Multimodal correlative imaging and modelling of phosphorus uptake from soil by hyphae of mycorrhizal fungi
Multimodal correlative imaging and modelling of phosphorus uptake from soil by hyphae of mycorrhizal fungi
Phosphorus (P) is essential for plant growth. Arbuscular mycorrhizal fungi (AMF) aid its uptake by acquiring P from sources distant from roots in return for carbon. Little is known about how AMF colonise soil pore-space, and models of AMF-enhanced P-uptake are poorly validated. We used synchrotron X-ray computed tomography to visualize mycorrhizas in soil and synchrotron X-ray fluorescence/X-ray absorption near edge structure (XRF/XANES) elemental mapping for P, sulphur (S) and aluminium (Al) in combination with modelling. We found that AMF inoculation had a suppressive effect on colonisation by other soil fungi and identified differences in structure and growth rate between hyphae of AMF and nonmycorrhizal fungi. Our results showed that AMF co-locate with areas of high P and low Al, and preferentially associate with organic-type P species over Al-rich inorganic P. We discovered that AMF avoid Al-rich areas as a source of P. Sulphur-rich regions were found to be correlated with higher hyphal density and an increased organic-associated P-pool, whilst oxidized S-species were found close to AMF hyphae. Increased S oxidation close to AMF suggested the observed changes were microbiome-related. Our experimentally-validated model led to an estimate of P-uptake by AMF hyphae that is an order of magnitude lower than rates previously estimated – a result with significant implications for the modelling of plant–soil–AMF interactions.
X-ray computed tomography, X-ray fluorescence, mycorrhizas, plant phosphorus uptake, rhizosphere modelling, synchrotron
688-703
Keyes, Samuel D
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Van Veelen, Arjen
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Mckay Fletcher, Daniel
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Scotson, Callum
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Koebernick, Nicolai
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Petroselli, Chiara
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Williams, Katherine
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Ruiz, Siul Aljadi
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Cooper, Laura
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Mayon, Robert B
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Duncan, Simon
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Dumont, Marc
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Jakobsen, Iver
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Oldroyd, Giles
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Tkacz, Andrzej
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Poole, Philip
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Mosselmans, Fred
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Borca, Camelia
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Huthwelker, Thomas
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Jones, David L.
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Roose, Tiina
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April 2022
Keyes, Samuel D
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Van Veelen, Arjen
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Mckay Fletcher, Daniel
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Scotson, Callum
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Koebernick, Nicolai
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Petroselli, Chiara
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Williams, Katherine
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Ruiz, Siul Aljadi
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Cooper, Laura
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Mayon, Robert B
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Duncan, Simon
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Dumont, Marc
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Jakobsen, Iver
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Oldroyd, Giles
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Tkacz, Andrzej
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Poole, Philip
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Mosselmans, Fred
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Borca, Camelia
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Huthwelker, Thomas
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Jones, David L.
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Roose, Tiina
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Keyes, Samuel D, Van Veelen, Arjen, Mckay Fletcher, Daniel, Scotson, Callum, Koebernick, Nicolai, Petroselli, Chiara, Williams, Katherine, Ruiz, Siul Aljadi, Cooper, Laura, Mayon, Robert B, Duncan, Simon, Dumont, Marc, Jakobsen, Iver, Oldroyd, Giles, Tkacz, Andrzej, Poole, Philip, Mosselmans, Fred, Borca, Camelia, Huthwelker, Thomas, Jones, David L. and Roose, Tiina
(2022)
Multimodal correlative imaging and modelling of phosphorus uptake from soil by hyphae of mycorrhizal fungi.
New Phytologist, 234 (2), .
(doi:10.1111/nph.17980).
