Advertisement

Trees

pp 1–11 | Cite as

Within-tree variability and sample storage effects of bordered pit membranes in xylem of Acer pseudoplatanus

  • Martyna M. KotowskaEmail author
  • Rebecca Thom
  • Ya Zhang
  • H. Jochen Schenk
  • Steven Jansen
Original Article

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.

Keywords

Bordered pit Electron microscopy Pit membrane Vessel Wood anatomy 

Notes

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).

Supplementary material

468_2019_1897_MOESM1_ESM.docx (8.3 mb)
Supplementary material 1 (DOCX 8454 kb)

References

  1. 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 105:293–301CrossRefPubMedGoogle Scholar
  2. 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 CrossRefGoogle Scholar
  3. 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 6:196–203CrossRefGoogle Scholar
  4. Brodribb TJ, Skelton RP, McAdam SAM et al (2016) Visual quantification of embolism reveals leaf vulnerability to hydraulic failure. New Phytol 209:1403–1409CrossRefPubMedGoogle Scholar
  5. 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 29:229–239CrossRefPubMedGoogle Scholar
  6. 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, WestportGoogle Scholar
  7. 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 131:41–48CrossRefPubMedPubMedCentralGoogle Scholar
  8. 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 55:1569–1575CrossRefPubMedGoogle Scholar
  9. Choat B, Lahr EC, Melcher PJ et al (2005) The spatial pattern of air seeding thresholds in mature sugar maple trees. Plant Cell Environ 28:1082–1089CrossRefGoogle Scholar
  10. 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 93:993–1000CrossRefPubMedGoogle Scholar
  11. Choat B, Cobb AR, Jansen S (2008) Structure and function of bordered pits: new discoveries and impacts on whole-plant hydraulic function. New Phytol 177:608–626CrossRefPubMedGoogle Scholar
  12. Choat B, Jansen S, Brodribb TJ et al (2012) Global convergence in the vulnerability of forests to drought. Nature 491:752CrossRefPubMedGoogle Scholar
  13. Czaninski Y (1979) Cytochimie ultrastructurale des parois du xyleme secondaire. Biol Cell 35:97–102Google Scholar
  14. 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 22:91–104CrossRefPubMedGoogle Scholar
  15. 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 93:1588–1600CrossRefPubMedGoogle Scholar
  16. Fang L, Catchmark JM (2014) Characterization of water-soluble exopolysaccharides from Gluconacetobacter xylinus and their impacts on bacterial cellulose crystallization and ribbon assembly. Cellulose 21:3965–3978CrossRefGoogle Scholar
  17. Giraudoux P (2017) “pgirmess”: data analysis in ecology. R package version 1.6.7. https://CRAN.R-project.org/package=pgirmess
  18. Hacke UG, Sperry JS, Pittermann J (2000) Drought experience and cavitation resistance in six shrubs from the Great Basin, Utah. Basic Appl Ecol 1:31–41CrossRefGoogle Scholar
  19. 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 CrossRefPubMedGoogle Scholar
  20. Hacke UG, Sperry JS, Wheeler JK, Castro L (2006) Scaling of angiosperm xylem structure with safety and efficiency. Tree Physiol 26:689–701CrossRefPubMedGoogle Scholar
  21. 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 115:187–199CrossRefPubMedPubMedCentralGoogle Scholar
  22. 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 39:1886–1894CrossRefPubMedGoogle Scholar
  23. Jansen S, Schenk HJ (2015) On the ascent of sap in the presence of bubbles. Am J Bot 102:1561–1563CrossRefPubMedGoogle Scholar
  24. Jansen S, Pletsers A, Sano Y (2008) The effect of preparation techniques on SEM-imaging of pit membranes. IAWA J 29:161–178CrossRefGoogle Scholar
  25. Jansen S, Choat B, Pletsers A (2009) Morphological variation of intervessel pit membranes and implications to xylem function in angiosperms. Am J Bot 96:409–419CrossRefPubMedGoogle Scholar
  26. Jansen S, Klepsch M, Li S et al (2018) Challenges in understanding air-seeding in angiosperm xylem. Acta Hortic 1222:13–20CrossRefGoogle Scholar
  27. 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 36:983–993CrossRefPubMedGoogle Scholar
  28. Kadunc A (2007) Factors influencing the formation of heartwood discolouration in sycamore (Acer pseudoplatanus L.). Eur J For Res 126:349–358CrossRefGoogle Scholar
  29. 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 19:31–37CrossRefPubMedGoogle Scholar
  30. 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 CrossRefPubMedPubMedCentralGoogle Scholar
