Multimodal correlative imaging and modelling of phosphorus uptake from soil by hyphae of mycorrhizal fungi

Summary 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 synch...

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Published inThe New phytologist Vol. 234; no. 2; pp. 688 - 703
Main Authors Keyes, Sam, Veelen, Arjen, McKay Fletcher, Dan, Scotson, Callum, Koebernick, Nico, Petroselli, Chiara, Williams, Katherine, Ruiz, Siul, Cooper, Laura, Mayon, Robbie, Duncan, Simon, Dumont, Marc, Jakobsen, Iver, Oldroyd, Giles, Tkacz, Andrzej, Poole, Philip, Mosselmans, Fred, Borca, Camelia, Huthwelker, Thomas, Jones, David L., Roose, Tiina
Format Journal Article
LanguageEnglish
Published England Wiley Subscription Services, Inc 01.04.2022
Wiley
John Wiley and Sons Inc
Subjects
Aluminium
Aluminum
Arbuscular mycorrhizas
ASTRONOMY AND ASTROPHYSICS
Colonization
Computed tomography
Fluorescence
Fungi
Growth rate
Hyphae
Inoculation
Microbiomes
Modelling
Mycorrhizae
mycorrhizas
Oxidation
Phosphorus
Plant growth
plant phosphorus uptake
Plant Roots - microbiology
rhizosphere modelling
Soil
Soil - chemistry
Soil Microbiology
Soil microorganisms
Soils
Sulfur
Sulphur
synchrotron
Synchrotrons
Tomography
Uptake
X‐ray computed tomography
X‐ray fluorescence
mycorrhizas
X-ray fluorescence
X-ray computed tomography
synchrotron
plant phosphorus uptake
rhizosphere modelling
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Abstract Summary 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.
AbstractList 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.
Summary 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.
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.
Author Dumont, Marc
Duncan, Simon
Jakobsen, Iver
Veelen, Arjen
Borca, Camelia
Scotson, Callum
Cooper, Laura
Mosselmans, Fred
Koebernick, Nico
McKay Fletcher, Dan
Mayon, Robbie
Petroselli, Chiara
Oldroyd, Giles
Roose, Tiina
Ruiz, Siul
Poole, Philip
Huthwelker, Thomas
Jones, David L.
Tkacz, Andrzej
Keyes, Sam
Williams, Katherine
AuthorAffiliation 1 Bioengineering Sciences Research Group Department of Mechanical Engineering School of Engineering Faculty of Engineering and Physical Sciences University of Southampton Southampton SO17 1BJ UK
2 Material Science and Technology Division Los Alamos National Laboratory Los Alamos NM 87545 USA
10 School of Natural Sciences Bangor University Bangor LL57 2DG UK
6 Crop Science Centre University of Cambridge 93 Lawrence Weaver Road Cambridge CB3 0LE UK
5 Department of Plant and Environmental Sciences University of Copenhagen Thorvaldsensvej 40 Frederiksberg DK‐1871 Denmark
9 Swiss Light Source PSI Forschungsstrasse 111 Villigen 5232 Switzerland
3 Stanford Synchrotron Radiation Lightsource SLAC National Accelerator Laboratory Menlo Park CA 94025 USA
4 School of Biological Sciences University of Southampton Southampton SO17 1BJ UK
8 Diamond Light Source Diamond House, Harwell Science & Innovation Campus Didcot OX11 0DE UK
7 Department of Plant Sciences University of Oxford South Parks Road Oxford OX1 3
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– name: 3 Stanford Synchrotron Radiation Lightsource SLAC National Accelerator Laboratory Menlo Park CA 94025 USA
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– name: 1 Bioengineering Sciences Research Group Department of Mechanical Engineering School of Engineering Faculty of Engineering and Physical Sciences University of Southampton Southampton SO17 1BJ UK
– name: 9 Swiss Light Source PSI Forschungsstrasse 111 Villigen 5232 Switzerland
– name: 4 School of Biological Sciences University of Southampton Southampton SO17 1BJ UK
– name: 11 5673 SoilsWest, Food Futures Institute Murdoch University 90 South Street Murdoch WA 6150 Australia
– name: 7 Department of Plant Sciences University of Oxford South Parks Road Oxford OX1 3RB UK
– name: 5 Department of Plant and Environmental Sciences University of Copenhagen Thorvaldsensvej 40 Frederiksberg DK‐1871 Denmark
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  surname: Keyes
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  organization: University of Southampton
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  organization: University of Southampton
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  surname: Scotson
  fullname: Scotson, Callum
  organization: University of Southampton
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  organization: University of Southampton
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  organization: University of Southampton
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  organization: University of Southampton
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  organization: University of Southampton
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  surname: Mayon
  fullname: Mayon, Robbie
  organization: University of Southampton
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  givenname: Simon
  surname: Duncan
  fullname: Duncan, Simon
  organization: University of Southampton
– sequence: 12
  givenname: Marc
  surname: Dumont
  fullname: Dumont, Marc
  organization: University of Southampton
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  organization: University of Copenhagen
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  organization: University of Cambridge
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  surname: Tkacz
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  organization: University of Oxford
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  organization: University of Oxford
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  surname: Mosselmans
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  orcidid: 0000-0001-8744-2060
  surname: Roose
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  email: t.roose@soton.ac.uk
  organization: University of Southampton
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Issue 2
Keywords mycorrhizas
X-ray fluorescence
X-ray computed tomography
synchrotron
plant phosphorus uptake
rhizosphere modelling
Language English
License Attribution
2022 The Authors New Phytologist © 2022 New Phytologist Foundation.
This is an open access article under the terms of the http://creativecommons.org/licenses/by/4.0/ License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.
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Notes These authors contributed equally to this work.
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Snippet Summary Phosphorus (P) is essential for plant growth. Arbuscular mycorrhizal fungi (AMF) aid its uptake by acquiring P from sources distant from roots in...
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...
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SubjectTerms Aluminium
Aluminum
Arbuscular mycorrhizas
ASTRONOMY AND ASTROPHYSICS
Colonization
Computed tomography
Fluorescence
Fungi
Growth rate
Hyphae
Inoculation
Microbiomes
Modelling
Mycorrhizae
mycorrhizas
Oxidation
Phosphorus
Plant growth
plant phosphorus uptake
Plant Roots - microbiology
rhizosphere modelling
Soil
Soil - chemistry
Soil Microbiology
Soil microorganisms
Soils
Sulfur
Sulphur
synchrotron
Synchrotrons
Tomography
Uptake
X‐ray computed tomography
X‐ray fluorescence
Title Multimodal correlative imaging and modelling of phosphorus uptake from soil by hyphae of mycorrhizal fungi
URI https://onlinelibrary.wiley.com/doi/abs/10.1111%2Fnph.17980
https://www.ncbi.nlm.nih.gov/pubmed/35043984
https://www.proquest.com/docview/2640226910/abstract/
https://search.proquest.com/docview/2621249231
https://www.osti.gov/servlets/purl/1856234
https://pubmed.ncbi.nlm.nih.gov/PMC9307049
Volume 234
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