Beyond air-seeding: Dynamic, multiphase interactions reveal a two-step mechanism of embolism propagation in angiosperm xylem
bioRxiv (Cold Spring Harbor Laboratory)
Abstract
Abstract Background The mechanism underlying drought-induced embolism in angiosperm xylem has been attributed to air-seeding. This concept describes the bulk flow of gas from embolised to neighbouring conduits through the penetration of gas-liquid menisci across pores in interconduit pit membranes. While there is compelling evidence for the spatial propagation of embolism, air-seeding rests on various simplifying assumptions. Among others, air-seeding presumes that xylem sap has physical properties comparable to pure water, that pit membranes can be approximated as structures with simple pores, and that embolism occurs whenever a gas-liquid interface crosses a pit membrane. Scope Recent experimental and theoretical work demonstrates that the biophysical conditions and processes governing gas-liquid interactions at interconduit pit membranes are fundamentally more dynamic and complex than assumed by air-seeding. These phenomena include: (1) gas movement through constriction pore networks, (2) insoluble, polar lipids at conduit surfaces and interfaces, (3) dynamic surface tension of xylem sap that depends on the local packing density of interfacial lipids, (4) bubble snap-off dynamics within pit membranes, (5) surfactant-stabilized nanobubbles in sap that is oversaturated with dissolved gas, and (6) electrostatic interactions between charged interfaces. Importantly, embolism propagation involves bubble generation and embolism formation as distinct, temporarily and spatially separated processes. Embolism formation occurs when nanobubbles become unstable, whereas nanobubbles below critical stability thresholds can remain stable in sap-filled conduits. Conclusions Together, these findings reconfirm that pit membranes function as safety valves enabling water transport according to the cohesion-tension theory, and provide mechanistic insights into embolism propagation. They address the question why plants do not suffer constant embolism formation despite negative xylem pressures. We conclude that a revised framework explicitly accounting for the 3D structure of pit membranes, and multiphase, dynamic processes operating within them are required to explain the biophysics underlying water transport and embolism resistance in angiosperm xylem.
Authors 56
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Steven Jansen corresponding
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Institute of Botany, Ulm University, Albert-Einstein-Allee 11, 89081 Ulm, Germany
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Institute of Biology, Structural and Functional Plant Diversity, Freie Universität Berlin, Altensteinstrasse 6, 14195 Berlin, Germany
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Technical University of Munich
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Root-Soil Interaction, School of Life Sciences, Technical University of Munich, Emil-Ramann-Str. 4, 85354 Freising, Germany
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Institute of Botany, University of Innsbruck, Sternwartestrasse 15, 6020 Innsbruck, Austria
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School of Earth and Environmental Sciences, Cardiff University, Main Building, Park Place, CF10 3AT, Cardiff, United Kingdom
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Institute of Botany, Ulm University, Albert-Einstein-Allee 11, 89081 Ulm, Germany
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Universitat de les Illes Balears
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INAGEA, University of the Balearic Islands, Carretera de Valldemossa, km 7.5, 07122 Palma, Spain
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Department of Forest and Rangeland Stewardship, Colorado State University, 1001 Amy Van Dyken Way, Fort Collins, CO 80523, United States of America
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Indian Institute of Science Education and Research Thiruvananthapuram
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School of Biology, Indian Institute of Science Education and Research Thiruvananthapuram (IISER TVM), Maruthamala P.O., Vithura, Thiruvananthapuram, Kerala 695551, India
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Centre National de la Recherche Scientifique · Centre de Coopération Internationale en Recherche Agronomique pour le Développement · Institut National de Recherche pour l'Agriculture, l'Alimentation et l'Environnement · UMR Botanique et Modélisation de l’Architecture des Plantes et des végétations · Institut de Recherche pour le Développement
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UMR AMAP, Univ. Montpellier, CNRS, IRD, CIRAD, INRAE, Montpellier, France
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Institute for Atmospheric and Earth System Research, Faculty of Agriculture and Forestry, University of Helsinki, Viikinkaari 11, 00790 Helsinki, Finland
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Affiliation as printed
Institute for Atmospheric and Earth System Research/Physics, University of Helsinki, Helsinki, Finland
