The Pneumatron: An automated pneumatic apparatus for estimating xylem vulnerability to embolism at high temporal resolution.


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 2020
Historique:
received: 04 06 2019
revised: 16 08 2019
accepted: 20 08 2019
pubmed: 29 8 2019
medline: 24 11 2020
entrez: 29 8 2019
Statut: ppublish

Résumé

Xylem vulnerability to embolism represents an important trait to determine species distribution patterns and drought resistance. However, estimating embolism resistance frequently requires time-consuming and ambiguous hydraulic lab measurements. Based on a recently developed pneumatic method, we present and test the "Pneumatron", a device that generates high time-resolution and fully automated vulnerability curves. Embolism resistance is estimated by applying a partial vacuum to extract air from an excised xylem sample, while monitoring the pressure change over time. Although the amount of gas extracted is strongly correlated with the percentage loss of xylem conductivity, validation of the Pneumatron was performed by comparison with the optical method for Eucalyptus camaldulensis leaves. The Pneumatron improved the precision of the pneumatic method considerably, facilitating the detection of small differences in the (percentage of air discharged [PAD] < 0.47%). Hence, the Pneumatron can directly measure the 50% PAD without any fitting of vulnerability curves. PAD and embolism frequency based on the optical method were strongly correlated (r

Identifiants

pubmed: 31461536
doi: 10.1111/pce.13647
doi:

Substances chimiques

Water 059QF0KO0R

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

131-142

Informations de copyright

© 2019 John Wiley & Sons Ltd.

