Alpine dwarf shrubs show high proportions of nonfunctional xylem: Visualization and quantification of species-specific patterns.
Ericaceae
embolism
growth form
hydraulic conductivity
hydraulic dysfunction
micro-CT
nondestructive imaging
water transport
woody plants
xylem anatomy
Journal
Plant, cell & environment
ISSN: 1365-3040
Titre abrégé: Plant Cell Environ
Pays: United States
ID NLM: 9309004
Informations de publication
Date de publication:
01 2022
01 2022
Historique:
revised:
15
07
2021
received:
13
04
2021
accepted:
15
07
2021
pubmed:
17
11
2021
medline:
23
2
2022
entrez:
16
11
2021
Statut:
ppublish
Résumé
Xylem conductive capacity is a key determinant of plant hydraulic function and intimately linked to photosynthesis and productivity, but can be impeded by temporary or permanent conduit dysfunctions. Here we show that persistent xylem dysfunctions in unstressed plants are frequent in Alpine dwarf shrubs and occur in various but species-specific cross-sectional patterns. Combined synchrotron micro-computed tomography (micro-CT) imaging, xylem staining, and flow measurements in saturated samples of six widespread Ericaceae species evidence a high proportion (19%-50%) of hydraulically nonfunctional xylem areas in the absence of drought stress, with regular distribution of dysfunctions between or within growth rings. Dysfunctions were only partly reversible and reduced the specific hydraulic conductivity to 1.38 to 3.57 ×10
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
55-68Subventions
Organisme : Austrian Science Fund FWF
ID : J 4300
Pays : Austria
Informations de copyright
© 2021 The Authors. Plant, Cell & Environment published by John Wiley & Sons Ltd.
Références
Alder, N.N., Pockman, W.T., Sperry, J.S. & Nuismer, S. (1997) Use of centrifugal force in the study of xylem cavitation. Journal of Experimental Botany, 48(3), 665-674.
Anadon-Rosell, A., Hasibeder, R., Palacio, S., Mayr, S., Ingrisch, J., Ninot, J.M. et al. (2017) Short-term carbon allocation dynamics in subalpine dwarf shrubs and their responses to experimental summer drought. Environmental and Experimental Botany, 141, 92-102.
Beikircher, B., Ameglio, T., Cochard, H. & Mayr, S. (2010) Limitation of the Cavitron technique by conifer pit aspiration. Journal of Experimental Botany, 61(12), 3382-3393.
Beikircher, B. & Mayr, S. (2016) Avoidance of harvesting and sampling artefacts in hydraulic analyses: a protocol tested on Malus domestica. Tree Physiology, 36(6), 797-803.
Bittencourt, P.R.L., Pereira, L. & Oliveira, R.S. (2016) On xylem hydraulic efficiencies, wood space-use and the safety-efficiency tradeoff. New Phytologist, 211(4), 1152-1155.
Brodersen, C.R., Roddy, A.B., Wason, J.W. & McElrone, A.J. (2019) Functional status of xylem through time. Annual Review of Plant Biology, 70, 407-433.
Brun, F., Pacilè, S., Accardo, A., Kourousias, G., Dreossi, D., Mancini, L. et al. (2015) Enhanced and flexible software tools for x-ray computed tomography at the Italian Synchrotron Radiation Facility Elettra. Fundamenta Informaticae, 141(2-3), 233-243.
Carrer, M., Pellizzari, E., Prendin, A.L., Pividori, M. & Brunetti, M. (2019) Winter precipitation - not summer temperature-is still the main driver for Alpine shrub growth. Science of the Total Environment, 682, 171-179.
Cernusca, A. (1976) Energie- und Wasserhaushalt eines alpinen Zwergstrauchbestandes während einer Föhnperiode. Archives for Meteorology, Geophysics, and Bioclimatology, Series B, 24, 219-241.
Choat, B., Jansen, S., Brodribb, T.J., Cochard, H., Delzon, S., Bhaskar, R. et al. (2012) Global convergence in the vulnerability of forests to drought. Nature, 491(7426), 752-756.
Choat, B., Brodersen, C.R. & McElrone, A.J. (2015) Synchrotron X-ray microtomography of xylem embolism in Sequoia sempervirens saplings during cycles of drought and recovery. New Phytologist, 205(3), 1095-1105.
