Abstract
Key message
Intervessel pit membranes in xylem tissue of Acer pseudoplatanus differ in their thickness both within and across plant organs and may undergo considerable shrinkage during dehydration and sample preparation.
Abstract
Intervessel pit membranes have been suggested to account for more than half of the total xylem hydraulic resistance in plants and play a major role in vulnerability to drought-induced hydraulic failure. While the thickness of intervessel pit membranes was found to be associated with xylem embolism resistance at an interspecific level, variation in pit membrane structure across different organs along the flow path within a single tree remains largely unknown. Based on transmission electron microscopy, we examined intra-tree variation of bordered pit and pit membrane characteristics in xylem of roots, stems, branches, petioles, and leaf veins of Acer pseudoplatanus. Moreover, potential preparation artefacts on pit membrane structure such as alcohol treatment and dehydration were tested. Our observations showed quantitative differences in bordered pits across organs, including variation in pit membrane thickness within and across organs. Vessel size was weakly related to intervessel wall thickness, but not significantly linked to pit membrane thickness. Gradual dehydration of wood samples resulted in irreversible shrinkage of pit membranes, together with increased levels of aspiration. These findings are relevant to explore similarity in xylem embolism resistance across plant organs.
Similar content being viewed by others
References
Alder NN, Sperry JS, Pockman WT (1996) Root and stem xylem embolism, stomatal conductance, and leaf turgor in Acer grandidentatum populations along a soil moisture gradient. Oecologia 105:293–301
Anfodillo T, Petit G, Crivellaro A (2013) Axial conduit widening in woody species: a still neglected anatomical pattern. IAWA J 34:352–364. https://doi.org/10.1163/22941932-00000030
Bonner LD, Thomas RJ (1972) The ultrastructure of intercellular passageways in vessels of yellow poplar (Liriodendron tulipifera, L.) part I: vessel pitting. Wood Sci Technol 6:196–203
Brodribb TJ, Skelton RP, McAdam SAM et al (2016) Visual quantification of embolism reveals leaf vulnerability to hydraulic failure. New Phytol 209:1403–1409
Burgess SSO, Pittermann J, Dawson TE (2006) Hydraulic efficiency and safety of branch xylem increases with height in Sequoia sempervirens (D. Don) crowns. Plant Cell Environ 29:229–239
Butterfield BG (1998) Microfibril angle in wood. In: The Proceedings of the IAWA/IUFRO international workshop on the significance of microfibril angle to wood quality. International Association of Wood Anatomists, Westport
Choat B, Ball M, Luly J, Holtum J (2003) Pit membrane porosity and water stress-induced cavitation in four co-existing dry rainforest tree species. Plant Physiol 131:41–48
Choat B, Jansen S, Zwieniecki MA et al (2004) Changes in pit membrane porosity due to deflection and stretching: the role of vestured pits. J Exp Bot 55:1569–1575
Choat B, Lahr EC, Melcher PJ et al (2005) The spatial pattern of air seeding thresholds in mature sugar maple trees. Plant Cell Environ 28:1082–1089
Choat B, Brodie TW, Cobb AR et al (2006) Direct measurements of intervessel pit membrane hydraulic resistance in two angiosperm tree species. Am J Bot 93:993–1000
Choat B, Cobb AR, Jansen S (2008) Structure and function of bordered pits: new discoveries and impacts on whole-plant hydraulic function. New Phytol 177:608–626
Choat B, Jansen S, Brodribb TJ et al (2012) Global convergence in the vulnerability of forests to drought. Nature 491:752
Czaninski Y (1979) Cytochimie ultrastructurale des parois du xyleme secondaire. Biol Cell 35:97–102
Domec JC, Gartner BL (2002) Age-and position-related changes in hydraulic versus mechanical dysfunction of xylem: inferring the design criteria for Douglas-fir wood structure. Tree Physiol 22:91–104
Domec J-C, Lachenbruch B, Meinzer FC (2006) Bordered pit structure and function determine spatial patterns of air-seeding thresholds in xylem of Douglas-fir (Pseudotsuga menziesii; Pinaceae) trees. Am J Bot 93:1588–1600
Fang L, Catchmark JM (2014) Characterization of water-soluble exopolysaccharides from Gluconacetobacter xylinus and their impacts on bacterial cellulose crystallization and ribbon assembly. Cellulose 21:3965–3978
Giraudoux P (2017) “pgirmess”: data analysis in ecology. R package version 1.6.7. https://CRAN.R-project.org/package=pgirmess
