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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Veröffentlicht in:The New phytologist 2022-04, Vol.234 (2), p.688-703
Hauptverfasser: 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
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container_end_page 703
container_issue 2
container_start_page 688
container_title The New phytologist
container_volume 234
creator 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
description 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.
doi_str_mv 10.1111/nph.17980
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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.</description><identifier>ISSN: 0028-646X</identifier><identifier>EISSN: 1469-8137</identifier><identifier>DOI: 10.1111/nph.17980</identifier><identifier>PMID: 35043984</identifier><language>eng</language><publisher>England: Wiley Subscription Services, Inc</publisher><subject>Aluminium ; Aluminum ; Arbuscular mycorrhizas ; ASTRONOMY AND ASTROPHYSICS ; 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</subject><ispartof>The New phytologist, 2022-04, Vol.234 (2), p.688-703</ispartof><rights>2022 The Authors © 2022 New Phytologist Foundation</rights><rights>2022 The Authors New Phytologist © 2022 New Phytologist Foundation.</rights><rights>2022. 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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.</description><subject>Aluminium</subject><subject>Aluminum</subject><subject>Arbuscular mycorrhizas</subject><subject>ASTRONOMY AND ASTROPHYSICS</subject><subject>Computed tomography</subject><subject>Fluorescence</subject><subject>Fungi</subject><subject>Growth rate</subject><subject>Hyphae</subject><subject>Inoculation</subject><subject>Microbiomes</subject><subject>Modelling</subject><subject>Mycorrhizae</subject><subject>mycorrhizas</subject><subject>Oxidation</subject><subject>Phosphorus</subject><subject>Plant growth</subject><subject>plant phosphorus uptake</subject><subject>Plant Roots - microbiology</subject><subject>rhizosphere modelling</subject><subject>Soil</subject><subject>Soil - chemistry</subject><subject>Soil Microbiology</subject><subject>Soil microorganisms</subject><subject>Soils</subject><subject>Sulfur</subject><subject>Sulphur</subject><subject>synchrotron</subject><subject>Synchrotrons</subject><subject>Tomography</subject><subject>Uptake</subject><subject>X‐ray computed tomography</subject><subject>X‐ray fluorescence</subject><issn>0028-646X</issn><issn>1469-8137</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2022</creationdate><recordtype>article</recordtype><sourceid>24P</sourceid><sourceid>WIN</sourceid><sourceid>EIF</sourceid><recordid>eNp1kU1rFTEUhoMo9lpd-Ack6KYups3X5E42gpRqhfqxUHAXMpnkTq6ZZJrMVMZfb65TiwoGQgjn4T3vOS8ATzE6xeWchbE_xVvRoHtggxkXVYPp9j7YIESaijP-9Qg8ynmPEBI1Jw_BEa0Ro6JhG7B_P_vJDbFTHuqYkvFqcjcGukHtXNhBFTpYqsb7wy9aOPYxl5vmDOdxUt8MtCkOMEfnYbvAfhl7ZQ7gsBz0evejKNs57Nxj8MAqn82T2_cYfHlz8fn8srr6-Pbd-eurSrMtQhUn2grRNlxRjoxpFLdMWVxzWhzT1lqhBKk7TjCt265tcINQ1yqqMUWCEE6PwatVd5zbwXTahCkpL8dUZkqLjMrJvyvB9XIXb6SgaIuYKALPV4GYJyezdpPRvY4hGD1J3JQVUlagk9suKV7PJk9ycFmXPalg4pwlKQYJE4Tigr74B93HOYWyg0IxVDwLjAr1cqV0ijknY-8cYyQPMcsSs_wVc2Gf_TniHfk71wKcrcB3583yfyX54dPlKvkTFMuy_w</recordid><startdate>202204</startdate><enddate>202204</enddate><creator>Keyes, Sam</creator><creator>Veelen, Arjen</creator><creator>McKay Fletcher, Dan</creator><creator>Scotson, Callum</creator><creator>Koebernick, Nico</creator><creator>Petroselli, Chiara</creator><creator>Williams, Katherine</creator><creator>Ruiz, Siul</creator><creator>Cooper, Laura</creator><creator>Mayon, Robbie</creator><creator>Duncan, Simon</creator><creator>Dumont, Marc</creator><creator>Jakobsen, Iver</creator><creator>Oldroyd, Giles</creator><creator>Tkacz, Andrzej</creator><creator>Poole, Philip</creator><creator>Mosselmans, Fred</creator><creator>Borca, Camelia</creator><creator>Huthwelker, Thomas</creator><creator>Jones, David L.