Choat, B. & Pittermann, J. (2009) New insights into bordered pit structure and cavitation resistance in angiosperms and conifers. New Phytologist, 182(3), 557-560.
Cochard, H., Delzon, S. & Badel, E. (2015) X-ray microtomography (micro-CT): a reference technology for high-resolution quantification of xylem embolism in trees. Plant, Cell and Environment, 38(1), 201-206.
Crivellaro, A. & Büntgen, U. (2020) New evidence of thermally constrained plant cell wall lignification. Trends in Plant Science, 25(4), 322-324.
Dai, Y., Wang, L. & Wan, X. (2020) Frost fatigue and its spring recovery of xylem conduits in ring-porous, diffuse-porous, and coniferous species in situ. Plant Physiology and Biochemistry, 146, 177-186.
De Micco, V., Balzano, A. & Wheeler, E.A. (2016) Tyloses and gums: a review of structure, function and occurrence of vessel occlusions. IAWA Journal, 37(2), 186-205.
Espino, S. & Schenk, H.J. (2009) Hydraulically integrated or modular? Comparing whole-plant-level hydraulic systems between two desert shrub species with different growth forms. New Phytologist, 183(1), 142-152.
Ewers, F.W., Ewers, J.M., Jacobsen, A.L. & López-Portillo, J. (2007) Vessel redundancy: modeling safety in numbers. IAWA Journal, 28(4), 373-388.
Fukuda, K., Kawaguchi, D., Aihara, T., Ogasa, M.Y., Miki, N.H., Haishi, T. et al. (2015) Vulnerability to cavitation differs between current-year and older xylem: non-destructive observation with a compact magnetic resonance imaging system of two deciduous diffuse-porous species. Plant, Cell and Environment, 38(12), 2508-2518.
Ganthaler, A. & Mayr, S. (2015a) Dwarf shrub hydraulics: two Vaccinium species (V. myrtillus, V. vitis-idaea) of the European Alps compared. Physiologia Plantarum, 155(4), 424-434.
Ganthaler, A. & Mayr, S. (2015b) Vaccinium gaultherioides: another insight into water relations of alpine dwarf shrubs. Journal of Plant Hydraulics, 2, e-004.
Ganthaler, A. & Mayr, S. (2021) Subalpine dwarf shrubs differ in vulnerability to xylem cavitation: an innovative staining approach enables new insights. Physiologia Plantarum, 172, 2011-2021. Available from: https://doi.org/10.1111/ppl.13429
Gärtner, H., Lucchinetti, S. & Schweingruber, F.H. (2014) New perspectives for wood anatomical analysis in dendrosciences: the GSL1-microtome. Dendrochronologia, 32(1), 47-51.
Gauthey, A., Peters, J.M.R., Carins-Murphy, M.R., Rodriguez-Dominguez, C.M., Li, X., Delzon, S. et al. (2020) Visual and hydraulic techniques produce similar estimates of cavitation resistance in woody species. New Phytologist, 228(3), 884-897.
Gleason, S.M., Westoby, M., Jansen, S., Choat, B., Hacke, U.G., Pratt, R.B. et al. (2016) Weak tradeoff between xylem safety and xylem-specific hydraulic efficiency across the world's woody plant species. New Phytologist, 209(1), 123-136.
Grabherr, G. (1980) Variability and ecology of the alpine dwarf shrub community Loiseleurio-Cetrarietum. Vegetatio, 41(2), 111-120.
Guan, X., Pereira, L., McAdam, S., Cao, K.F. & Jansen, S. (2021) No gas source, no problem: Proximity to pre-existing embolism and segmentation affect embolism spreading in angiosperm xylem by gas diffusion. Plant, Cell and Environment, 44, 1329-1345. Available from: https://doi.org/10.1111/pce.14016
Hacke, U., Stiller, V., Sperry, J.S., Pittermann, J. & McCulloh, K.A. (2001) Cavitation fatigue. Embolism and refilling cycles can weaken the cavitation resistance of xylem. Plant Physiology, 125(2), 779-786.
Hargrave, K.R., Kolb, K.J., Ewers, F.W. & Davis, S.D. (1994) Conduit diameter and drought induced embolism in Salvia mellifera Greene (Labiatae). New Phytologist, 126(4), 695-705.
