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Xylem surfactants introduce a new element to the cohesion-tension theory

H Jochen Schenk, Susana Espino, David M Romo, Neda Nima, Aissa YT Do, Joseph M Michaud, Brigitte Papahadjopoulos-Sternberg, Jinlong Yang, Yi Y Zuo, Kathy Steppe UGent, et al. (2017) PLANT PHYSIOLOGY. 173(2). p.1177-1196
abstract
Vascular plants transport water under negative pressure without constantly creating gas bubbles that would disable their hydraulic systems. Attempts to replicate this feat in artificial systems almost invariably result in bubble formation, except under highly controlled conditions with pure water and only hydrophilic surfaces present. In theory, conditions in the xylem should favor bubble nucleation even more: there are millions of conduits with at least some hydrophobic surfaces, and xylem sap is saturated or sometimes supersaturated with atmospheric gas and may contain surface-active molecules that can lower surface tension. So how do plants transport water under negative pressure? Here, we show that angiosperm xylem contains abundant hydrophobic surfaces as well as insoluble lipid surfactants, including phospholipids, and proteins, a composition similar to pulmonary surfactants. Lipid surfactants were found in xylem sap and as nanoparticles under transmission electron microscopy in pores of intervessel pit membranes and deposited on vessel wall surfaces. Nanoparticles observed in xylem sap via nanoparticle-tracking analysis included surfactant-coated nanobubbles when examined by freeze-fracture electron microscopy. Based on their fracture behavior, this technique is able to distinguish between dense-core particles, liquid-filled, bilayer-coated vesicles/liposomes, and gas-filled bubbles. Xylem surfactants showed strong surface activity that reduces surface tension to low values when concentrated as they are in pit membrane pores. We hypothesize that xylem surfactants support water transport under negative pressure as explained by the cohesion-tension theory by coating hydrophobic surfaces and nanobubbles, thereby keeping the latter below the critical size at which bubbles would expand to form embolisms.
Please use this url to cite or link to this publication:
author
organization
year
type
journalArticle (original)
publication status
published
subject
keyword
INTERVESSEL PIT MEMBRANE, IN-VIVO VISUALIZATIONS, GAS CAVITATION NUCLEI, X-RAY MICROTOMOGRAPHY, PULMONARY SURFACTANT, ELECTRON-MICROSCOPY, PHOSPHOLIPASE-D, WATER-STRESS, GLYCINE-MAX, NEGATIVE PRESSURES
journal title
PLANT PHYSIOLOGY
Plant Physiol.
volume
173
issue
2
pages
1177 - 1196
Web of Science type
Article
Web of Science id
000394140800020
ISSN
0032-0889
1532-2548
DOI
10.1104/pp.16.01039
language
English
UGent publication?
yes
classification
A1
copyright statement
I have transferred the copyright for this publication to the publisher
id
8524267
handle
http://hdl.handle.net/1854/LU-8524267
date created
2017-06-19 20:24:19
date last changed
2017-07-03 10:45:12
@article{8524267,
  abstract     = {Vascular plants transport water under negative pressure without constantly creating gas bubbles that would disable their hydraulic systems. Attempts to replicate this feat in artificial systems almost invariably result in bubble formation, except under highly controlled conditions with pure water and only hydrophilic surfaces present. In theory, conditions in the xylem should favor bubble nucleation even more: there are millions of conduits with at least some hydrophobic surfaces, and xylem sap is saturated or sometimes supersaturated with atmospheric gas and may contain surface-active molecules that can lower surface tension. So how do plants transport water under negative pressure? Here, we show that angiosperm xylem contains abundant hydrophobic surfaces as well as insoluble lipid surfactants, including phospholipids, and proteins, a composition similar to pulmonary surfactants. Lipid surfactants were found in xylem sap and as nanoparticles under transmission electron microscopy in pores of intervessel pit membranes and deposited on vessel wall surfaces. Nanoparticles observed in xylem sap via nanoparticle-tracking analysis included surfactant-coated nanobubbles when examined by freeze-fracture electron microscopy. Based on their fracture behavior, this technique is able to distinguish between dense-core particles, liquid-filled, bilayer-coated vesicles/liposomes, and gas-filled bubbles. Xylem surfactants showed strong surface activity that reduces surface tension to low values when concentrated as they are in pit membrane pores. We hypothesize that xylem surfactants support water transport under negative pressure as explained by the cohesion-tension theory by coating hydrophobic surfaces and nanobubbles, thereby keeping the latter below the critical size at which bubbles would expand to form embolisms.},
  author       = {Schenk, H Jochen and Espino, Susana and Romo, David M and Nima, Neda and Do, Aissa YT and Michaud, Joseph M and Papahadjopoulos-Sternberg, Brigitte and Yang, Jinlong and Zuo, Yi Y and Steppe, Kathy and Jansen, Steven},
  issn         = {0032-0889},
  journal      = {PLANT PHYSIOLOGY},
  keyword      = {INTERVESSEL PIT MEMBRANE,IN-VIVO VISUALIZATIONS,GAS CAVITATION NUCLEI,X-RAY MICROTOMOGRAPHY,PULMONARY SURFACTANT,ELECTRON-MICROSCOPY,PHOSPHOLIPASE-D,WATER-STRESS,GLYCINE-MAX,NEGATIVE PRESSURES},
  language     = {eng},
  number       = {2},
  pages        = {1177--1196},
  title        = {Xylem surfactants introduce a new element to the cohesion-tension theory},
  url          = {http://dx.doi.org/10.1104/pp.16.01039},
  volume       = {173},
  year         = {2017},
}

Chicago
Schenk, H Jochen, Susana Espino, David M Romo, Neda Nima, Aissa YT Do, Joseph M Michaud, Brigitte Papahadjopoulos-Sternberg, et al. 2017. “Xylem Surfactants Introduce a New Element to the Cohesion-tension Theory.” Plant Physiology 173 (2): 1177–1196.
APA
Schenk, H. J., Espino, S., Romo, D. M., Nima, N., Do, A. Y., Michaud, J. M., Papahadjopoulos-Sternberg, B., et al. (2017). Xylem surfactants introduce a new element to the cohesion-tension theory. PLANT PHYSIOLOGY, 173(2), 1177–1196.
Vancouver
1.
Schenk HJ, Espino S, Romo DM, Nima N, Do AY, Michaud JM, et al. Xylem surfactants introduce a new element to the cohesion-tension theory. PLANT PHYSIOLOGY. 2017;173(2):1177–96.
MLA
Schenk, H Jochen, Susana Espino, David M Romo, et al. “Xylem Surfactants Introduce a New Element to the Cohesion-tension Theory.” PLANT PHYSIOLOGY 173.2 (2017): 1177–1196. Print.