A semi-automated method for measuring xylem vessel length distribution

Pereira, Luciano; Miranda, Marcela T.; Pires, Gabriel S.; Pacheco, Vinícius S.; Guan, Xinyi; Kaack, Lucian; Karimi, Zohreh; Machado, Eduardo C.; Jansen, Steven; Tyree, Melvin T.; Ribeiro, Rafael V.

doi:10.1007/s40626-020-00189-4

Published: 14 October 2020

A semi-automated method for measuring xylem vessel length distribution

Luciano Pereira ORCID: orcid.org/0000-0003-2225-2957^1,2,3,
Marcela T. Miranda^1,2,
Gabriel S. Pires²,
Vinícius S. Pacheco²,
Xinyi Guan³,
Lucian Kaack³,
Zohreh Karimi⁴,
Eduardo C. Machado¹,
Steven Jansen³,
Melvin T. Tyree⁵ &
Rafael V. Ribeiro²

Theoretical and Experimental Plant Physiology volume 32, pages 331–340 (2020)Cite this article

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Abstract

Knowledge about the length of xylem vessels is essential to understand water transport in plants because these multicellular units show a 100-fold variation, from less than a centimeter to many meters. However, the available methods to estimate vessel length (VL) distribution are excessively time consuming and do not allow large and in-depth surveys. Here, we describe a semi-automated method to measure hydraulically-weighted VL (VL_H) using an automated Pneumatron device. Gas conductivity of a xylem tissue with a certain length is estimated with the Pneumatron in a straightforward and precise way, theoretically similar to the air-injection method. Besides giving results similar to the silicone-injection method, the pneumatic-based method enables faster and easier measurements of more than 50 samples per day, which is a significant advantage. Herein, a detailed description of the methodology is presented as well as the software and an R-script for data analysis. The method described represents an important contribution to studies on plant hydraulic architecture and can improve our understanding about the role of VL_H in plant performance under varying water availability.

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References

Bittencourt P, Pereira L, Oliveira R (2018) Pneumatic method to measure plant xylem embolism. Bio-Protocol 8:1–14. https://doi.org/10.21769/bioprotoc.3059
CAS Article Google Scholar
Cai J, Tyree MT (2010) The impact of vessel size on vulnerability curves: data and models for within-species variability in saplings of aspen Populus tremuloides Michx. Plant Cell Environ 33:1059–1069. https://doi.org/10.1111/j.1365-3040.2010.02127.x
Article PubMed Google Scholar
Cai J, Tyree MT (2014) Measuring vessel length in vascular plants: can we divine the truth? History, theory, methods, and contrasting models. Trees 28:643–655. https://doi.org/10.1007/s00468-014-0999-9
Article Google Scholar
Cohen S, Bennink J, Tyree M (2003) Air method measurements of apple vessel length distributions with improved apparatus and theory. J Exp Bot 54:1889–1897. https://doi.org/10.1093/jxb/erg202
CAS Article PubMed Google Scholar
Greenidge KNH (1952) An approach to the study of vessel length in hardwood species. Am J Bot 39:570–574. https://doi.org/10.1002/j.1537-2197.1952.tb13070.x
Article Google Scholar
Jacobsen AL, Brandon Pratt R, Tobin MF et al (2012) A global analysis of xylem vessel length in woody plants. Am J Bot 99:1583–1591. https://doi.org/10.3732/ajb.1200140
Article PubMed Google Scholar
Jansen S, Guan X, Kaack L et al (2020) The pneumatron estimates xylem embolism resistance in angiosperms based on gas diffusion kinetics: a mini-review. Acta Hortic (in press)
Kaack L, Altaner CM, Carmesin C et al (2019) Function and three-dimensional structure of intervessel pit membranes in angiosperms: a review. IAWA J 40:673–702. https://doi.org/10.1163/22941932-40190259
Article Google Scholar
Levionnois S, Ziegler C, Jansen S et al (2020) Vulnerability and hydraulic segmentations at the stem–leaf transition: coordination across Neotropical trees. New Phytol. https://doi.org/10.1111/nph.16723
Article PubMed Google Scholar
Link RM, Schuldt B, Choat B et al (2018) Maximum-likelihood estimation of xylem vessel length distributions. J Theor Biol 455:329–341. https://doi.org/10.1016/j.jtbi.2018.07.036
Article PubMed Google Scholar
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. https://doi.org/10.1007/s00468-017-1610-y
Article Google Scholar
Medeiros JS, Lens F, Maherali H, Jansen S (2019) Vestured pits and scalariform perforation plate morphology modify the relationships between angiosperm vessel diameter, climate and maximum plant height. New Phytol 221:1802–1813. https://doi.org/10.1111/nph.15536
CAS Article PubMed Google Scholar
Pan R, Geng J, Cai J, Tyree MT (2015) A comparison of two methods for measuring vessel length in woody plants. Plant Cell Environ 38:2519–2526. https://doi.org/10.1111/pce.12566
CAS Article PubMed Google Scholar
Pereira L, Bittencourt PRL, Oliveira RS et al (2016) Plant pneumatics: stem air flow is related to embolism—new perspectives on methods in plant hydraulics. New Phytol 211:357–370. https://doi.org/10.1111/nph.13905
Article PubMed Google Scholar
Pereira L, Bittencourt PRL, Pacheco VS et al (2020) The pneumatron: an automated pneumatic apparatus for estimating xylem vulnerability to embolism at high temporal resolution. Plant Cell Environ 43:131–142. https://doi.org/10.1111/pce.13647
CAS Article PubMed Google Scholar
Scholz A, Klepsch M, Karimi Z, Jansen S (2013a) How to quantify conduits in wood? Front Plant Sci 4:1–11. https://doi.org/10.3389/fpls.2013.00056
Article Google Scholar
Scholz A, Rabaey D, Stein A et al (2013b) 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
Article PubMed Google Scholar
Sperry JS, Hacke UG, Wheeler JK (2005) Comparative analysis of end wall resistivity in xylem conduits. Plant Cell Environ 28:456–465. https://doi.org/10.1111/j.1365-3040.2005.01287.x
Article Google Scholar
Tyree MT, Zimmermann MH (2002) Xylem structure and the ascent of sap. Springer, Berlin
Book Google Scholar
Wang R, Zhang L, Zhang S et al (2014) Water relations of Robinia pseudoacacia L.: do vessels cavitate and refill diurnally or are R-shaped curves invalid in Robinia? Plant Cell Environ 37:2667–2678. https://doi.org/10.1111/pce.12315
Article PubMed Google Scholar
Wheeler JK, Sperry JS, Hacke UG, Hoang N (2005) Inter-vessel pitting and cavitation in woody Rosaceae and other vessel led 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
Article Google Scholar
Williamson VG, Milburn JA (2017) Xylem vessel length and distribution: does analysis method matter? A study using Acacia. Aust J Bot 65:292–303. https://doi.org/10.1071/BT16220
Article Google Scholar
Wu M, Zhang Y, Oya T et al (2020) Root xylem in three woody angiosperm species is not more vulnerable to embolism than stem xylem. Plant Soil 450:479–495. https://doi.org/10.1007/s11104-020-04525-0
CAS Article Google Scholar
Zhang Y, Carmesin C, Kaack L et al (2020) High porosity with tiny pore constrictions and unbending pathways characterize the 3D structure of intervessel pit membranes in angiosperm xylem. Plant Cell Environ 43:116–130. https://doi.org/10.1111/pce.13654
CAS Article PubMed Google Scholar
Zhang Y, Lamarque LJ, Torres-Ruiz JM et al (2018) Testing the plant pneumatic method to estimate xylem embolism resistance in stems of temperate trees. Tree Physiol 38:1016–1025. https://doi.org/10.1093/treephys/tpy015
Article PubMed PubMed Central Google Scholar

