Integrating physiology, anatomy, and modelling to understand xylem embolism spreading in angiosperms based on gas diffusion kinetics

• Applicant: Professor Dr. Steven Jansen
• Subject Area: Ecology and Biodiversity of Plants and Ecosystems
• Term: from 2021 to 2024
• Project identifier: Deutsche Forschungsgemeinschaft (DFG) - Project number 457287575

• Final Report Year: 2025

Final Report Abstract

This project examined sap transport in the wood of flowering plants. Solar energy ultimately drives this process, with cohesive forces among water molecules enabling transport under negative pressure. However, water-conducting cells (conduits) are open to gas, which is always present either in the gas phase or dissolved in sap. Gas movement in conduits raises concerns about transport efficiency and safety, as embolism (gas filling the transport pathway) can block sap flow. Understanding this process is crucial for assessing drought resistance. Therefore, this project investigated how changes in gas pressure and concentration relate to embolism formation. Using lab-based experiments, anatomical observations, and modelling, we examined gas movement through porous cell walls, gas content in sap, and embolism spread mechanisms. Pneumatic experiments tracked gas entry in cut-open branches, while flow-centrifuge tests on spinning stem segments revealed that embolism spreads between conduits via pores in conduit walls. Gas transport was about 200 times faster axially than radially, mainly due to conduit anatomy. Since axial gas diffusion over 15 cm can take several minutes, we showed that embolism is not solely driven by negative pressure. Including time as a factor improved embolism resistance measurements by ca. 8.5%. Experiments on living plants demonstrated daily patterns in extractable gas, with higher amounts during high transpiration periods. These fluctuations likely reflect changes in gas saturation, though their role in embolism formation remains unclear. We explored this link via lipidcoated nanobubbles and the multiphase interactions between sap, gas, and polar lipids, an area further pursued in ongoing research by physicists. Anatomical data and experiments were complemented with modelling to better understand gas movement in wood. Although embolism formation is not solely dependent on gas diffusion kinetics, our models showed strong agreement with experimental results. We also developed a pneumatic model to measure embolism resistance using an automated device. However, we could not quantify hydraulic resistance at nodes, stem bifurcations, or stem-leaf transitions, and preliminary data suggest no major hydraulic bottlenecks from tree tip to base. This project led to 13 peer-reviewed publications. Findings were presented at national and international conferences and shared with the public through our "talking trees" at Ulm University’s botanical garden and in Ulm city.

Publications

• Hydraulic safety-vessel diameter relationships of 20 temperate broadleaf tree species. British Ecological Society: the across borders conference. 15-15 December 2021, Liverpool, UK
  Isasa E., Link R.M., Jansen S., Cabra J.S. & Schuldt B.
  
• A crucial phase in plants – it's a gas, gas, gas!. New Phytologist, 233(4), 1556-1559.
  Jansen, Steven; Bittencourt, Paulo; Pereira, Luciano; Schenk, H. Jochen & Kunert, Norbert
  
• A unit pipe pneumatic model to simulate gas kinetics during measurements of embolism in excised angiosperm xylem. Tree Physiology, 43(1), 88-101.
  Yang, Dongmei; Pereira, Luciano; Peng, Guoquan; Ribeiro, Rafael V.; Kaack, Lucian; Jansen, Steven & Tyree, Melvin T.
  
• Dissolved gas in xylem sap is affected by water potential and temperature, but does not follow Henry’s law for bulk solutions. 5th Xylem International Meeting, 19-21 September 2022, Würzburg
  Pereira L., Jansen S., Miranda M.T., Pacheco V.S., Kaack L., Pires G.S., Guan X., Mayer J.L.S., Machado E.C., Schenk H.J. & Ribeiro R.V.
  
• Dynamic changes in gas concentration in the sap of plants reiterate the enigma of plant water transport under negative pressure. InterPore 2022, 30 May – 2 June 2022. Abu Dhabi
  Pereira L., Jansen S., Miranda M.T., Pacheco V.S., Kaack L., Pires G.S., Guan X., Machado E.C., Schenk H.J., Tyree M.T. & Ribeiro R.V.
  
• Dynamic changes in gas solubility of xylem sap reiterate the enigma of plant water transport under negative pressure.
  Pereira, Luciano; Jansen, Steven; Miranda, Marcela T.; Pacheco, Vinícius S.; Kaack, Lucian; Pires, Gabriel S.; Guan, Xinyi; Mayer, Juliana L.S.; Machado, Eduardo C.; Schenk, H. Jochen & Ribeiro, Rafael V.
  
• On the structure and mechanistic function of angiosperm pit membranes. 5th Xylem International Meeting, 19-21 September 2022, Würzburg
  Kaack L. & Jansen S.
  
• Reconciling discrepancies in measurements of vulnerability to xylem embolism with the pneumatic method. New Phytologist, 237(2), 374-383.
  Brum, Mauro; Pereira, Luciano; Ribeiro, Rafael Vasconcelos; Jansen, Steven; Bittencourt, Paulo R. L.; Oliveira, Rafael S. & Saleska, Scott R.
  
• The functional significance of porous media and polar lipids for fluid transport in angiosperm xylem. 5th Xylem International Meeting, 19-21 September 2022, Würzburg
  Jansen S.
  
• The relative area of vessels in xylem correlates with stem embolism resistance within and between genera. Tree Physiology, 43(1), 75-87.
  Avila, Rodrigo T.; Kane, Cade N.; Batz, Timothy A.; Trabi, Christophe; Damatta, Fábio M.; Jansen, Steven & McAdam, Scott A. M.
  
