Skip to main content
PMC home page
Journal of Biological Physics logoLink to Journal of Biological Physics
. 2005 Jan;31(1):57–71. doi: 10.1007/s10867-005-6094-0

The Significance of Pit Shape for Hydraulic Isolation of Embolized Conduits of Vascular Plants During Novel Refilling

W Konrad 1, A Roth-Nebelsick 1,✉
PMCID: PMC3482091  PMID: 23345884

Abstract

During plant water transport, the water in the conducting tissue (xylem) is under tension. The system is then in a metastable state and prone to bubble development and subsequent embolism blocking further water transport. It has recently been demonstrated, that embolism can be repaired under tension (= novel refilling). A model (Pit Valve Mechanism = PVM) has also been suggested which is based on the development of a special meniscus in the pores (pits) between adjacent conduits. This meniscus is expected to be able to isolate embolized conduits from neighbouring conduits during embolism repair. In this contribution the stability of this isolating meniscus against perturbations is considered which inevitably occur in natural environments. It can be shown that pit shape affects the stability of PVM fundamentally in the case of perturbation. The results show that a concave pit shape significantly supports the stability of PVM. Concave pit shape should thus be of selective value for species practicing novel refilling.

Full Text

The Full Text of this article is available as a PDF (732.4 KB).

References

  • 1.Tyree M.T., Ewers F. The Hydraulic Architecture of Trees and Other Woody Plants. New Phytol. 1991;199:345–360. [Google Scholar]
  • 2.Zimmermann M.H. Xylem Structure and the Ascent of Sap. Berlin: Springer-Verlag; 1983. [Google Scholar]
  • 3.Holbrook N.M., Ahrens E.T., Burns M.J., Zwieniecki M.A. In Vivo Observation of Cavitation and Embolism Repair Using Magnetic Resonance Imaging. Plant Physiol. 2001;126:27–31. doi: 10.1104/pp.126.1.27. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 4.Pickard W.F. The Ascent of Sap in Plants. Prog. Biophys. Mol. Biol. 1981;37:181–229. doi: 10.1016/0079-6107(82)90023-2. [DOI] [Google Scholar]
  • 5.Pockman W.T., Sperry J.S., O’Leary J.W. Sustained and Significant Negative Water Pressure in Xylem. Nature. 1995;378:715–716. doi: 10.1038/378715a0. [DOI] [Google Scholar]
  • 6.Milburn J.A. Cavitation and Embolisms in Xylem Conduits. In: Raghavendra A.S., editor. Physiology of Trees. New York: Wiley; 1991. pp. 163–174. [Google Scholar]
  • 7.Tyree M.T., Sperry J.S. The Vulnerability of Xylem to Cavitation and Embolism. Annu. Rev. Plant Physiol., Plant Mol. Biol. 1989;40:19–38. [Google Scholar]
  • 8.Tyree M.T., Yang S. Water-Storage Capacity of Thuja, Tsuga and Acer Stems Measured by Dehydration Isotherms: The Contribution of Capillary Water and Cavitation. Planta. 1990;182:420–426. doi: 10.1007/BF02411394. [DOI] [PubMed] [Google Scholar]
  • 9.Hölttä T., Vesala T., Perämäki M., Nikinmaa E. Relationships Between Embolism, Stem Water Tension and Diameter Changes. J. Theor. Biol. 2002;215:23–38. doi: 10.1006/jtbi.2001.2485. [DOI] [PubMed] [Google Scholar]
  • 10.Sperry J.S., Tyree M.T. Mechanism of Water Stress-Induced Xylem Embolism. Plant Physiol. 1988;88:581–587. doi: 10.1104/pp.88.3.581. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 11.Bucci S.J., Scholz F.G., Goldstein G., Meinzer F.C., Sternberg L., Da S.L. Dynamic Changes in Hydraulic Conductivity in Petioles of Two Savanna Tree Species: Factors and Mechanisms Contributing to the Refilling of Embolized Vessels. Plant Cell Environ. 2003;26:1633–1645. doi: 10.1046/j.0140-7791.2003.01082.x. [DOI] [Google Scholar]
  • 12.Hacke U.G., Sperry J.S. Limits to Xylem Refilling Under Negative Pressure in Laurus nobilis and Acer negundo. Plant Cell Environ. 2003;26:303–311. doi: 10.1046/j.1365-3040.2003.00962.x. [DOI] [Google Scholar]