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Acknowledgements

The authors acknowledge the São Paulo Research Foundation (FAPESP, Brazil) for the research grant (E.C.M, R.V.R., L.P. and M.T.M., Grant 2019/15276-8), fellowship (L.P. and R.V.R., Grant 2017/14075‐3) and scholarship (M.T.M. and R.V.R., Grant 2018/09834‐5). E.C.M. and R.V.R. are fellows of the National Council for Scientific and Technological Development (CNPq, Brazil). S.J., L.K., and X.G. acknowledge financial support from the German Research Foundation (DFG, Project Nr. 383393940 and 410768178). We thank two anonymous reviewers for useful comments on an earlier version of this manuscript.

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Authors and Affiliations

Laboratory of Plant Physiology “Coaracy M. Franco”, Center R&D in Ecophysiology and Biophysics, Agronomic Institute (IAC), Campinas SP, Brazil
Luciano Pereira, Marcela T. Miranda & Eduardo C. Machado
Laboratory of Crop Physiology, Department of Plant Biology, Institute of Biology, University of Campinas (UNICAMP), Campinas SP, Brazil
Luciano Pereira, Marcela T. Miranda, Gabriel S. Pires, Vinícius S. Pacheco & Rafael V. Ribeiro
Institute of Systematic Botany and Ecology, Ulm University, Ulm, Germany
Luciano Pereira, Xinyi Guan, Lucian Kaack & Steven Jansen
Department of Biology, Faculty of Science, Golestan University, Gorgan, Iran
Zohreh Karimi
College of Chemistry and Life Sciences, Zhejiang Normal University, Jinhua, 321004, China
Melvin T. Tyree

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Luciano Pereira
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Marcela T. Miranda
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Gabriel S. Pires
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Vinícius S. Pacheco
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Xinyi Guan
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Lucian Kaack
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Zohreh Karimi
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Eduardo C. Machado
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Steven Jansen
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Melvin T. Tyree
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Rafael V. Ribeiro
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Correspondence to Luciano Pereira or Rafael V. Ribeiro.

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Pereira, L., Miranda, M.T., Pires, G.S. et al. A semi-automated method for measuring xylem vessel length distribution. Theor. Exp. Plant Physiol. 32, 331–340 (2020). https://doi.org/10.1007/s40626-020-00189-4

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Received: 03 August 2020
Accepted: 03 October 2020
Published: 14 October 2020
Issue Date: December 2020
DOI: https://doi.org/10.1007/s40626-020-00189-4

Keywords

Plant hydraulics
Pneumatic method
Pneumatron
Vessel
Xylem
Water relations