Hacke UG, Sperry JS, Pittermann J (2000) Drought experience and cavitation resistance in six shrubs from the Great Basin, Utah. Basic Appl Ecol 1:31–41
Hacke UG, Sperry JS, Pockman WT et al (2001) Trends in wood density and structure are linked to prevention of xylem implosion by negative pressure. Oecologia 126:457–461. https://doi.org/10.1007/s004420100628
Hacke UG, Sperry JS, Wheeler JK, Castro L (2006) Scaling of angiosperm xylem structure with safety and efficiency. Tree Physiol 26:689–701
Herbette S, Bouchet B, Brunel N et al (2014) Immunolabelling of intervessel pits for polysaccharides and lignin helps in understanding their hydraulic properties in Populus tremula × alba. Ann Bot 115:187–199
Hochberg U, Albuquerque C, Rachmilevitch S et al (2016) Grapevine petioles are more sensitive to drought induced embolism than stems: evidence from in vivo MRI and microcomputed tomography observations of hydraulic vulnerability segmentation. Plant Cell Environ 39:1886–1894
Jansen S, Schenk HJ (2015) On the ascent of sap in the presence of bubbles. Am J Bot 102:1561–1563
Jansen S, Pletsers A, Sano Y (2008) The effect of preparation techniques on SEM-imaging of pit membranes. IAWA J 29:161–178
Jansen S, Choat B, Pletsers A (2009) Morphological variation of intervessel pit membranes and implications to xylem function in angiosperms. Am J Bot 96:409–419
Jansen S, Klepsch M, Li S et al (2018) Challenges in understanding air-seeding in angiosperm xylem. Acta Hortic 1222:13–20
Johnson DM, Wortemann R, McCulloh KA et al (2016) A test of the hydraulic vulnerability segmentation hypothesis in angiosperm and conifer tree species. Tree Physiol 36:983–993
Kadunc A (2007) Factors influencing the formation of heartwood discolouration in sycamore (Acer pseudoplatanus L.). Eur J For Res 126:349–358
Kavanagh KL, Bond BJ, Aitken SN et al (1999) Shoot and root vulnerability to xylem cavitation in four populations of Douglas-fir seedlings. Tree Physiol 19:31–37
Klepsch MM, Schmitt M, Paul Knox J, Jansen S (2016) The chemical identity of intervessel pit membranes in Acer challenges hydrogel control of xylem hydraulic conductivity. AoB Plants. https://doi.org/10.1093/aobpla/plw052
Klepsch M, Zhang Y, Kotowska MM et al (2018) Is xylem of angiosperm leaves less resistant to embolism than branches? Insights from microCT, hydraulics, and anatomy. J Exp Bot 69:5611–5623
Kotowska MM, Hertel D, Abou Rajab Y et al (2015) Patterns in hydraulic architecture from roots to branches in six tropical tree species from cacao agroforestry and their relation to wood density and stem growth. Front Plant Sci 6:191
Lens F, Sperry JS, Christman MA et al (2011) Testing hypotheses that link wood anatomy to cavitation resistance and hydraulic conductivity in the genus Acer. New Phytol 190:709–723. https://doi.org/10.1111/j.1469-8137.2010.03518.x
Li S, Lens F, Espino S et al (2016) Intervessel pit membrane thickness as a key determinant of embolism resistance in angiosperm xylem. IAWA J 37:152–171
Liu M, Pan R, Tyree MT (2018) Intra-specific relationship between vessel length and vessel diameter of four species with long-to-short species-average vessel lengths: further validation of the computation algorithm. Trees 32:51–60
Losso A, Bär A, Dämon B et al (2019) Insights from in vivo micro-CT analysis: testing the hydraulic vulnerability segmentation in Acer pseudoplatanus and Fagus sylvatica seedlings. New Phytol 221:1831–1842
Martinez-Sanz M, Pettolino F, Flanagan B et al (2017) Structure of cellulose microfibrils in mature cotton fibres. Carbohydr Polym 175:450–463
Martinez-Vilalta J, Prat E, Oliveras I, Pinol J (2002) Xylem hydraulic properties of roots and stems of nine Mediterranean woody species. Oecologia 133:19–29. https://doi.org/10.1007/s00442-002-1009-2
McElrone AJ, Pockman WT, Martinez-Vilalta J, Jackson RB (2004) Variation in xylem structure and function in stems and roots of trees to 20 m depth. New Phytol 163:507–517. https://doi.org/10.1111/j.1469-8137.2004.01127.x
Meyra AG, Kuz VA, Zarragoicoechea GJ (2007) Geometrical and physicochemical considerations of the pit membrane in relation to air seeding: the pit membrane as a capillary valve. Tree Physiol 27:1401–1405
Nardini A, Dimasi F, Klepsch M, Jansen S (2012) Ion-mediated enhancement of xylem hydraulic conductivity in four Acer species: relationships with ecological and anatomical features. Tree Physiol 32:1434–1441
Olson ME, Anfodillo T, Rosell JA et al (2014) Universal hydraulics of the flowering plants: vessel diameter scales with stem length across angiosperm lineages, habits and climates. Ecol Lett 17:988–997