Hartmann, H. & Trumbore, S. (2016) Understanding the roles of non-structural carbohydrates in forest trees - From what we can measure to what we want to know. New Phytologist, 211(2), 386-403.
Hietz, P., Rosner, S., Sorz, J. & Mayr, S. (2008) Comparison of methods to quantify loss of hydraulic conductivity in Norway spruce. Annals of Forest Science, 65(5), 502.
Hölttä, T., Kurppa, M. & Nikinmaa, E. (2013) Scaling of xylem and phloem transport capacity and resource usage with tree size. Frontiers in Plant Science, 4, 496.
Hubbard, R.M., Stiller, V., Ryan, M.G. & Sperry, J.S. (2001) Stomatal conductance and photosynthesis vary linearly with plant hydraulic conductance in ponderosa pine. Plant, Cell and Environment, 24(1), 113-121.
Jacobsen, A.L., Pratt, R.B., Davis, S.D. & Ewers, F.W. (2007) Cavitation resistance and seasonal hydraulics differ among three arid Californian plant communities. Plant, Cell and Environment, 30(12), 1599-1609.
Jacobsen, A.L., Rodriguez-Zaccaro, F.D., Lee, T.F., Valdovinos, J., Toschi, H.S., Martinez, J.A. et al. (2015) Grapevine xylem development, architecture and function. In: Hacke, U.G. (Ed.) Functional and ecological xylem anatomy. Cham: Springer. pp. 133-162.
Jacobsen, A.L., Valdovinos-Ayala, J. & Pratt, R.B. (2018) Functional lifespans of xylem vessels: Development, hydraulic function, and post-function of vessels in several species of woody plants. American Journal of Botany, 105(2), 142-150.
Jimenez, S.M., Nadezhdina, N., Cermak, J. & Morales, D. (2000) Radial variation in sap flow in five laurel forest tree species in Tenerife, Canary Islands. Tree Physiology, 20(17), 1149-1156.
Kitin, P. & Funada, R. (2016) Earlywood vessels in ring-porous trees become functional for water transport after bud burst and before the maturation of the current-year leaves. IAWA Journal, 37(2), 315-331.
Klein, T., Zeppel, M.J.B., Anderegg, W.R.L., Bloemen, J., De Kauwe, M.G., Hudson, P. et al. (2018) Xylem embolism refilling and resilience against drought-induced mortality in woody plants: processes and trade-offs. Ecological Research, 33(5), 839-855.
Knipfer, T., Brodersen, C.R., Zedan, A., Kluepfel, D.A. & McElrone, A.J. (2015) Patterns of drought-induced embolism formation and spread in living walnut saplings visualized using X-ray microtomography. Tree Physiology, 35(7), 744-755.
Knipfer, T., Reyes, C., Earles, J.M., Berry, Z.C., Johnson, D., Brodersen, C.R. et al. (2019) Spatiotemporal coupling of vessel cavitation and discharge of stored xylem water in a tree sapling. Plant Physiology, 179(4), 1658-1668.
Körner, C. (2003) Alpine plant life. Functional plant ecology of high mountain ecosystems, 2nd edn. Berlin: Springer.
Kron, K.A., Judd, W.S., Stevens, P.F., Crayn, D.M., Anderberg, A.A., Gadek, P.A. et al. (2002) Phylogenetic classification of Ericaceae: Molecular and morphological evidence. Botanical Review, 68(3), 335-423.
Lamarque, L.J., Corso, D., Torres-Ruiz, J.M., Badel, E., Brodribb, T.J., Burlett, R. et al. (2018) An inconvenient truth about xylem resistance to embolism in the model species for refilling Laurus nobilis L. Annals of Forest Science, 75, 88.
Landolt, E. (2010) Flora indicativa. Ökologische Zeigerwerte und biologische Kennzeichen zur Flora der Schweiz und der Alpen, 2nd edition. Bern: Haupt Verlag.
Larcher, W., Bauer, H., Bendetta, G., Harrasser, J., Hilscher, H. & Mair, B. (1969) Anwendung und Zuverlässigkeit der Tetrazoliummethode zur Feststellung von Schäden in pflanzlichen Geweben. Mikroskopie, 25, 207-218.
Larcher, W. (2003) Physiological plant ecology: Ecophysiology and stress physiology of functional groups, 4th edition. Berlin Heidelberg New York: Springer.