Références

Adams, H. D., Zeppel, M. J. B., Anderegg, W. R. L., Hartmann, H., Landhäusser, S. M., Tissue, D. T., … McDowell, N. G. (2017). A multi-species synthesis of physiological mechanisms in drought-induced tree mortality. Nature Ecology & Evolution, 1, 1285-1291. https://doi.org/10.1038/s41559-017-0248-x
Barros, F. V., Bittencourt, P. R. L., Brum, M., Restrepo-Coupe, N., Pereira, L., Teodoro, G. S., … Oliveira, R. S. (2019). Hydraulic traits explain differential responses of Amazonian forests to the 2015 El Nino-induced drought. New Phytologist, nph.15909. https://doi.org/10.1111/nph.15909
Brodersen, C. R., McElrone, A. J., Choat, B., Matthews, M. A., & Shackel, K. A. (2010). The dynamics of embolism repair in xylem: In vivo visualizations using high-resolution computed tomography. Plant Physiology, 154, 1088-1095. https://doi.org/10.1104/pp.110.162396
Brodribb, T. J., Skelton, R. P., Mcadam, S. A. M., Bienaimé, D., Lucani, C. J., & Marmottant, P. (2016). Visual quantification of embolism reveals leaf vulnerability to hydraulic failure. New Phytologist, 209, 1403-1409. https://doi.org/10.1111/nph.13846
Charrier, G., Torres-Ruiz, J. M., Badel, E., Burlett, R., Choat, B., Cochard, H., … Delzon, S. (2016). Evidence for hydraulic vulnerability segmentation and lack of xylem refilling under tension. Plant Physiology, 172, 1657-1668. https://doi.org/10.1104/pp.16.01079
Choat, B., Brodribb, T. J., Brodersen, C. R., Duursma, R. A., López, R., & Medlyn, B. E. (2018). Triggers of tree mortality under drought. Nature, 558, 531-539. https://doi.org/10.1038/s41586-018-0240-x
Cochard, H. (2002). A technique for measuring xylem hydraulic conductance under high negative pressures. Plant, Cell and Environment, 25, 815-819. https://doi.org/10.1046/j.1365-3040.2002.00863.x
Cochard, H., Badel, E., Herbette, S., Delzon, S., Choat, B., & Jansen, S. (2013). Methods for measuring plant vulnerability to cavitation: A critical review. Journal of Experimental Botany, 64, 4779-4791. https://doi.org/10.1093/jxb/ert193
Espino, S., & Schenk, H. J. (2011). Mind the bubbles: Achieving stable measurements of maximum hydraulic conductivity through woody plant samples. Journal of Experimental Botany, 62, 1119-1132. https://doi.org/10.1093/jxb/erq338
Hacke, U. G., Venturas, M. D., MacKinnon, E. D., Jacobsen, A. L., Sperry, J. S., & Pratt, R. B. (2015). The standard centrifuge method accurately measures vulnerability curves of long-vesselled olive stems. New Phytologist, 205, 116-127. https://doi.org/10.1111/nph.13017
Jansen, S., Gortan, E., Lens, F., Lo Gullo, M. A., Salleo, S., Scholz, A., … Nardini, A. (2011). Do quantitative vessel and pit characters account for ion-mediated changes in the hydraulic conductance of angiosperm xylem? New Phytologist, 189, 218-228. https://doi.org/10.1111/j.1469-8137.2010.03448.x
Jansen, S., Schuldt, B., & Choat, B. (2015). Current controversies and challenges in applying plant hydraulic techniques. New Phytologist, 205, 961-964. https://doi.org/10.1111/nph.13229
Lachenbruch, B., & McCulloh, K. A. (2014). Traits, properties, and performance: How woody plants combine hydraulic and mechanical functions in a cell, tissue, or whole plant. New Phytologist, 204, 747-764. https://doi.org/10.1111/nph.13035
Lamarque, L. J., Corso, D., Torres-Ruiz, J. M., Badel, E., Brodribb, T. J., Burlett, R., … Delzon, S. (2018). An inconvenient truth about xylem resistance to embolism in the model species for refilling Laurus nobilis L. Annals of Forest Science, 75, 88. https://doi.org/10.1007/s13595-018-0768-9
Melcher, P. J., Holbrook, N. M., Burns, M. J., Zwieniecki, M. A., Cobb, A. R., Brodribb, T. J., … Sack, L. (2012). Measurements of stem xylem hydraulic conductivity in the laboratory and field. Methods in Ecology and Evolution, 3, 685-694. https://doi.org/10.1111/j.2041-210X.2012.00204.x
Milburn, J. A. (1973). Cavitation in Ricinus by acoustic detection: Induction in excised leaves by various factors. Planta, 110, 253-265. https://doi.org/10.1007/BF00387637
Oliveira, R. S., Costa, F. R. C., van Baalen, E., de Jonge, A., Bittencourt, P. R., Almanza, Y., … Poorter, L. (2019). Embolism resistance drives the distribution of Amazonian rainforest tree species along hydro-topographic gradients. New Phytologist, 221, 1457-1465. https://doi.org/10.1111/nph.15463
Pammenter, N. W., & Vander, W. C. (1998). A mathematical and statistical analysis of the curves illustrating vulnerability of xylem to cavitation. Tree physiology, 18, 589-593. https://doi.org/10.1093/treephys/18.8-9.589
Pereira, L., Bittencourt, P. R. L., Oliveira, R. S., Junior, M. B. M., Barros, F. V., Ribeiro, R. V., & Mazzafera, P. (2016). Plant pneumatics: Stem air flow is related to embolism - new perspectives on methods in plant hydraulics. New Phytologist, 211, 357-370. https://doi.org/10.1111/nph.13905
Pereira, L., & Ribeiro, R. V. (2018). Radial stem flow and its importance when measuring xylem hydraulic conductance. Theoretical and Experimental Plant Physiology, 30, 71-75. https://doi.org/10.1007/s40626-018-0103-8
Pratt, R. B., Jacobsen, A. L., Ewers, F. W., & Davis, S. D. (2007). Relationships among xylem transport, biomechanics and storage in stems and roots of nine Rhamnaceae species of the California chaparral. New Phytologist, 174, 787-798. https://doi.org/10.1111/j.1469-8137.2007.02061.x
R Core Team (2013) R: A language and environment for statistical computing.
Rodriguez-Zaccaro, F. D., Valdovinos-Ayala, J., Percolla, M. I., Venturas, M. D., Pratt, R. B., & Jacobsen, A. L. (2019). Wood structure and function change with maturity: Age of the vascular cambium is associated with xylem changes in current-year growth. Plant, Cell & Environment, 42, 1816-1831. https://doi.org/10.1111/pce.13528
Sperry, J. S., Donnelly, J. R., & Tyree, M. T. (1988). A method for measuring hydraulic conductivity and embolisms in xylem. Plant, Cell & Environment, 11, 25-40.
Venturas, M. D., Pratt, R. B., Jacobsen, A. L., Castro, V., Fickle, J. C., & Hacke, U. G. (2019). Direct comparison of four methods to construct xylem vulnerability curves: differences among techniques are linked to vessel network characteristics. Plant, Cell & Environment, 1-15.
Vergeynst, L. L., Dierick, M., Bogaerts, J. A. N., Cnudde, V., & Steppe, K. (2014). Cavitation: A blessing in disguise? New method to establish vulnerability curves and assess hydraulic capacitance of woody tissues. Tree Physiology, 35, 400-409.
Yin, P., & Cai, J. (2018). New possible mechanisms of embolism formation when measuring vulnerability curves by air injection in a pressure sleeve. Plant, Cell & Environment, 41, 1361-1368. https://doi.org/10.1111/pce.13163
Zhang, Y., Lamarque, L. J., Torres-Ruiz, J. M., Schuldt, B., Karimi, Z., Li, S., … Jansen, S. (2018). Testing the plant pneumatic method to estimate xylem embolism resistance in stems of temperate trees. Tree Physiology, 38, 1016-1025. https://doi.org/10.1093/treephys/tpy015
Zhang, Y.-J., Rockwell, F. E., Graham, A. C., Alexander, T., & Holbrook, N. M. (2016). Reversible leaf xylem collapse: A potential “circuit breaker” against cavitation. Plant Physiology, 172, 2261-2274. https://doi.org/10.1104/pp.16.01191

