Microbiota responses to mutations affecting NO homeostasis in Arabidopsis thaliana
Summary Interactions between plants and microorganisms are pivotal for plant growth and productivity. Several plant molecular mechanisms that shape these microbial communities have been identified. However, the importance of nitric oxide (NO) produced by plants for the associated microbiota remains...
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Veröffentlicht in: | The New phytologist 2024-12, Vol.244 (5), p.2008-2023 |
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creator | Berger, Antoine Pérez‐Valera, Eduardo Blouin, Manuel Breuil, Marie‐Christine Butterbach‐Bahl, Klaus Dannenmann, Michael Besson‐Bard, Angélique Jeandroz, Sylvain Valls, Josep Spor, Aymé Subramaniam, Logapragasan Pétriacq, Pierre Wendehenne, David Philippot, Laurent |
description | Summary
Interactions between plants and microorganisms are pivotal for plant growth and productivity. Several plant molecular mechanisms that shape these microbial communities have been identified. However, the importance of nitric oxide (NO) produced by plants for the associated microbiota remains elusive.
Using Arabidopsis thaliana isogenic mutants overproducing NO (nox1, NO overexpression) or down‐producing NO (i.e. nia1nia2 impaired in the expression of both nitrate reductases NR1/NIA1 and NR2/NIA2; the 35s::GSNOR1 line overexpressing nitrosoglutathione reductase (GSNOR) and 35s::AHB1 line overexpressing haemoglobin 1 (AHB1)), we investigated how altered NO homeostasis affects microbial communities in the rhizosphere and in the roots, soil microbial activity and soil metabolites.
We show that the rhizosphere microbiome was affected by the mutant genotypes, with the nox1 and nia1nia2 mutants causing opposite shifts in bacterial and fungal communities compared with the wild‐type (WT) Col‐0 in the rhizosphere and roots, respectively. These mutants also exhibited distinctive soil metabolite profiles than those from the other genotypes while soil microbial activity did not differ between the mutants and the WT Col‐0.
Our findings support our hypothesis that changes in NO production by plants can influence the plant microbiome composition with differential effects between fungal and bacterial communities. |
doi_str_mv | 10.1111/nph.20159 |
format | Article |
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Interactions between plants and microorganisms are pivotal for plant growth and productivity. Several plant molecular mechanisms that shape these microbial communities have been identified. However, the importance of nitric oxide (NO) produced by plants for the associated microbiota remains elusive.
Using Arabidopsis thaliana isogenic mutants overproducing NO (nox1, NO overexpression) or down‐producing NO (i.e. nia1nia2 impaired in the expression of both nitrate reductases NR1/NIA1 and NR2/NIA2; the 35s::GSNOR1 line overexpressing nitrosoglutathione reductase (GSNOR) and 35s::AHB1 line overexpressing haemoglobin 1 (AHB1)), we investigated how altered NO homeostasis affects microbial communities in the rhizosphere and in the roots, soil microbial activity and soil metabolites.
We show that the rhizosphere microbiome was affected by the mutant genotypes, with the nox1 and nia1nia2 mutants causing opposite shifts in bacterial and fungal communities compared with the wild‐type (WT) Col‐0 in the rhizosphere and roots, respectively. These mutants also exhibited distinctive soil metabolite profiles than those from the other genotypes while soil microbial activity did not differ between the mutants and the WT Col‐0.
