title: Xylem Surfactants Introduce a New Element to the Cohesion-Tension Theory.
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.
authors.affiliation: Department of Biological Science, California State University, Fullerton, California 92831 (H.J.S., S.E., D.M.R., N.N., A.Y.T.D., J.M.M.); jschenk@fullerton.edu.|NanoAnalytical Laboratory, San Francisco, California 94118 (B.P.-S.); jschenk@fullerton.edu.|Department of Mechanical Engineering, University of Hawaii, Honolulu, Hawaii 96822 (J.Y., Y.Y.Z.); jschenk@fullerton.edu.|Laboratory of Plant Ecology, Department of Applied Ecology and Environmental Biology, Faculty of Bioscience Engineering, Ghent University, B-9000 Ghent, Belgium (K.S.); and jschenk@fullerton.edu.|Institute of Systematic Botany and Ecology, Ulm University, D-89081 Ulm, Germany (S.J.) jschenk@fullerton.edu.
authors.forename: H Jochen
authors.identifier: 0000-0001-6261-2780
authors.initials: HJ
authors.lastname: Schenk
authors.affiliation: Department of Biological Science, California State University, Fullerton, California 92831 (H.J.S., S.E., D.M.R., N.N., A.Y.T.D., J.M.M.).|NanoAnalytical Laboratory, San Francisco, California 94118 (B.P.-S.).|Department of Mechanical Engineering, University of Hawaii, Honolulu, Hawaii 96822 (J.Y., Y.Y.Z.).|Laboratory of Plant Ecology, Department of Applied Ecology and Environmental Biology, Faculty of Bioscience Engineering, Ghent University, B-9000 Ghent, Belgium (K.S.); and.|Institute of Systematic Botany and Ecology, Ulm University, D-89081 Ulm, Germany (S.J.).
authors.forename: Susana
authors.initials: S
authors.lastname: Espino
authors.affiliation: Department of Biological Science, California State University, Fullerton, California 92831 (H.J.S., S.E., D.M.R., N.N., A.Y.T.D., J.M.M.).|NanoAnalytical Laboratory, San Francisco, California 94118 (B.P.-S.).|Department of Mechanical Engineering, University of Hawaii, Honolulu, Hawaii 96822 (J.Y., Y.Y.Z.).|Laboratory of Plant Ecology, Department of Applied Ecology and Environmental Biology, Faculty of Bioscience Engineering, Ghent University, B-9000 Ghent, Belgium (K.S.); and.|Institute of Systematic Botany and Ecology, Ulm University, D-89081 Ulm, Germany (S.J.).
authors.forename: David M
authors.identifier: 0000-0003-3307-9416
authors.initials: DM
authors.lastname: Romo
authors.affiliation: Department of Biological Science, California State University, Fullerton, California 92831 (H.J.S., S.E., D.M.R., N.N., A.Y.T.D., J.M.M.).|NanoAnalytical Laboratory, San Francisco, California 94118 (B.P.-S.).|Department of Mechanical Engineering, University of Hawaii, Honolulu, Hawaii 96822 (J.Y., Y.Y.Z.).|Laboratory of Plant Ecology, Department of Applied Ecology and Environmental Biology, Faculty of Bioscience Engineering, Ghent University, B-9000 Ghent, Belgium (K.S.); and.|Institute of Systematic Botany and Ecology, Ulm University, D-89081 Ulm, Germany (S.J.).
authors.forename: Neda
authors.initials: N
authors.lastname: Nima
authors.affiliation: Department of Biological Science, California State University, Fullerton, California 92831 (H.J.S., S.E., D.M.R., N.N., A.Y.T.D., J.M.M.).|NanoAnalytical Laboratory, San Francisco, California 94118 (B.P.-S.).|Department of Mechanical Engineering, University of Hawaii, Honolulu, Hawaii 96822 (J.Y., Y.Y.Z.).|Laboratory of Plant Ecology, Department of Applied Ecology and Environmental Biology, Faculty of Bioscience Engineering, Ghent University, B-9000 Ghent, Belgium (K.S.); and.|Institute of Systematic Botany and Ecology, Ulm University, D-89081 Ulm, Germany (S.J.).
authors.forename: Aissa Y T
authors.initials: AY
authors.lastname: Do
authors.affiliation: Department of Biological Science, California State University, Fullerton, California 92831 (H.J.S., S.E., D.M.R., N.N., A.Y.T.D., J.M.M.).|NanoAnalytical Laboratory, San Francisco, California 94118 (B.P.-S.).|Department of Mechanical Engineering, University of Hawaii, Honolulu, Hawaii 96822 (J.Y., Y.Y.Z.).|Laboratory of Plant Ecology, Department of Applied Ecology and Environmental Biology, Faculty of Bioscience Engineering, Ghent University, B-9000 Ghent, Belgium (K.S.); and.|Institute of Systematic Botany and Ecology, Ulm University, D-89081 Ulm, Germany (S.J.).