• Vessel diameter corresponds to vessel length in relation to water transport and xylem function. 5th Xylem International Meeting, 19-21 September 2022, Würzburg
  Valadares G., Seiboth M., Kaack L., Pereira L. & Jansen S.
  
• Xylem hydraulic conductivity measurements during flow-controlled experiments suggest the presence of nanobubbles that move with the flow and accumulate at vessel ends. Copernicus GmbH.
  Krieger, Louis; Schymanski, Stanislaus & Jansen, Steven
  
• Angiosperms follow a convex trade-off to optimize hydraulic safety and efficiency. 1st International Meeting on the Gas phase in plants. Hyytiälä Research Station, Finland, 12-14 September 2023
  Pereira L., Kaack L., Guan X., Silva L.M., Miranda M., Pires G.S., Ribeiro R.V., Schenk H.J. & Jansen S.
  
• Angiosperms follow a convex trade‐off to optimize hydraulic safety and efficiency. New Phytologist, 240(5), 1788-1801.
  Pereira, Luciano; Kaack, Lucian; Guan, Xinyi; Silva, Luciano de Melo; Miranda, Marcela T.; Pires, Gabriel S.; Ribeiro, Rafael V.; Schenk, H. Jochen & Jansen, Steven
  
• Assessing the agreement between the pneumatic and the flow‐centrifuge method for estimating xylem safety in temperate diffuse‐porous tree species. Plant Biology, 25(7), 1171-1185.
  Paligi, S. S.; Link, R. M.; Isasa, E.; Bittencourt, P.; Cabral, J. S.; Jansen, S.; Oliveira, R. S.; Pereira, L. & Schuldt, B.
  
• Comparative anatomy vs mechanistic understanding: how to interpret the diameter-vulnerability link. IAWA Journal, 44(3-4), 368-380.
  Lens, Frederic; Gleason, Sean M.; Bortolami, Giovanni; Brodersen, Craig; Delzon, Sylvain & Jansen, Steven
  
• Gas diffusion kinetics in relation to embolism formation and propagation in angiosperm xylem: a mini-review of the latest experimental and modelling evidence. ISHS, XII International Workshop on Sap Flow, New Zealand, Rotorua, 31/10/2023 – 3/11 2023
  Silva L.d.M., Pereira L., Kaack L. & Jansen S.
  
• Lipid-Coated Nanobubbles in Plants. Nanomaterials, 13(11), 1776.
  Ingram, Stephen; Jansen, Steven & Schenk, H. Jochen
  
• Pores Inwater Conducting Cells of Plants. Album of Porous Media, 101-101. Springer International Publishing.
  Jansen, Steven
  
• Rootstocks affect the vulnerability to embolism and pit membrane thickness in grafted shoots of Citrus trees. 1st International Meeting on the Gas phase in plants. Hyytiälä Research Station, Finland, 12-14 September 2023
  Miranda M.T., Pires G.S., Pereira L., Lima R.F., Silva S.F., Mayer J.L.S., Azevedo F.A., Machado E.C., Jansen S. & Ribeiro R.V.
  
• The gas phase in plants – what’s next? 1st International Meeting on the Gas phase in plants. Hyytiälä Research Station, Finland, 12-14 September 2023
  Jansen S.
  
• {pneumatron} – an R package for managing embolism vulnerability curves with the Pneumatic method. 1st International Meeting on the Gas phase in plants. Hyytiälä Research Station, Finland, 12-14 September 2023
  Pires G.S., Pereira L., Miranda M.T., Kreinert S., Machado E.C., Jansen S. & Ribeiro R.V.
  
• Embolism propagation does not rely on pressure only: time-based shifts in xylem vulnerability curves of angiosperms determine the accuracy of the flow-centrifuge method. Tree Physiology, 46(13), 81-95.
  Silva, Luciano M.; Pfaff, Jonas; Pereira, Luciano; Miranda, Marcela T. & Jansen, Steven
  
• Gold perfusion experiments support the multi‐layered, mesoporous nature of intervessel pit membranes in angiosperm xylem. New Phytologist, 242(2), 493-506.
  Zhang, Ya; Pereira, Luciano; Kaack, Lucian; Liu, Jiabao & Jansen, Steven
  
• The potential link between gas diffusion and embolism spread in angiosperm xylem: Evidence from flow‐centrifuge experiments and modelling. Plant, Cell & Environment, 47(12), 4977-4991.
  Silva, Luciano M.; Pereira, Luciano; Kaack, Lucian; Guan, Xinyi; Pfaff, Jonas; Trabi, Christophe L. & Jansen, Steven
  
• Time-based shifts in xylem vulnerability curves of angiosperms based on the flow-centrifuge method. GfÖ meeting Freising, Germany, 9-13 September 2024
  Silva L.M., Pfaff J., Pereira L., Miranda M.T. & Jansen S.
  
• Xylem sap residue in cut-open conduits can affect gas discharge in pneumatic experiments. Tree Physiology, 46(13), 70-80.
  Miranda, Marcela T.; Pereira, Luciano; Pires, Gabriel S.; Guan, Xinyi; Silva, Luciano M.; Kreinert, Swetlana; Machado, Eduardo C.; Jansen, Steven & Ribeiro, Rafael V.
  
• Gas diffusion kinetics in relation to embolism formation and propagation in angiosperm xylem: a mini-review. Acta Horticulturae(1419), 123-134.
  Silva, L.M.; Bujnowski, B.; Pereira, L.; Miranda, M.T.; Schenk, H.J. & Jansen, S.
  
• Xylem conduit dimensions show no hydraulic bottleneck along the axis of an angiosperm tree.
  Kreinert, Swetlana; Kaack, Lucian; Pereira, Luciano; Miranda, Marcela; Mäck, Stefan; Schuler, Jonas & Jansen, Steven