Surfactants may shed novel light on water transport in plants under negative pressure
Ecology and Biodiversity of Plants and Ecosystems
Plant Physiology
Final Report Abstract
This project explored the functional significance of polar lipids and porous cell walls for water transport in plants. By accounting for contamination, the presence of polar lipids could unambiguously be shown in xylem sap of angiosperms. After cell death of water conducting cells, polar lipids were found to be left-overs from cell contents, and mainly included phospholipids and galactolipids. Since small concentrations of these lipids have a highly effective surface tension at gas-liquid interfaces, they contribute to the entry of tiny, lipidcoated gas bubbles in sap. Although the fate of these nano-sized bubbles requires more research, they can be stable by the dynamic surface tension of the lipid shell, which is concentration and time dependent. Moreover, while the hydrophobic tails of the polar lipids cling on inner walls of water conducting cells, the head groups contribute to the hydrophilic nature of these walls. The porous cell wall structure between neighbouring water conducting cells was found to represent mesoporous media, with pore sizes between 5 and 50 nm, and a wall thickness between 200 and 1,000 nm. An important finding was that flow through the porous walls strongly depended on the number of pore constrictions within a single, typically unbending pore pathway. Pore constrictions represent bottlenecks between interconnected pore voids, and play a key role in the movement of sap and gas between adjacent cells. Most importantly, pore constriction sizes decreased strongly with increasing thickness of the porous wall, but were less affected by the total surface area of adjacent walls. This novel insight explains how plants are able to construct pipelines for safe sap transport without sacrificing much transport efficiency to supply their photosynthetic organs. Moreover, we found that deformation and shrinkage of the porous walls was associated with an increasing wall stiffness, which gradually occurred in plants over consecutive years. The wall stiffness was also found to be sufficiently high to avoid bending and flexing under normal growing conditions, which contributes to our understanding of fluid transport and nanobubble formation. Taken together, the available evidence highlights that xylem sap lipids and porous cell walls represent key-concepts that enable water transport under negative pressure without constant hydraulic failure. The novel insights gained by this project put us in a better position to mimic transport under negative pressure in “synthetic trees”, or evaporation-driven transport devices, which have not been fully achieved yet. Both experimental and modelling approaches may offer exciting, complementary approaches to achieve this goal. More research is also needed to understand how exactly large gas bubbles can be formed that block the xylem transport system. Novel research questions and challenges raised in this project will be addressed by the research team of the PI in future research. Most of the challenges encountered in this project were related to technical issues, especially the prevention of preparation artefacts and potential failure of negative transport systems due to manipulation. So far, output of the project resulted in various scientific publications, presentations at both national and international meetings, and a workshop at Ulm University on “Negative pressure in multiphase environments”. Finally, media attention to the project was reported by the following sources: (1) Mai 2019: Wegbereiter des bionischen Baumstamms (UniUlm Intern); (2) 19 August 2019: report about our ChinaTron and artificial stem systems in Die Linde „Bionischer Baumstamm hilft Wassertransport in Pflanzen zu verstehen“ (https://dielinde.online/4994/bionischer-baumstamm-hilft-wassertransport-in-pflanzen-zu-verstehen/), and "Deutschlandweit einziges Chinatron an der Uni Ulm: Wegbereiter des bionischen Baumstamms” (https://nachrichten.idw-online.de/2019/08/19/deutschlandweit-einziges-chinatron-an-der-uni-ulm-wegbereiter-des-bionischen-baumstamms/); (3) 30 August 2019: Video on SWR2 Aktuell „Wann und warum kollabieren Pflanzen“; and (4) 5 May 2020: Press release related to the paper by Kanduć et al (2020, PNAS) - What limits the suction power of plants? (IDW), Lipids limit the suction power of plants (Technische Universität Darmstadt).
Publications
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(2020) Cavitation in lipid bilayers poses strict negative pressure stability limit in biological liquids. PNAS 117: 10733-10739
Kanduč M., Schneck E., Loche P., Jansen S., Schenk H.J., Netz R.R.
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(2020) Dynamic surface tension of xylem sap lipids. Tree Physiology 40: 433-444
Yang J., Michaud J., Jansen S., Schenk H.J., Zuo Y.
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(2020) High porosity with tiny pore constrictions and unbending pathways characterise the 3D structure of intervessel pit membranes in angiosperm xylem. Plant, Cell and Environment 43: 116-130
Zhang Y., Carmesin C., Kaack L., Klepsch M.M., Kotowska M., Matei T., Schenk H.J., Weber M., Walter P., Schmidt V., Jansen S.
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(2021) An increase in xylem embolism resistance of grapevine leaves during the growing season is coordinated with stomatal regulation, turgor loss point, and intervessel pit membranes. New Phytologist 229: 1955-1969
Sorek Y., Grinshtein S., Netzer Y., Shtein I., Jansen S., Hochberg U.
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(2021) Lipids in xylem sap of woody plants across the angiosperm phylogeny. The Plant Journal 105:1477-1494
Schenk H.J., Michaud J.M., Espino S., Melendres T., Roth M.R., Welti R., Kaack L., Jansen S.
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(2021) Pore constrictions in intervessel pit membranes provide a mechanistic explanation for xylem embolism resistance in angiosperms. New Phytologist 230: 1829-1843
Kaack L., Weber M., Isasa E., Karimi Z., Li S., Pereira L., Trabi C., Zhang Y., Schenk H.J., Schuldt B., Schmidt V., Jansen S.