Pereira L, Domingues-Junior AP, Jansen S et al (2018) Is embolism resistance in plant xylem associated with quantity and characteristics of lignin? Trees 32:349–358
Pesacreta TC, Groom LH, Rials TG (2005) Atomic force microscopy of the intervessel pit membrane in the stem of Sapium sebiferum (Euphorbiaceae). IAWA J 26:397–426
Pfautsch S, Aspinwall MJ, Drake JE et al (2018) Traits and trade-offs in whole-tree hydraulic architecture along the vertical axis of Eucalyptus grandis. Ann Bot 121:129–141
Schacht H (1859) Über die Tüpfel der Gefäss-und Holzzellen. Bot Zeitung 17:238–239
Schenk HJ, Espino S, Romo DM et al (2017) Xylem surfactants introduce a new element to the cohesion-tension theory. Plant Physiol 173:1177–1196
Schenk HJ, Espino S, Rich-Cavazos SM, Jansen S (2018) From the sap’s perspective: the nature of vessel surfaces in angiosperm xylem. Am J Bot 105:172–185
Schmid R, Machado RD (1968) Pit membranes in hardwoods—fine structure and development. Protoplasma 66:185–204
Scholz A, Rabaey D, Stein A et al (2013) The evolution and function of vessel and pit characters with respect to cavitation resistance across 10 Prunus species. Tree Physiol 33:684–694. https://doi.org/10.1093/treephys/tpt050
Schuldt B, Knutzen F, Delzon S et al (2016) How adaptable is the hydraulic system of European beech in the face of climate change-related precipitation reduction? New Phytol 210:443–458
Schulte PJ, Gibson AC (1988) Hydraulic conductance and tracheid anatomy in six species of extant seed plants. Can J Bot 66:1073–1079
Shane MW, McCully ME, Canny MJ (2000) Architecture of branch–root junctions in maize: structure of the connecting xylem and the porosity of pit membranes. Ann Bot 85:613–624
Skelton RP, Brodribb TJ, Choat B (2017) Casting light on xylem vulnerability in an herbaceous species reveals a lack of segmentation. New Phytol 214:561–569
Sperry JS, Hacke UG (2004) Analysis of circular bordered pit function I. Angiosperm vessels with homogenous pit membranes. Am J Bot 91:369–385
Sperry JS, Saliendra NZ (1994) Intra-plant and inter-plant variation in xylem cavitation in Betula occidentalis. Plant Cell Environ 17:1233–1241. https://doi.org/10.1111/j.1365-3040.1994.tb02021.x
Sperry JS, Tyree MT (1988) Mechanism of water stress-induced xylem embolism. Plant Physiol 88:581–587
Sperry JS, Hacke UG, Pittermann J (2006) Size and function in conifer tracheids and angiosperm vessels. Am J Bot 93:1490–1500
Sperry JS, Nichols KL, Sullivan JE, Eastlack SE (1994) Xylem embolism in ring‐porous, diffuse‐porous, and coniferous trees of northern Utah and interior Alaska. Ecology 75(6):1736–1752
Tixier A, Herbette S, Jansen S et al (2014) Modelling the mechanical behaviour of pit membranes in bordered pits with respect to cavitation resistance in angiosperms. Ann Bot 114:325–334
Tyree MT, Ewers FW (1991) The hydraulic architecture of trees and other woody plants. New Phytol 119:345–360. https://doi.org/10.1111/j.1469-8137.1991.tb00035.x
Tyree MT, Sperry JS (1989) Vulnerability of xylem to cavitation and embolism. Annu Rev Plant Biol 40:19–36
Wheeler JK, Sperry JS, Hacke UG, Hoang N (2005) Inter-vessel pitting and cavitation in woody Rosaceae and other vesselled plants: a basis for a safety versus efficiency trade-off in xylem transport. Plant Cell Environ 28:800–812. https://doi.org/10.1111/j.1365-3040.2005.01330.x
Zhang Y, Klepsch M, Jansen S (2017) Bordered pits in xylem of vesselless angiosperms and their possible misinterpretation as perforation plates. Plant Cell Environ 40:2133–2146
Zimmermann MH (1983) Xylem structure and the ascent of sap. Springer, New York
Acknowledgements
We thank the Botanical Garden of Ulm University for support and providing plant material. We would like to acknowledge the Electron Microscopy Section of Ulm University for technical support with electron microscopy. The project was financially supported by the German Research Foundation (DFG; JA 2174/5-1, nr. 383393940). Contributions to this research by H. J. Schenk were made possible by funding from the National Science Foundation (IOS-1558108).
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by Francisco M. Cánovas.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Kotowska, M.M., Thom, R., Zhang, Y. et al. Within-tree variability and sample storage effects of bordered pit membranes in xylem of Acer pseudoplatanus. Trees 34, 61–71 (2020). https://doi.org/10.1007/s00468-019-01897-4
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00468-019-01897-4