Pore constrictions in intervessel pit membranes provide a mechanistic explanation for xylem embolism resistance in angiosperms
Open Access
- 17 February 2021
- journal article
- research article
- Published by Wiley in New Phytologist
- Vol. 230 (5), 1829-1843
- https://doi.org/10.1111/nph.17282
Abstract
Embolism spreading in angiosperm xylem occurs via mesoporous pit membranes between vessels. Here, we investigate how the size of pore constrictions in pit membranes is related to pit membrane thickness and embolism resistance. Pit membranes were modelled as multiple layers to investigate how pit membrane thickness and the number of intervessel pits per vessel determine pore constriction sizes, the probability of encountering large pores, and embolism resistance. These estimations were complemented by measurements of pit membrane thickness, embolism resistance, and number of intervessel pits per vessel in stem xylem (n = 31, 31, and 20 species, respectively). The modelled constriction sizes in pit membranes decreased with increasing membrane thickness, explaining the measured relationship between pit membrane thickness and embolism resistance. The number of pits per vessel affected constriction size and embolism resistance much less than pit membrane thickness. Moreover, a strong relationship between modelled and measured embolism resistance was observed. Pore constrictions provide a mechanistic explanation why pit membrane thickness determines embolism resistance, and suggest that hydraulic safety can be uncoupled from hydraulic efficiency. Although embolism spreading remains puzzling and encompasses more than pore constriction sizes, angiosperms are unlikely to have leaky pit membranes, which enables tensile transport of water.Keywords
Funding Information
- Deutsche Forschungsgemeinschaft (JA 2174/5‐1, 383393940)
- National Science Foundation (IOS‐1754850)
- Ministerium für Wissenschaft, Forschung und Kunst Baden-Württemberg (7533‐7‐11.10‐16)
This publication has 78 references indexed in Scilit:
- In Vivo Visualizations of Drought-Induced Embolism Spread in Vitis viniferaPlant Physiology, 2013
- Nobody’s perfect: can irregularities in pit structure influence vulnerability to cavitation?Frontiers in Plant Science, 2013
- Phenotypic and developmental plasticity of xylem in hybrid poplar saplings subjected to experimental drought, nitrogen fertilization, and shadingJournal of Experimental Botany, 2012
- Testing hypotheses that link wood anatomy to cavitation resistance and hydraulic conductivity in the genus AcerNew Phytologist, 2010
- Do quantitative vessel and pit characters account for ion‐mediated changes in the hydraulic conductance of angiosperm xylem?New Phytologist, 2010
- The relevance of xylem network structure for plant hydraulic efficiency and safetyJournal of Theoretical Biology, 2007
- Pit Membrane Porosity and Water Stress-Induced Cavitation in Four Co-Existing Dry Rainforest Tree SpeciesPlant Physiology, 2003
- Relationships between Embolism, Stem Water Tension, and Diameter ChangesJournal of Theoretical Biology, 2002
- Cortical microtubule involvement in bordered pit formation in secondary xylem vessel elements ofAesculus hippocastanum L. (Hippocastanaceae): A correlative study using electron microscopy and indirect immunofluorescence microscopyProtoplasma, 1997
- Pit membranes in hardwoods?Fine structure and developmentProtoplasma, 1968