Our findings support our hypothesis that changes in NO production by plants can influence the plant microbiome composition with differential effects between fungal and bacterial communities.</description><identifier>ISSN: 0028-646X</identifier><identifier>ISSN: 1469-8137</identifier><identifier>EISSN: 1469-8137</identifier><identifier>DOI: 10.1111/nph.20159</identifier><identifier>PMID: 39329426</identifier><language>eng</language><publisher>England: Wiley Subscription Services, Inc</publisher><subject>Agricultural sciences ; Arabidopsis - genetics ; Arabidopsis - microbiology ; Arabidopsis Proteins - genetics ; Arabidopsis Proteins - metabolism ; Arabidopsis thaliana ; Bacteria - genetics ; Bacteria - metabolism ; Biological activity ; Composition effects ; endosphere ; Fungi ; Genotypes ; Glutamate receptors ; Haemoglobin ; Hemoglobin ; Homeostasis ; Life Sciences ; Metabolites ; Microbial activity ; Microbial flora ; microbiome ; Microbiomes ; Microbiota ; Microbiota - genetics ; Microorganisms ; Molecular modelling ; Mutants ; Mutation - genetics ; Nitrate Reductase - genetics ; Nitrate Reductase - metabolism ; Nitric oxide ; Nitric Oxide - metabolism ; Plant growth ; Plant layout ; Plant Roots - genetics ; Plant Roots - microbiology ; Plants ; Reductases ; Rhizosphere ; Roots ; Soil ; Soil investigations ; Soil Microbiology ; Soil microorganisms ; Soil profiles ; Soil study ; Vegetal Biology</subject><ispartof>The New phytologist, 2024-12, Vol.244 (5), p.2008-2023</ispartof><rights>2024 The Author(s). © 2024 New Phytologist Foundation.</rights><rights>2024 The Author(s). New Phytologist © 2024 New Phytologist Foundation.</rights><rights>Copyright © 2024 New Phytologist Trust</rights><rights>Distributed under a Creative Commons Attribution 4.0 International License</rights><lds50>peer_reviewed</lds50><woscitedreferencessubscribed>false</woscitedreferencessubscribed><cites>FETCH-LOGICAL-c2779-a0949bf95e7f6ef131827c412546bedddc2e0d244c352113e85cc8f7d64edf033</cites><orcidid>0000-0003-4832-738X ; 0000-0002-0364-6654 ; 0000-0002-1088-102X ; 0000-0003-2671-3992 ; 0000-0003-0119-7696 ; 0000-0001-9499-6598 ; 0000-0001-8151-7420 ; 0000-0002-3928-9070 ; 0000-0001-6924-3586 ; 0000-0003-3461-4492 ; 0000-0002-1359-4114 ; 0000-0002-4707-9559</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.20159$$EPDF$$P50$$Gwiley$$H</linktopdf><linktohtml>$$Uhttps://onlinelibrary.wiley.com/doi/full/10.1111%2Fnph.20159$$EHTML$$P50$$Gwiley$$H</linktohtml><link.rule.ids>230,314,780,784,885,1417,27924,27925,45574,45575</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/39329426$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink><backlink>$$Uhttps://hal.science/hal-04712868$$DView record in HAL$$Hfree_for_read</backlink></links><search><creatorcontrib>Berger, Antoine</creatorcontrib><creatorcontrib>Pérez‐Valera, Eduardo</creatorcontrib><creatorcontrib>Blouin, Manuel</creatorcontrib><creatorcontrib>Breuil, Marie‐Christine</creatorcontrib><creatorcontrib>Butterbach‐Bahl, Klaus</creatorcontrib><creatorcontrib>Dannenmann, Michael</creatorcontrib><creatorcontrib>Besson‐Bard, Angélique</creatorcontrib><creatorcontrib>Jeandroz, Sylvain</creatorcontrib><creatorcontrib>Valls, Josep</creatorcontrib><creatorcontrib>Spor, Aymé</creatorcontrib><creatorcontrib>Subramaniam, Logapragasan</creatorcontrib><creatorcontrib>Pétriacq, Pierre</creatorcontrib><creatorcontrib>Wendehenne, David</creatorcontrib><creatorcontrib>Philippot, Laurent</creatorcontrib><title>Microbiota responses to mutations affecting NO homeostasis in Arabidopsis thaliana</title><title>The New phytologist</title><addtitle>New Phytol</addtitle><description>Summary
Interactions between plants and microorganisms are pivotal for plant growth and productivity. Several plant molecular mechanisms that shape these microbial communities have been identified. However, the importance of nitric oxide (NO) produced by plants for the associated microbiota remains elusive.
Using Arabidopsis thaliana isogenic mutants overproducing NO (nox1, NO overexpression) or down‐producing NO (i.e. nia1nia2 impaired in the expression of both nitrate reductases NR1/NIA1 and NR2/NIA2; the 35s::GSNOR1 line overexpressing nitrosoglutathione reductase (GSNOR) and 35s::AHB1 line overexpressing haemoglobin 1 (AHB1)), we investigated how altered NO homeostasis affects microbial communities in the rhizosphere and in the roots, soil microbial activity and soil metabolites.
We show that the rhizosphere microbiome was affected by the mutant genotypes, with the nox1 and nia1nia2 mutants causing opposite shifts in bacterial and fungal communities compared with the wild‐type (WT) Col‐0 in the rhizosphere and roots, respectively. These mutants also exhibited distinctive soil metabolite profiles than those from the other genotypes while soil microbial activity did not differ between the mutants and the WT Col‐0.