authors.forename: Joseph M
authors.initials: JM
authors.lastname: Michaud
authors.affiliation: Department of Biological Science, California State University, Fullerton, California 92831 (H.J.S., S.E., D.M.R., N.N., A.Y.T.D., J.M.M.).|NanoAnalytical Laboratory, San Francisco, California 94118 (B.P.-S.).|Department of Mechanical Engineering, University of Hawaii, Honolulu, Hawaii 96822 (J.Y., Y.Y.Z.).|Laboratory of Plant Ecology, Department of Applied Ecology and Environmental Biology, Faculty of Bioscience Engineering, Ghent University, B-9000 Ghent, Belgium (K.S.); and.|Institute of Systematic Botany and Ecology, Ulm University, D-89081 Ulm, Germany (S.J.).
authors.forename: Brigitte
authors.initials: B
authors.lastname: Papahadjopoulos-Sternberg
authors.affiliation: Department of Biological Science, California State University, Fullerton, California 92831 (H.J.S., S.E., D.M.R., N.N., A.Y.T.D., J.M.M.).|NanoAnalytical Laboratory, San Francisco, California 94118 (B.P.-S.).|Department of Mechanical Engineering, University of Hawaii, Honolulu, Hawaii 96822 (J.Y., Y.Y.Z.).|Laboratory of Plant Ecology, Department of Applied Ecology and Environmental Biology, Faculty of Bioscience Engineering, Ghent University, B-9000 Ghent, Belgium (K.S.); and.|Institute of Systematic Botany and Ecology, Ulm University, D-89081 Ulm, Germany (S.J.).
authors.forename: Jinlong
authors.initials: J
authors.lastname: Yang
authors.affiliation: Department of Biological Science, California State University, Fullerton, California 92831 (H.J.S., S.E., D.M.R., N.N., A.Y.T.D., J.M.M.).|NanoAnalytical Laboratory, San Francisco, California 94118 (B.P.-S.).|Department of Mechanical Engineering, University of Hawaii, Honolulu, Hawaii 96822 (J.Y., Y.Y.Z.).|Laboratory of Plant Ecology, Department of Applied Ecology and Environmental Biology, Faculty of Bioscience Engineering, Ghent University, B-9000 Ghent, Belgium (K.S.); and.|Institute of Systematic Botany and Ecology, Ulm University, D-89081 Ulm, Germany (S.J.).
authors.forename: Yi Y
authors.identifier: 0000-0002-3992-3238
authors.initials: YY
authors.lastname: Zuo
authors.affiliation: Department of Biological Science, California State University, Fullerton, California 92831 (H.J.S., S.E., D.M.R., N.N., A.Y.T.D., J.M.M.).|NanoAnalytical Laboratory, San Francisco, California 94118 (B.P.-S.).|Department of Mechanical Engineering, University of Hawaii, Honolulu, Hawaii 96822 (J.Y., Y.Y.Z.).|Laboratory of Plant Ecology, Department of Applied Ecology and Environmental Biology, Faculty of Bioscience Engineering, Ghent University, B-9000 Ghent, Belgium (K.S.); and.|Institute of Systematic Botany and Ecology, Ulm University, D-89081 Ulm, Germany (S.J.).
authors.forename: Kathy
authors.initials: K
authors.lastname: Steppe
authors.affiliation: Department of Biological Science, California State University, Fullerton, California 92831 (H.J.S., S.E., D.M.R., N.N., A.Y.T.D., J.M.M.).|NanoAnalytical Laboratory, San Francisco, California 94118 (B.P.-S.).|Department of Mechanical Engineering, University of Hawaii, Honolulu, Hawaii 96822 (J.Y., Y.Y.Z.).|Laboratory of Plant Ecology, Department of Applied Ecology and Environmental Biology, Faculty of Bioscience Engineering, Ghent University, B-9000 Ghent, Belgium (K.S.); and.|Institute of Systematic Botany and Ecology, Ulm University, D-89081 Ulm, Germany (S.J.).
authors.forename: Steven
authors.identifier: 0000-0002-4476-5334
authors.initials: S
authors.lastname: Jansen
mesh_terms: D055592:Biophysical Phenomena; D005614:Freeze Fracturing; D005976:Glutaral / Q000737:chemistry; D019684:Magnoliopsida / Q000502:physiology* / Q000648:ultrastructure; D008954:Models, Biological; D053758:Nanoparticles / Q000737:chemistry / Q000648:ultrastructure; D009993:Osmium Tetroxide / Q000737:chemistry; D053147:Plant Exudates / Q000378:metabolism; D011312:Pressure; D013500:Surface Tension; D013501:Surface-Active Agents / Q000378:metabolism*; D052584:Xylem / Q000502:physiology* / Q000648:ultrastructure
chemical_list: D053147:Plant Exudates; D013501:Surface-Active Agents; D009993:Osmium Tetroxide; D005976:Glutaral