  31. 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 69:5611–5623PubMedPubMedCentralGoogle Scholar
  32. 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 6:191CrossRefPubMedPubMedCentralGoogle Scholar
  33. 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 CrossRefPubMedGoogle Scholar
  34. 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 37:152–171CrossRefGoogle Scholar
  35. 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 32:51–60CrossRefGoogle Scholar
  36. 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 221:1831–1842CrossRefPubMedGoogle Scholar
  37. Martinez-Sanz M, Pettolino F, Flanagan B et al (2017) Structure of cellulose microfibrils in mature cotton fibres. Carbohydr Polym 175:450–463CrossRefPubMedGoogle Scholar
  38. 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 CrossRefPubMedGoogle Scholar
  39. 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 CrossRefGoogle Scholar
  40. 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 27:1401–1405CrossRefPubMedGoogle Scholar
  41. 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 32:1434–1441CrossRefPubMedGoogle Scholar
  42. 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 17:988–997CrossRefPubMedGoogle Scholar
  43. Pereira L, Domingues-Junior AP, Jansen S et al (2018) Is embolism resistance in plant xylem associated with quantity and characteristics of lignin? Trees 32:349–358CrossRefGoogle Scholar
  44. Pesacreta TC, Groom LH, Rials TG (2005) Atomic force microscopy of the intervessel pit membrane in the stem of Sapium sebiferum (Euphorbiaceae). IAWA J 26:397–426CrossRefGoogle Scholar
  45. 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 121:129–141CrossRefPubMedPubMedCentralGoogle Scholar
  46. Schacht H (1859) Über die Tüpfel der Gefäss-und Holzzellen. Bot Zeitung 17:238–239Google Scholar
  47. Schenk HJ, Espino S, Romo DM et al (2017) Xylem surfactants introduce a new element to the cohesion-tension theory. Plant Physiol 173:1177–1196CrossRefPubMedGoogle Scholar
  48. 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 105:172–185CrossRefPubMedGoogle Scholar
  49. Schmid R, Machado RD (1968) Pit membranes in hardwoods—fine structure and development. Protoplasma 66:185–204CrossRefGoogle Scholar
  50. 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 CrossRefPubMedGoogle Scholar
  51. 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 210:443–458CrossRefPubMedGoogle Scholar
  52. Schulte PJ, Gibson AC (1988) Hydraulic conductance and tracheid anatomy in six species of extant seed plants. Can J Bot 66:1073–1079CrossRefGoogle Scholar
  53. 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 85:613–624CrossRefGoogle Scholar
  54. Skelton RP, Brodribb TJ, Choat B (2017) Casting light on xylem vulnerability in an herbaceous species reveals a lack of segmentation. New Phytol 214:561–569CrossRefPubMedGoogle Scholar
  55. Sperry JS, Hacke UG (2004) Analysis of circular bordered pit function I. Angiosperm vessels with homogenous pit membranes. Am J Bot 91:369–385CrossRefPubMedGoogle Scholar
  56. 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 CrossRefGoogle Scholar
  57. Sperry JS, Tyree MT (1988) Mechanism of water stress-induced xylem embolism. Plant Physiol 88:581–587CrossRefPubMedPubMedCentralGoogle Scholar
  58. Sperry JS, Hacke UG, Pittermann J (2006) Size and function in conifer tracheids and angiosperm vessels. Am J Bot 93:1490–1500CrossRefPubMedGoogle Scholar
  59. 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):1736–1752CrossRefGoogle Scholar
  60. 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 114:325–334CrossRefPubMedPubMedCentralGoogle Scholar
  61. 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 CrossRefGoogle Scholar
  62. Tyree MT, Sperry JS (1989) Vulnerability of xylem to cavitation and embolism. Annu Rev Plant Biol 40:19–36CrossRefGoogle Scholar
  63. 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 CrossRefGoogle Scholar
  64. Zhang Y, Klepsch M, Jansen S (2017) Bordered pits in xylem of vesselless angiosperms and their possible misinterpretation as perforation plates. Plant Cell Environ 40:2133–2146CrossRefPubMedGoogle Scholar
  65. Zimmermann MH (1983) Xylem structure and the ascent of sap. Springer, New YorkCrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Institute of Systematic Botany and EcologyUlm UniversityUlmGermany
  2. 2.Albrecht-von-Haller Institute for Plant SciencesUniversity of GoettingenGöttingenGermany
  3. 3.Department of Biological ScienceCalifornia State University FullertonFullertonUSA

Personalised recommendations