Non-invasive hydrodynamic imaging in plant roots at cellular resolution

Flavius C Pascut; Valentin Couvreur; Daniela Dietrich; Nicky Leftley; Guilhem Reyt; Yann Boursiac; Monica Calvo-Polanco; Ilda Casimiro; Christophe Maurel; David E Salt; Xavier Draye; Darren M Wells; Malcolm J Bennett; Kevin F Webb

doi:10.1038/s41467-021-24913-z

Non-invasive hydrodynamic imaging in plant roots at cellular resolution

Flavius C Pascut, Valentin Couvreur, Daniela Dietrich, Nicky Leftley, Guilhem Reyt, Yann Boursiac, Monica Calvo-Polanco, Ilda Casimiro, Christophe Maurel, David E Salt, Xavier Draye, Darren M Wells, Malcolm J Bennett, Kevin F Webb

School of Biological Sciences

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Abstract

A key impediment to studying water-related mechanisms in plants is the inability to non-invasively image water fluxes in cells at high temporal and spatial resolution. Here, we report that Raman microspectroscopy, complemented by hydrodynamic modelling, can achieve this goal - monitoring hydrodynamics within living root tissues at cell- and sub-second-scale resolutions. Raman imaging of water-transporting xylem vessels in Arabidopsis thaliana mutant roots reveals faster xylem water transport in endodermal diffusion barrier mutants. Furthermore, transverse line scans across the root suggest water transported via the root xylem does not re-enter outer root tissues nor the surrounding soil when en-route to shoot tissues if endodermal diffusion barriers are intact, thereby separating 'two water worlds'.

Original language	English
Article number	4682
Pages (from-to)	4682
Journal	Nature Communications
Volume	12
Issue number	1
Early online date	3 Aug 2021
DOIs	https://doi.org/10.1038/s41467-021-24913-z
Publication status	Published - Dec 2021

Bibliographical note

Funding Information:
This work was supported by awards from the Biotechnology and Biological Sciences Research Council (grant Nos. BB/K010212/1 to K.F.W., BB/T001437/1 to M.J.B./D.M.W., BB/V003534/1 to D.E.S./M.J.B., BB/L027739/1, and BB/N023927/1 to D.E.S.) The Leverhulme Trust (RPG-2016-409, to M.J.B./D.M.W./K.F.W.), and from the ERA-NET Coordinating Action in Plant Sciences program (ERACAPS13.089_RootBarriers to DES). V.C. was funded by as Research Fellow by the Belgian Fonds de la Recherche Scientifique (F.R.S.-FNRS, grant number: 1208619F), M.C.-P. has received funding from the EU’s Seventh Framework Program under grant agreement N° FP7-609398 (AgreenSkills + contract), I.C. was funded by Junta de Extremadura Spain (GR18168). K.F.W. was funded by a Royal Academy of Engineering/EPSRC Postdoctoral Fellowship (EP/G058121/1).

Publisher Copyright:
© 2021, The Author(s).

Keywords

Arabidopsis/anatomy & histology
Biological Transport
Hydrodynamics
Models, Biological
Mutation
Plant Roots/anatomy & histology
Plant Shoots/metabolism
Plant Stomata/metabolism
Spectrum Analysis, Raman
Water/metabolism
Xylem/metabolism

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title = "Non-invasive hydrodynamic imaging in plant roots at cellular resolution",

abstract = "A key impediment to studying water-related mechanisms in plants is the inability to non-invasively image water fluxes in cells at high temporal and spatial resolution. Here, we report that Raman microspectroscopy, complemented by hydrodynamic modelling, can achieve this goal - monitoring hydrodynamics within living root tissues at cell- and sub-second-scale resolutions. Raman imaging of water-transporting xylem vessels in Arabidopsis thaliana mutant roots reveals faster xylem water transport in endodermal diffusion barrier mutants. Furthermore, transverse line scans across the root suggest water transported via the root xylem does not re-enter outer root tissues nor the surrounding soil when en-route to shoot tissues if endodermal diffusion barriers are intact, thereby separating 'two water worlds'.",

