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

(2017) PLANT PHYSIOLOGY. 173(2). p.1177-1196
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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.
Keywords
INTERVESSEL PIT MEMBRANE, IN-VIVO VISUALIZATIONS, GAS CAVITATION NUCLEI, X-RAY MICROTOMOGRAPHY, PULMONARY SURFACTANT, ELECTRON-MICROSCOPY, PHOSPHOLIPASE-D, WATER-STRESS, GLYCINE-MAX, NEGATIVE PRESSURES

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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.
@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},
}

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