  • 13.Salleo S., LoGullo M., Depaoli M., Zippo M. Xylem Recovery from Cavitation-Induced Embolism in Young Plants of Laurus nobilis: A Possible Mechanism. New Phytol. 1996;132:47–56. doi: 10.1111/j.1469-8137.1996.tb04507.x. [DOI] [PubMed] [Google Scholar]
  • 14.Tyree M.T., Salleo S., Nardini A., LoGullo M.A., Mosca R. Refilling of Embolized Vessels in Young Stems of Laurel: Do We Need a New Paradigm? Plant Physiol. 1999;120:11–21. doi: 10.1104/pp.120.1.11. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 15.Steudle E. The Cohesion-Tension Mechanism and the Acquisition of Water by Plant Roots. Annu. Rev. Plant Physiol., Plant Mol. Biol. 2001;52:847–875. doi: 10.1146/annurev.arplant.52.1.847. [DOI] [PubMed] [Google Scholar]
  • 16.Vesala T., Hölttä T., Perämäki M., Nikinmaa E. Refilling of a Hydraulically Isolated Embolized Xylem Vessel: Model Calculations. Ann. Bot. 2003;91:419–428. doi: 10.1093/aob/mcg022. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 17.Holbrook N.M., Zwieniecki M.A. Embolism Repair and Xylem Tension. Do we need a Miracle? Plant Physiol. 1999;120:7–10. doi: 10.1104/pp.120.1.7. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 18.Konrad W., Roth-Nebelsick A.The Dynamics of Gas Bubbles in Conduits of Vascular Plants and Implications for Embolism Repair J. Theor. Biol. 200322443–61. 10.1016/S0022-5193(03)00138-3MR2069248 [DOI] [PubMed] [Google Scholar]
  • 19.Shen F., Gao R., Liu W., Zhang W. Physical Analysis of the Process of Cavitation in Xylem Sap. Tree Physiol. 2002;22:655–659. doi: 10.1093/treephys/22.9.655. [DOI] [PubMed] [Google Scholar]
  • 20.Wheeler E.A. Intervascular Pit Membranes in Ulmus and Celtis Native to the United States. IAWA Bulletin. 1983;4:79–88. [Google Scholar]
  • 21.Hacke U.G., Stiller V., Sperry J.S., Pittermann J., McCulloh K.A. Cavitation Fatigue. Embolism and Refilling Cycles Can Weaken the Cavitation Resistance of Xylem. Plant Physiology. 2001;125:779–786. doi: 10.1104/pp.125.2.779. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 22.Carlquist S. Comparative Wood Anatomy. Heidelberg, New York: Berlin; 2001. [Google Scholar]
  • 23.Cochard H., Ewers F., Tyree M.T. Water Relations of a Tropical Vinelike Bamboo (Rhipidocladum racemiflorum): Root Pressures, Vulnerability to Cavitation and Seasonal Changes in Embolism. J. Exp. Bot. 1994;45:1085–1089. [Google Scholar]
  • 24.Ewers F.W., Fisher J.B., Fichtner K. Water Flux and Xylem Structure in Vines. In: Putz F.E., Mooney H.A., editors. The Biology of Vines. Cambridge: Cambridge University Press; 1991. pp. 127–160. [Google Scholar]
  • 25.Fisher J.B., Angeles G., Ewers F.W., Lopez-Portillo J. Survey of Root Pressure in Tropical Vines and Woody Species. Int. J. Plant Sci. 1997;158:44–50. doi: 10.1086/297412. [DOI] [Google Scholar]
  • 26.Lösch R. Wasserhaushalt der Pflanzen. Wiebelsheim: Quelle und Meyer; 2001. [Google Scholar]
  • 27.Magnani F., Borghetti M. Interpretation of Seasonal Changes of Xylem Embolism and Plant Hydraulic Resistance. Plant Cell Environ. 1995;18:689–696. [Google Scholar]
  • 28.Tyree M.T., Fiscus E.L., Wullschleger S.D., Dixon M.A. Detection of Xylem Cavitation in Corn Under Field Conditions. Plant Physiol. 1986;82:597–599. doi: 10.1104/pp.82.2.597. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 29.Yang S., Tyree M.T. A Theoretical Model of Hydraulic Conductivity Recovery From Embolism With Comparison to Experimental Data on Acer saccharum. Plant Cell Environ. 1992;15:633–643. [Google Scholar]
  • 30.Zwieniecki M.A., Holbrook N.M. Bordered Pit Structure and Vessel Wall Surface Properties. Implications for Embolism Repair. Plant Physiol. 2000;123:1015–1020. doi: 10.1104/pp.123.3.1015. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 31.Zwieniecki M.A., Melcher P.J., Holbrook N.M. Hydraulic Properties of Individual Xylem Vessels of Fraxinus americana. J. Exp. Bot. 2001;52:257–264. doi: 10.1093/jexbot/52.355.257. [DOI] [PubMed] [Google Scholar]

Articles from Journal of Biological Physics are provided here courtesy of Springer Science+Business Media B.V.

RESOURCES