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author = "Pascut, {Flavius C} and Valentin Couvreur and Daniela Dietrich and Nicky Leftley and Guilhem Reyt and Yann Boursiac and Monica Calvo-Polanco and Ilda Casimiro and Christophe Maurel and Salt, {David E} and Xavier Draye and Wells, {Darren M} and Bennett, {Malcolm J} and Webb, {Kevin F}",

note = "Funding Information: This work was supported by awards from the Biotechnology and Biological Sciences Research Council (grant Nos. BB/K010212/1 to K.F.W., BB/T001437/1 to M.J.B./D.M.W., BB/V003534/1 to D.E.S./M.J.B., BB/L027739/1, and BB/N023927/1 to D.E.S.) The Leverhulme Trust (RPG-2016-409, to M.J.B./D.M.W./K.F.W.), and from the ERA-NET Coordinating Action in Plant Sciences program (ERACAPS13.089_RootBarriers to DES). V.C. was funded by as Research Fellow by the Belgian Fonds de la Recherche Scientifique (F.R.S.-FNRS, grant number: 1208619F), M.C.-P. has received funding from the EU{\textquoteright}s Seventh Framework Program under grant agreement N° FP7-609398 (AgreenSkills + contract), I.C. was funded by Junta de Extremadura Spain (GR18168). K.F.W. was funded by a Royal Academy of Engineering/EPSRC Postdoctoral Fellowship (EP/G058121/1). Publisher Copyright: {\textcopyright} 2021, The Author(s).",

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doi = "10.1038/s41467-021-24913-z",

language = "English",

volume = "12",

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T1 - Non-invasive hydrodynamic imaging in plant roots at cellular resolution

AU - Pascut, Flavius C

AU - Couvreur, Valentin

AU - Dietrich, Daniela

AU - Leftley, Nicky

AU - Reyt, Guilhem

AU - Boursiac, Yann

AU - Calvo-Polanco, Monica

AU - Casimiro, Ilda

AU - Maurel, Christophe

AU - Salt, David E

AU - Draye, Xavier

AU - Wells, Darren M

AU - Bennett, Malcolm J

AU - Webb, Kevin F

N1 - Funding Information: This work was supported by awards from the Biotechnology and Biological Sciences Research Council (grant Nos. BB/K010212/1 to K.F.W., BB/T001437/1 to M.J.B./D.M.W., BB/V003534/1 to D.E.S./M.J.B., BB/L027739/1, and BB/N023927/1 to D.E.S.) The Leverhulme Trust (RPG-2016-409, to M.J.B./D.M.W./K.F.W.), and from the ERA-NET Coordinating Action in Plant Sciences program (ERACAPS13.089_RootBarriers to DES). V.C. was funded by as Research Fellow by the Belgian Fonds de la Recherche Scientifique (F.R.S.-FNRS, grant number: 1208619F), M.C.-P. has received funding from the EU’s Seventh Framework Program under grant agreement N° FP7-609398 (AgreenSkills + contract), I.C. was funded by Junta de Extremadura Spain (GR18168). K.F.W. was funded by a Royal Academy of Engineering/EPSRC Postdoctoral Fellowship (EP/G058121/1). Publisher Copyright: © 2021, The Author(s).

PY - 2021/12

Y1 - 2021/12

N2 - A key impediment to studying water-related mechanisms in plants is the inability to non-invasively image water fluxes in cells at high temporal and spatial resolution. Here, we report that Raman microspectroscopy, complemented by hydrodynamic modelling, can achieve this goal - monitoring hydrodynamics within living root tissues at cell- and sub-second-scale resolutions. Raman imaging of water-transporting xylem vessels in Arabidopsis thaliana mutant roots reveals faster xylem water transport in endodermal diffusion barrier mutants. Furthermore, transverse line scans across the root suggest water transported via the root xylem does not re-enter outer root tissues nor the surrounding soil when en-route to shoot tissues if endodermal diffusion barriers are intact, thereby separating 'two water worlds'.

AB - A key impediment to studying water-related mechanisms in plants is the inability to non-invasively image water fluxes in cells at high temporal and spatial resolution. Here, we report that Raman microspectroscopy, complemented by hydrodynamic modelling, can achieve this goal - monitoring hydrodynamics within living root tissues at cell- and sub-second-scale resolutions. Raman imaging of water-transporting xylem vessels in Arabidopsis thaliana mutant roots reveals faster xylem water transport in endodermal diffusion barrier mutants. Furthermore, transverse line scans across the root suggest water transported via the root xylem does not re-enter outer root tissues nor the surrounding soil when en-route to shoot tissues if endodermal diffusion barriers are intact, thereby separating 'two water worlds'.

KW - Arabidopsis/anatomy & histology

KW - Biological Transport

KW - Hydrodynamics

KW - Models, Biological

KW - Mutation

KW - Plant Roots/anatomy & histology

KW - Plant Shoots/metabolism

KW - Plant Stomata/metabolism

KW - Spectrum Analysis, Raman

KW - Water/metabolism

KW - Xylem/metabolism

U2 - 10.1038/s41467-021-24913-z

DO - 10.1038/s41467-021-24913-z

M3 - Article (Academic Journal)

C2 - 34344886

SN - 2041-1723

VL - 12

SP - 4682

JO - Nature Communications

JF - Nature Communications

IS - 1

M1 - 4682

ER -

Non-invasive hydrodynamic imaging in plant roots at cellular resolution

Abstract

Bibliographical note

Keywords

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