</creator><creator>Roose, Tiina</creator><general>Wiley Subscription Services, Inc</general><general>Wiley</general><general>John Wiley and Sons Inc</general><scope>24P</scope><scope>WIN</scope><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7QO</scope><scope>7SN</scope><scope>8FD</scope><scope>C1K</scope><scope>F1W</scope><scope>FR3</scope><scope>H95</scope><scope>L.G</scope><scope>M7N</scope><scope>P64</scope><scope>RC3</scope><scope>7X8</scope><scope>OIOZB</scope><scope>OTOTI</scope><scope>5PM</scope><orcidid>https://orcid.org/0000-0001-8744-2060</orcidid><orcidid>https://orcid.org/0000-0001-6569-2931</orcidid><orcidid>https://orcid.org/0000000187442060</orcidid><orcidid>https://orcid.org/0000000165692931</orcidid></search><sort><creationdate>202204</creationdate><title>Multimodal correlative imaging and modelling of phosphorus uptake from soil by hyphae of mycorrhizal fungi</title><author>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</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c4700-62cf99b86a360ee8a6f4af15633983bff9a925d62135bdb81800dba3c13092263</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2022</creationdate><topic>Aluminium</topic><topic>Aluminum</topic><topic>Arbuscular mycorrhizas</topic><topic>ASTRONOMY AND ASTROPHYSICS</topic><topic>Computed tomography</topic><topic>Fluorescence</topic><topic>Fungi</topic><topic>Growth rate</topic><topic>Hyphae</topic><topic>Inoculation</topic><topic>Microbiomes</topic><topic>Modelling</topic><topic>Mycorrhizae</topic><topic>mycorrhizas</topic><topic>Oxidation</topic><topic>Phosphorus</topic><topic>Plant growth</topic><topic>plant phosphorus uptake</topic><topic>Plant Roots - microbiology</topic><topic>rhizosphere modelling</topic><topic>Soil</topic><topic>Soil - chemistry</topic><topic>Soil Microbiology</topic><topic>Soil microorganisms</topic><topic>Soils</topic><topic>Sulfur</topic><topic>Sulphur</topic><topic>synchrotron</topic><topic>Synchrotrons</topic><topic>Tomography</topic><topic>Uptake</topic><topic>X‐ray computed tomography</topic><topic>X‐ray fluorescence</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Keyes, Sam</creatorcontrib><creatorcontrib>Veelen, Arjen</creatorcontrib><creatorcontrib>McKay Fletcher, Dan</creatorcontrib><creatorcontrib>Scotson, Callum</creatorcontrib><creatorcontrib>Koebernick, Nico</creatorcontrib><creatorcontrib>Petroselli, Chiara</creatorcontrib><creatorcontrib>Williams, Katherine</creatorcontrib><creatorcontrib>Ruiz, Siul</creatorcontrib><creatorcontrib>Cooper, Laura</creatorcontrib><creatorcontrib>Mayon, Robbie</creatorcontrib><creatorcontrib>Duncan, Simon</creatorcontrib><creatorcontrib>Dumont, Marc</creatorcontrib><creatorcontrib>Jakobsen, Iver</creatorcontrib><creatorcontrib>Oldroyd, Giles</creatorcontrib><creatorcontrib>Tkacz, Andrzej</creatorcontrib><creatorcontrib>Poole, Philip</creatorcontrib><creatorcontrib>Mosselmans, Fred</creatorcontrib><creatorcontrib>Borca, Camelia</creatorcontrib><creatorcontrib>Huthwelker, Thomas</creatorcontrib><creatorcontrib>Jones, David L.</creatorcontrib><creatorcontrib>Roose, Tiina</creatorcontrib><creatorcontrib>Los Alamos National Laboratory (LANL), Los Alamos, NM (United States)</creatorcontrib><creatorcontrib>SLAC National Accelerator Laboratory (SLAC), Menlo Park, CA (United States)</creatorcontrib><collection>Wiley Online Library Open Access</collection><collection>Wiley Free Content</collection><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Biotechnology Research Abstracts</collection><collection>Ecology Abstracts</collection><collection>Technology Research Database</collection><collection>Environmental Sciences and Pollution Management</collection><collection>ASFA: Aquatic Sciences and Fisheries Abstracts</collection><collection>Engineering Research Database</collection><collection>Aquatic Science &amp; 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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.</abstract><cop>England</cop><pub>Wiley Subscription Services, Inc</pub><pmid>35043984</pmid><doi>10.1111/nph.17980</doi><tpages>703</tpages><orcidid>https://orcid.org/0000-0001-8744-2060</orcidid><orcidid>https://orcid.org/0000-0001-6569-2931</orcidid><orcidid>https://orcid.org/0000000187442060</orcidid><orcidid>https://orcid.org/0000000165692931</orcidid><oa>free_for_read</oa></addata></record>
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subjects Aluminium
Aluminum
Arbuscular mycorrhizas
ASTRONOMY AND ASTROPHYSICS
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
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