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 |
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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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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.</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. This article is published under http://creativecommons.org/licenses/by/4.0/ (the “License”). Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c4700-62cf99b86a360ee8a6f4af15633983bff9a925d62135bdb81800dba3c13092263</citedby><cites>FETCH-LOGICAL-c4700-62cf99b86a360ee8a6f4af15633983bff9a925d62135bdb81800dba3c13092263</cites><orcidid>0000-0001-8744-2060 ; 0000-0001-6569-2931 ; 0000000187442060 ; 0000000165692931</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://onlinelibrary.wiley.com/doi/pdf/10.1111%2Fnph.17980$$EPDF$$P50$$Gwiley$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://onlinelibrary.wiley.com/doi/full/10.1111%2Fnph.17980$$EHTML$$P50$$Gwiley$$Hfree_for_read</linktohtml><link.rule.ids>230,314,777,781,882,1412,1428,27905,27906,45555,45556,46390,46814</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/35043984$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink><backlink>$$Uhttps://www.osti.gov/servlets/purl/1856234$$D View this record in Osti.gov$$Hfree_for_read</backlink></links><search><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><title>Multimodal correlative imaging and modelling of phosphorus uptake from soil by hyphae of mycorrhizal fungi</title><title>The New phytologist</title><addtitle>New Phytol</addtitle><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.</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 & Fisheries Abstracts (ASFA) 1: Biological Sciences & Living Resources</collection><collection>Aquatic Science & Fisheries Abstracts (ASFA) Professional</collection><collection>Algology Mycology and Protozoology Abstracts (Microbiology C)</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Genetics Abstracts</collection><collection>MEDLINE - Academic</collection><collection>OSTI.GOV - Hybrid</collection><collection>OSTI.GOV</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>The New phytologist</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Keyes, Sam</au><au>Veelen, Arjen</au><au>McKay Fletcher, Dan</au><au>Scotson, Callum</au><au>Koebernick, Nico</au><au>Petroselli, Chiara</au><au>Williams, Katherine</au><au>Ruiz, Siul</au><au>Cooper, Laura</au><au>Mayon, Robbie</au><au>Duncan, Simon</au><au>Dumont, Marc</au><au>Jakobsen, Iver</au><au>Oldroyd, Giles</au><au>Tkacz, Andrzej</au><au>Poole, Philip</au><au>Mosselmans, Fred</au><au>Borca, Camelia</au><au>Huthwelker, Thomas</au><au>Jones, David L.</au><au>Roose, Tiina</au><aucorp>Los Alamos National Laboratory (LANL), Los Alamos, NM (United States)</aucorp><aucorp>SLAC National Accelerator Laboratory (SLAC), Menlo Park, CA (United States)</aucorp><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Multimodal correlative imaging and modelling of phosphorus uptake from soil by hyphae of mycorrhizal fungi</atitle><jtitle>The New phytologist</jtitle><addtitle>New Phytol</addtitle><date>2022-04</date><risdate>2022</risdate><volume>234</volume><issue>2</issue><spage>688</spage><epage>703</epage><pages>688-703</pages><issn>0028-646X</issn><eissn>1469-8137</eissn><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.</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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