeitschrift Fur Pflanzenphysiologie 65: 195-209.
49. Pammenter NW, Vander Willigen C. 1998. A mathematical and statistical analysis of the curves illustrating vulnerability of xylem to cavitation. Tree Physiology 18: 589-593.
50. Pickard WF. 1981. The ascent of sap in plants. Progress in Biophysics & Molecular Biology 37: 181-229.
51. Pittermann J, Choat B, Jansen S, Stuart SA, Lynn L, Dawson TE. 2010. The relationships between xylem safety and hydraulic efficiency in the Cupressaceae: the evolution of pit Membrane form and function. Plant Physiology 153: 1919-1931.
52. Pittermann J, Sperry JS, Hacke UG, Wheeler JK, Sikkema EH. 2005. Torus-margo pits help conifers compete with angiosperms. Science 310: 1924.
53. Pockman WT, Sperry JS, Oleary JW. 1995. Sustained and significant negative water-pressure in xylem. Nature 378: 715-716.
54. Ponomarenko A, Vincent O, Pietriga A, Cochard H, Badel É, Marmottant P. 2014. Ultrasonic emissions reveal individual cavitation bubbles in water-stressed wood. Journal of the Royal Society Interface 11: 20140480.
55. Salleo S, Lo Gullo MA, Trifilo P, Nardini A. 2004. 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 & Environment 27: 1065-1076.
56. Salleo S, LoGullo MA, DePaoli D, Zippo M. 1996. Xylem recovery from cavitation-induced embolism in young plants of Laurus nobilis: a possible mechanism. New Phytologist 132: 47-56.
57. Siau JF. 1984. Transport processes in wood. Berlin, Germany: Springer-Verlag.
58. Simonin KA, Santiago LS, Dawson TE. 2009. Fog interception by Sequoia sempervirens (D. Don) crowns decouples physiology from soil water deficit. Plant, Cell & Environment 32: 882-892.
59. Sobrado MA, Grace J, Jarvis PG. 1992. The limits to xylem embolism recovery in Pinus sylvestris L. Journal of Experimental Botany 43: 831-836.
60. Sperry JS, Holbrook NM, Zimmermann MH, Tyree MT. 1987. Spring filling of xylem vessels in wild grapevine. Plant Physiology 83: 414-417.
61. Sperry JS, Nichols KL, Sullivan JEM, Eastlack SE. 1994. Xylem embolism in ring-porous, diffuse-porous, and coniferous trees of northern Utah and interior Alaska. Ecology 75: 1736-1752.
62. Sperry JS, Tyree MT. 1988. Mechanism of water stress-induced xylem embolism. Plant Physiology 88: 581-587.
63. Sperry JS, Tyree MT. 1990. Water stress-induced xylem embolism in 3 species of conifers. Plant, Cell & Environment 13: 427-436.
64. Stiller V, Sperry JS, Lafitte R. 2005. Embolized conduits of rice (Oryza sativa, Poaceae) refill despite negative xylem pressure. American Journal of Botany 92: 1970-1974.
65. Tyree MT, Salleo S, Nardini A, Lo Gullo MA, Mosca R. 1999. Refilling of embolized vessels in young stems of laurel. Do we need a new paradigm? Plant Physiology 120: 11-21.
66. Tyree MT, Sperry JS. 1989. Vulnerability of xylem to cavitation and embolism. Annual Review of Plant Physiology and Plant Molecular Biology 40: 19-38.
67. Tyree MT, Zimmermann MH. 2002. Xylem structure and the ascent of sap. New York, NY, USA: Springer-Verlag.
68. Urli M, Porte 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.
69. Utsumi Y, Sano Y, Funada R, Ohtani J, Fujikawa S. 2003. Seasonal and perennial changes in the distribution of water in the sapwood of conifers in a sub-frigid zone. Plant Physiology 131: 1826-1833.
70. Wei CF, Tyree MT, Steudle E. 1999. Direct measurement of xylem pressure in leaves of intact maize plants. A test of the cohesion-tension theory taking hydraulic architecture into consideration. Plant Physiology 121: 1191-1205.
71. 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. Plant, Cell & Environment 36: 1938-1949.
72. Wheeler TD, Stroock AD. 2008. The transpiration of water at negative pressures in a synthetic tree. Nature 455: 208-212.
73. Zhang C, Fujita M, Takabe K. 2003. Contact and non-contact proportions between axial elements and rays. IAWA Journal 24: 247-255.
74. Zheng Q, Durben DJ, Wolf GH, Angell CA. 1991. Liquids at large negative pressures - water at the homogeneous nucleation limit. Science 254: 829-832.
75. Zimmermann MH. 1983. Xylem structure and the ascent of sap. New York, NY, USA: Springer-Verlag.
76. Zimmermann MH, Brown CL. 1971. Trees: structure and function. New York, NY, USA; Berlin, Heidelberg, Germany: Springer-Verlag.
77. Zwieniecki MA, Holbrook NM. 2000. Bordered pit structure and vessel wall surface properties. implications for embolism repair. Plant Physiology 123: 1015-1020.
78. Zwieniecki MA, Holbrook NM. 2009. Confronting Maxwell's demon: biophysics of xylem embolism repair. Trends in Plant Science 14: 530-534.
79. Zwieniecki MA, Melcher PJ, Ahrens ET. 2013. Analysis of spatial and temporal dynamics of xylem refilling in Acer rubrum L. using magnetic resonance imaging. Frontiers in Plant Science 4: 265.