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Affiliation as printed
Institute of Botany, Ulm University, Albert-Einstein-Allee 11, 89081 Ulm, Germany
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Czech University of Life Sciences Prague
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Department of Forest Ecology, Faculty of Forestry and Wood Sciences, Czech University of Life Sciences Prague, Kamýcká 129, 16500 Prague, Czech Republic
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Department of Experimental Biology, Faculty of Science, Masaryk University, Kamenice 5, 62500 Brno, Czech Republic
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Department of Theoretical Physics, Jožef Stefan Institute, Jamova 39, 1000 Ljubljana, Slovenia
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Tampere University · University of Tampere
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Data Science Research Centre / Tampere Institute for Advanced Study, Tampere University, Korkeakoulunkatu 1, 33720 Tampere, Finland
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School of Natural Sciences, Macquarie University, 4-6 Eastern Road, Macquarie Park, NSW 2109, Australia
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Institute of Botany, Ulm University, Albert-Einstein-Allee 11, 89081 Ulm, Germany
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University of Helsinki · University of Eastern Finland
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Department of Forest Sciences, Faculty of Agriculture and Forestry, University of Helsinki, Helsinki, Finland
School of Forest Sciences, University of Eastern Finland, Joensuu, Finland
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Frederic Lens Aachen Plant Sciences Institute of Biology Leiden Research Group Functional Traits Naturalis Biodiversity Center
Leiden University · Naturalis Biodiversity Center
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Plant Sciences, Institute of Biology Leiden, Sylviusweg 72, 2333 BE Leiden, The Netherlands
Research Group Functional Traits, Naturalis Biodiversity Center, Darwinweg 2, 2333 CR Leiden, The Netherlands
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Centre National de la Recherche Scientifique · Centre de Coopération Internationale en Recherche Agronomique pour le Développement · Université de Montpellier · Institut National de Recherche pour l'Agriculture, l'Alimentation et l'Environnement · UMR Botanique et Modélisation de l’Architecture des Plantes et des végétations · Institut de Recherche pour le Développement
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AMAP, Université de Montpellier, CIRAD, CNRS, INRAE, IRD, Montpellier, France
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Technische Universität Dresden
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Chair of Forest Botany, Faculty of Environmental Science, TUD Dresden University of Technology, 01737 Tharandt, Germany
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Institute for Atmospheric and Earth System Research, Faculty of Science, University of Helsinki, Gustaf Hällströmin katu 2, 00560 Helsinki, Finland
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Institute of Botany, University of Innsbruck, Sternwartestrasse 15, 6020 Innsbruck, Austria
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Purdue University West Lafayette
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Department of Botany and Plant Pathology, Purdue University, 915 Mitch Daniels Blvd, West Lafayette, IN 47909, USA
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Red de Ecologia Funcional, Instituto de Ecologia, A.C., Carretera antigua a Coatepec No. 351, El Haya, Xalapa 91073, Veracruz, Mexico
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California State University, Fullerton
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Department of Biological Science, California State University Fullerton, 800 N. State College Boulevard, Fullerton, CA 92831, USA
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Universidade Estadual de Campinas (UNICAMP)
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Institute of Biology, University of Campinas (UNICAMP), Rua Monteiro Lobato 255, 13083-862 Campinas SP, Brazil
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Department of Botany and Plant Ecology, Weber State University, 1415 Edvalson St., Dept. 2504, Ogden, UT 84408, USA
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Indian Institute of Technology Guwahati
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Department of Mechanical Engineering, Indian Institute of Technology Guwahati (IIT Guwahati), Amingaon, North Guwahati, Guwahati, Assam 781039, India
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School of Biological and Social Sciences, SRUC, Parkgate, Dumfries DG1 3NE, United Kingdom
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Department of Life Sciences, University of Trieste, Via L. Giorgieri 10, 34127 Trieste, Italy
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Institute of Botany, Ulm University, Albert-Einstein-Allee 11, 89081 Ulm, Germany