Auteurs

Luciano Pereira (L)

Laboratory of Plant Physiology "Coaracy M. Franco", Center R&D in Ecophysiology and Biophysics, Agronomic Institute (IAC), Campinas, Brazil.
Laboratory of Crop Physiology, Department of Plant Biology, Institute of Biology, P.O. Box 6109, University of Campinas (UNICAMP), Campinas, 13083-970, Brazil.

Paulo R L Bittencourt (PRL)

College of Life and Environmental Sciences, University of Exeter, Exeter, United Kingdom.
Department of Plant Biology, Institute of Biology, P.O. Box 6109, UNICAMP, Campinas, 13083-970, Brazil.

Vinícius S Pacheco (VS)

Department of Plant Biology, Institute of Biology, P.O. Box 6109, UNICAMP, Campinas, 13083-970, Brazil.

Marcela T Miranda (MT)

Laboratory of Plant Physiology "Coaracy M. Franco", Center R&D in Ecophysiology and Biophysics, Agronomic Institute (IAC), Campinas, Brazil.

Ya Zhang (Y)

Institute of Systematic Botany and Ecology, Ulm University, Ulm, 89081, Germany.

Rafael S Oliveira (RS)

Department of Plant Biology, Institute of Biology, P.O. Box 6109, UNICAMP, Campinas, 13083-970, Brazil.

Peter Groenendijk (P)

Department of Plant Biology, Institute of Biology, P.O. Box 6109, UNICAMP, Campinas, 13083-970, Brazil.

Eduardo C Machado (EC)

Laboratory of Plant Physiology "Coaracy M. Franco", Center R&D in Ecophysiology and Biophysics, Agronomic Institute (IAC), Campinas, Brazil.

Melvin T Tyree (MT)

College of Chemistry and Life Sciences, Zhejiang Normal University, Jinhua, 321004, China.

Steven Jansen (S)

Institute of Systematic Botany and Ecology, Ulm University, Ulm, 89081, Germany.

Lucy Rowland (L)

College of Life and Environmental Sciences, University of Exeter, Exeter, United Kingdom.

Rafael V Ribeiro (RV)

Laboratory of Crop Physiology, Department of Plant Biology, Institute of Biology, P.O. Box 6109, University of Campinas (UNICAMP), Campinas, 13083-970, Brazil.

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