Loepfe, L., Martinez-Vilalta, J., Pinol, J. & Mencuccini, M. (2007) The relevance of xylem network structure for plant hydraulic efficiency and safety. Journal of Theoretical Biology, 247(4), 788-803.
Losso, A., Bär, A., Dämon, B., Dullin, C., Ganthaler, A., Petruzzellis, F. et al. (2019) Insights from in vivo micro-CT analysis: testing the hydraulic vulnerability segmentation in Fagus sylvatica and Acer pseudoplatanus seedlings. New Phytologist, 221(4), 1831-1842.
Maestre, F.T., Eldridge, D.J. & Soliveres, S. (2016) A multifaceted view on the impacts of shrub encroachment. Applied Vegetation Science, 19(3), 369-370.
Maranon-Jiminez, S., Van den Bulcke, J., Piayda, A., Van Acker, J., Cuntz, M., Rebmann, C. et al. (2017) X-ray computed microtomography characterizes the wound effect that causes sap flow underestimation by thermal dissipation sensors. Tree Physiology, 38(2), 288-302.
Mayr, S. & Cochard, H. (2003) A new method for vulnerability analysis of small xylem areas reveals that compression wood of Norway spruce has lower hydraulic safety than opposite wood. Plant, Cell and Environment, 26(8), 1365-1371.
Mayr, S., Rothart, B. & Wolfschwenger, M. (2006) Temporal and spatial pattern of embolism induced by pressure collar techniques in twigs of Picea abies. Journal of Experimental Botany, 57(12), 3157-3163.
Mayr, S., Schmid, P., Beikircher, B., Feng, F. & Badel, E. (2020) Die hard: timberline conifers survive annual winter embolism. New Phytologist, 226(1), 13-20.
Melcher, P.J., Zwieniecki, M.A. & Holbrook, N.M. (2003) Vulnerability of xylem vessels to cavitation in sugar maple. Scaling from individual vessels to whole branches. Plant Physiology, 131(4), 1775-1780.
McCulloh, K.A. & Woodruff, D.R. (2012) Linking stomatal sensitivity and whole-tree hydraulic architecture. Tree Physiology, 32(4), 369-372.
McDowell, N., Barnard, H., Bond, B., Hinckley, T., Hubbard, R., Ishii, H. et al. (2002) The relationship between tree height and leaf area: sapwood area ratio. Oecologia, 132(1), 12-20.
Nadezhdina, N., Čermák, J. & Ceulemans, R. (2002) Radial patterns of sap flow in woody stems of dominant and understory species: scaling errors associated with positioning of sensors. Tree Physiology, 22(13), 907-918.
Nardini, A., Savi, T., Losso, A., Petit, G., Pacilè, S., Tromba, G. et al. (2017) X-ray microtomography observations of xylem embolism in stems of Laurus nobilis are consistent with hydraulic measurements of percentage loss of conductance. New Phytologist, 213(3), 1068-1075.
Neuner, G. (2014) Frost resistance in alpine woody plants. Frontiers in Plant Science, 5, 654.
Nolf, M., Rosani, A., Ganthaler, A., Beikircher, B. & Mayr, S. (2016) Herb hydraulics: Inter- and intraspecific variation in three Ranunculus species. Plant Physiology, 170(4), 2085-2094.
Paganin, D., Mayo, S.C., Gureyev, T.E., Miller, P.R. & Wilkins, S.W. (2002) Simultaneous phase and amplitude extraction from a single defocused image of a homogeneous object. Journal of Microscopy, 206(1), 33-40.
Petit, G. & Anfodillo, T. (2009) Plant physiology in theory and practice: Analysis is of the WBE model for vascular plants. Journal of Theoretical Biology, 259(1), 1-4.
Petruzzellis, F., Pagliarani, C., Savi, T., Losso, A., Cavalletto, S., Tromba, G. et al. (2018) The pitfalls of in vivo imaging techniques: evidence for cellular damage caused by synchrotron X-ray computed micro-tomography. New Phytologist, 220(1), 104-110.
Pratt, R.B. & Jacobsen, A.L. (2017) Conflicting demands on angiosperm xylem: tradeoffs among storage, transport and biomechanics. Plant, Cell and Environment, 40(6), 897-913.
Roth-Nebelsick, A. (2019) It's contagious: calculation and analysis of xylem vulnerability to embolism by a mechanistic approach based on epidemic modelling. Trees, 33(5), 1519-1533.