Abstract
Phosphorus (P) is essential for plant growth. Arbuscular mycorrhizal fungi (AMF) aid its uptake by acquiring P from sources distant from roots in return for carbon. Little is known about how AMF colonise soil pore-space, and models of AMF-enhanced P-uptake are poorly validated. We used synchrotron X-ray computed tomography to visualize mycorrhizas in soil and synchrotron X-ray fluorescence/X-ray absorption near edge structure (XRF/XANES) elemental mapping for P, sulphur (S) and aluminium (Al) in combination with modelling. We found that AMF inoculation had a suppressive effect on colonisation by other soil fungi and identified differences in structure and growth rate between hyphae of AMF and nonmycorrhizal fungi. Our results showed that AMF co-locate with areas of high P and low Al, and preferentially associate with organic-type P species over Al-rich inorganic P. We discovered that AMF avoid Al-rich areas as a source of P. Sulphur-rich regions were found to be correlated with higher hyphal density and an increased organic-associated P-pool, whilst oxidized S-species were found close to AMF hyphae. Increased S oxidation close to AMF suggested the observed changes were microbiome-related. Our experimentally-validated model led to an estimate of P-uptake by AMF hyphae that is an order of magnitude lower than rates previously estimated – a result with significant implications for the modelling of plant–soil–AMF interactions.
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Accepted/In Press date: 3 January 2022
e-pub ahead of print date: 19 January 2022
Published date: April 2022
Additional Information:
Funding Information:
AvV, SK, RM, CS, DMF, SR, CP, KW and TR were funded by ERC Consolidator Grant no. 646809‐DIMR. NK, LC and TR were funded by BBSRC SARISA BB/L02620/1, SD was funded by BBSRC Case Studentship BB/L502625/1, DMF was funded by an EPSRC PhD studentship, TR was also funded by BBSRC BB/P004180/1, NERC NE/L00237/1, EPSRC EP/M020355/1, and AT and PP were funded by BBSRC grants BB/N013387/1 and BB/R017859/1. We would also like to acknowledge the help of Dr Keith Daily in modelling and Pengrui Cai in sequencing analysis. Finally, we gratefully acknowledge the support of the US Department of Energy through the LANL/LDRD Program and the G. T. Seaborg Institute to AvV. Los Alamos National Laboratory is operated by Triad National Security, LLC, for the National Nuclear Security Administration of the US Department of Energy (contract no. 89233218CNA000001).
Funding Information:
AvV, SK, RM, CS, DMF, SR, CP, KW and TR were funded by ERC Consolidator Grant no. 646809-DIMR. NK, LC and TR were funded by BBSRC SARISA BB/L02620/1, SD was funded by BBSRC Case Studentship BB/L502625/1, DMF was funded by an EPSRC PhD studentship, TR was also funded by BBSRC BB/P004180/1, NERC NE/L00237/1, EPSRC EP/M020355/1, and AT and PP were funded by BBSRC grants BB/N013387/1 and BB/R017859/1. We would also like to acknowledge the help of Dr Keith Daily in modelling and Pengrui Cai in sequencing analysis. Finally, we gratefully acknowledge the support of the US Department of Energy through the LANL/LDRD Program and the G. T. Seaborg Institute to AvV. Los Alamos National Laboratory is operated by Triad National Security, LLC, for the National Nuclear Security Administration of the US Department of Energy (contract no. 89233218CNA000001).
Publisher Copyright:
© 2022 The Authors New Phytologist © 2022 New Phytologist Foundation
Keywords:
X-ray computed tomography, X-ray fluorescence, mycorrhizas, plant phosphorus uptake, rhizosphere modelling, synchrotron
Identifiers
Local EPrints ID: 454110
URI: http://eprints.soton.ac.uk/id/eprint/454110
ISSN: 0028-646X
PURE UUID: d5a7a2bc-5360-4f89-b7c5-39a85a49c71b
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Date deposited: 31 Jan 2022 17:43
Last modified: 17 Mar 2024 04:01
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Contributors
Author:
Arjen Van Veelen
Author:
Daniel Mckay Fletcher
Author:
Callum Scotson
Author:
Nicolai Koebernick
Author:
Chiara Petroselli
Author:
Robert B Mayon
Author:
Simon Duncan
Author:
Iver Jakobsen
Author:
Giles Oldroyd
Author:
Andrzej Tkacz
Author:
Philip Poole
Author:
Fred Mosselmans
Author:
Camelia Borca
Author:
Thomas Huthwelker
Author:
David L. Jones
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