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Plant Ecology and Ecosystems Research, Albrecht von Haller Institute for Plant Sciences, University of Goettingen, Untere Karspüle 2, 37073 Göttingen, Germany
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Estonian University of Life Sciences · Universitat de les Illes Balears
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Institute of Agricultural and Environmental Sciences, Estonian University of Life Sciences, Kreutzwaldi 1, 51006 Tartu, Estonia
Research Group on Plant Biology Under Mediterranean Conditions, INAGEA, University of the Balearic Islands, Carretera de Valldemossa, km 7.5, 07122 Palma, Spain
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Czech University of Life Sciences Prague
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Department of Forest Ecology, Faculty of Forestry and Wood Sciences, Czech University of Life Sciences, Kamýcká 129, 165 00 Praha, Czech Republic
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Universidade Estadual de Campinas (UNICAMP)
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Institute of Biology, University of Campinas (UNICAMP), Rua Monteiro Lobato 255, 13083-862 Campinas SP, Brazil
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Purdue University West Lafayette
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Department of Botany and Plant Pathology, Purdue University, 915 Mitch Daniels Blvd, West Lafayette, IN 47909, USA
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Institute of Botany, Department of Ecosystem Management, Climate and Biodiversity, BOKU University, Gregor-Mendel-Straße 33, 1180 Vienna, Austria
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Department of Geography, Faculty of Environment, Science and Economy, University of Exeter, North Park Road, EX4 4QE, UK
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University of California, Los Angeles
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Department of Ecology and Evolutionary Biology, University of California, Los Angeles, 621 Charles E. Young Drive South, Los Angeles, California 90095, USA
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Institute for Atmospheric and Earth System Research, Faculty of Science, University of Helsinki, Gustaf Hällströmin katu 2, 00560 Helsinki, Finland
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Southeast Asia Rainforest Research Partnership (SEARRP), Southeast Asia Rainforest Research Partnership (SEARRP), S10-S12, Lorong Puncak 1, 88400 Kota Kinabalu, Malaysia
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Institute of Botany, Ulm University, Albert-Einstein-Allee 11, 89081 Ulm, Germany
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Technische Universität Darmstadt
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Institute for Condensed Matter Physics, Technische Universität Darmstadt, Hochschulstrasse 8, 64289 Darmstadt, Germany
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Technische Universität Dresden
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Chair of Forest Botany, TUD Dresden University of Technology, Pienner Str. 7, 01737 Tharandt, Germany
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Institute of Biology, University of Graz, Holteigasse 6, 8010 Graz, Austria
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Department of Forest Botany, Dendrology and Geobiocoenology, Faculty of Forestry and Wood Technology, Mendel University in Brno, Zemedelska 3, 61300 Brno, Czech Republic
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Department of Life Sciences, University of Trieste, Via L. Giorgieri 10, 34127 Trieste, Italy
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Institute of Botany / Core Facility light microscopy, Ulm University, Albert-Einstein-Alle 11, 89081 Ulm, Germany
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Institute for Atmospheric and Earth System Research, Faculty of Science, University Of Helsinki, Helsinki, Finland
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Kansas, Lipidomics Research Center, Division of Biology, Kansas State University, 1717 Clafin Rd, Manhattan, KS 66506, USA
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Key Laboratory of Bioresource Protection and Utilization of Anhui Province · Anhui Normal University
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The Anhui Provincial Key Laboratory of Biodiversity Conservation and Ecological Security in the Yangtze River Basin, College of Life Sciences, Anhui Normal University, Wuhu, 241000, Anhui, China
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Swiss Federal Institute for Forest, Snow and Landscape Research
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Swiss Federal Institute for Forest, Snow and Landscape Research WSL, Forest and Soil Ecology, Zurcherstrasse 111, 8903 Birmensdorf, Switzerland
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California State University, Fullerton
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Department of Biological Science, California State University Fullerton, 800 N. State College Boulevard, Fullerton, CA 92831, USA
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