Sanchez-Martinez, P., Martinez-Vilalta, J., Dexter, K.G., Segovia, R.A. & Mencuccini, M. (2020) Adaptation and coordinated evolution of plant hydraulic traits. Ecology Letters, 23(11), 1599-1610.
Schenk, H.J., Espino, S., Goedhart, C.M., Nordenstahl, M., Martinez-Cabrera, H.I. & Jones, C.S. (2008) Hydraulic integration and shrub growth form linked across continental aridity gradients. Proceedings of the National Academy of Sciences of the United States of America, 105(32), 11248-11253.
Schweingruber, F.H., Börner, A. & Schulze, E.D. (2011) Atlas of stem anatomy in herbs, shrubs and trees. Berlin: Springer.
Schweingruber, F.H. & Landolt, W. (2005) The xylem database. A web production of the Swiss Federal Research Institute WSL. Available at: https://www.wsl.ch/dendroprot/xylemdb [Accessed 19th November 2020].
Secchi, F., Pagliarani, C. & Zwieniecki, M.A. (2017) The functional role of xylem parenchyma cells and aquaporins during recovery from severe water stress. Plant, Cell and Environment, 40(6), 858-871.
Sergent, A.S., Varela, S.A., Barigah, T.S., Badel, E., Cochard, H., Dalla-Salda, G. et al. (2020) A comparison of five methods to assess embolism resistance in trees. Forest Ecology and Management, 468(15), 118175.
Sperry, J.S. (2003) Evolution of water transport and xylem structure. International Journal of Plant Sciences, 164(S3), 115-127.
Sperry, J.S. (2013) Cutting-edge research or cutting-edge artefact? An overdue control experiment complicates the xylem refilling story. Plant, Cell and Environment, 36(11), 1916-1918.
Sperry, J.S., Donnelly, J.R. & Tyree, M.T. (1988) A method for measuring hydraulic conductivity and embolism in xylem. Plant, Cell and Environment, 11(1), 35-40.
Sperry, J.S. & Sullivan, J.E.M. (1992) Xylem embolism in response to freeze-thaw cycles and water stress in ring-porous, diffuse-porous, and conifer species. Plant Physiology, 100(2), 605-613.
Sturite, I., Henriksen, T.M. & Breland, T.A. (2005) Distinguishing between metabolically active and inactive roots by combined staining with 2,3,5-triphenyltetrazolium chloride and image colour analysis. Plant and Soil, 271(1), 75-82.
Taneda, H. & Sperry, J.S. (2008) A case-study of water transport in co-occurring ring- versus diffuse-porous trees: contrasts in water-status, conducting capacity, cavitation and vessel refilling. Tree Physiology, 28(11), 1641-1651.
Tyree, M.T. & Zimmermann, M.H. (2002) Xylem structure and the ascent of sap. Berlin: Springer.
Umebayashi, T., Utsumi, Y., Koga, S., Inoue, S., Matsumura, J., Oda, K. et al. (2010) Xylem water-conducting patterns of 34 broadleaved evergreen trees in southern Japan. Trees, 24(3), 571-583.
Utsumi, Y., Sano, Y., Ohtani, J. & Fujikawa, S. (1996) Seasonal changes in the distribution of water in the outer growth rings of Fraxinus mandshurica var japonica: a study by cryo-scanning electron microscopy. IAWA Journal, 17(2), 113-124.
Utsumi, Y., Sano, Y., Fujikawa, S., Funada, R. & Ohtani, J. (1998) Visualization of cavitated vessels in winter and refilled vessels in spring in diffuse-porous trees by cryo-scanning electron microscopy. Plant Physiology, 117(4), 1463-1471.
Von Arx, G., Crivellaro, A., Prendin, A.L., Cufar, K. & Carrer, M. (2016) Quantitative wood anatomy-practical guidelines. Frontiers in Plant Science, 7, 781.
Wang, N., Liu, W., Huang, J. & Ma, K. (2014) The structure-mechanical relationship of palm vascular tissue. Journal of the Mechanical Behavior of Biomedical Materials, 36, 1-11.
Zhang, W., Feng, F. & Tyree, M.T. (2018) Seasonality of cavitation and frost fatigue in Acer mono Maxim. Plant, Cell & Environment, 41(6), 1278-1286.