Our findings support our hypothesis that changes in NO production by plants can influence the plant microbiome composition with differential effects between fungal and bacterial communities.</description><subject>Agricultural sciences</subject><subject>Arabidopsis - genetics</subject><subject>Arabidopsis - microbiology</subject><subject>Arabidopsis Proteins - genetics</subject><subject>Arabidopsis Proteins - metabolism</subject><subject>Arabidopsis thaliana</subject><subject>Bacteria - genetics</subject><subject>Bacteria - metabolism</subject><subject>Biological activity</subject><subject>Composition effects</subject><subject>endosphere</subject><subject>Fungi</subject><subject>Genotypes</subject><subject>Glutamate receptors</subject><subject>Haemoglobin</subject><subject>Hemoglobin</subject><subject>Homeostasis</subject><subject>Life Sciences</subject><subject>Metabolites</subject><subject>Microbial activity</subject><subject>Microbial flora</subject><subject>microbiome</subject><subject>Microbiomes</subject><subject>Microbiota</subject><subject>Microbiota - genetics</subject><subject>Microorganisms</subject><subject>Molecular modelling</subject><subject>Mutants</subject><subject>Mutation - genetics</subject><subject>Nitrate Reductase - genetics</subject><subject>Nitrate Reductase - metabolism</subject><subject>Nitric oxide</subject><subject>Nitric Oxide - metabolism</subject><subject>Plant growth</subject><subject>Plant layout</subject><subject>Plant Roots - genetics</subject><subject>Plant Roots - microbiology</subject><subject>Plants</subject><subject>Reductases</subject><subject>Rhizosphere</subject><subject>Roots</subject><subject>Soil</subject><subject>Soil investigations</subject><subject>Soil Microbiology</subject><subject>Soil microorganisms</subject><subject>Soil profiles</subject><subject>Soil study</subject><subject>Vegetal Biology</subject><issn>0028-646X</issn><issn>1469-8137</issn><issn>1469-8137</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2024</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNp1kU1r3DAQhkVoSbZJDvkDxdBLe3Cib0vHJTTZwuaD0EJuQpZHWQXbci27Jf--2m6aQCG6iBkenpHmReiE4FOSz1k_bE4pJkLvoQXhUpeKsOodWmBMVSm5vD9AH1J6xBhrIek-OmCaUc2pXKC7q-DGWIc42WKENMQ-QSqmWHTzZKeQy8J6D24K_UNxfVNsYgcxTTaFVIS-WI62Dk0ctuW0sW2wvT1C771tExw_34fox8XX7-ercn1z-e18uS4drSpdWqy5rr0WUHkJnjCiaOU4oYLLGpqmcRRwQzl3TFBCGCjhnPJVIzk0HjN2iL7svHmuGcbQ2fHJRBvMark22x7mFaFKql8ks5937DDGnzOkyXQhOWhb20Ock2GEYI4FUVvtp__QxziPff5JpihXWishXofn7aU0gn95AcFmG4rJoZi_oWT247NxrjtoXsh_KWTgbAf8Di08vW0y17ernfIPvYiVCA</recordid><startdate>202412</startdate><enddate>202412</enddate><creator>Berger, Antoine</creator><creator>Pérez‐Valera, Eduardo</creator><creator>Blouin, Manuel</creator><creator>Breuil, Marie‐Christine</creator><creator>Butterbach‐Bahl, Klaus</creator><creator>Dannenmann, Michael</creator><creator>Besson‐Bard, Angélique</creator><creator>Jeandroz, Sylvain</creator><creator>Valls, Josep</creator><creator>Spor, Aymé</creator><creator>Subramaniam, Logapragasan</creator><creator>Pétriacq, Pierre</creator><creator>Wendehenne, David</creator><creator>Philippot, Laurent</creator><general>Wiley Subscription Services, Inc</general><general>Wiley</general><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>1XC</scope><orcidid>https://orcid.org/0000-0003-4832-738X</orcidid><orcidid>https://orcid.org/0000-0002-0364-6654</orcidid><orcidid>https://orcid.org/0000-0002-1088-102X</orcidid><orcidid>https://orcid.org/0000-0003-2671-3992</orcidid><orcidid>https://orcid.org/0000-0003-0119-7696</orcidid><orcidid>https://orcid.org/0000-0001-9499-6598</orcidid><orcidid>https://orcid.org/0000-0001-8151-7420</orcidid><orcidid>https://orcid.org/0000-0002-3928-9070</orcidid><orcidid>https://orcid.org/0000-0001-6924-3586</orcidid><orcidid>https://orcid.org/0000-0003-3461-4492</orcidid><orcidid>https://orcid.org/0000-0002-1359-4114</orcidid><orcidid>https://orcid.org/0000-0002-4707-9559</orcidid></search><sort><creationdate>202412</creationdate><title>Microbiota responses to mutations affecting NO homeostasis in Arabidopsis thaliana</title><author>Berger, Antoine ; 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Interactions between plants and microorganisms are pivotal for plant growth and productivity. Several plant molecular mechanisms that shape these microbial communities have been identified. However, the importance of nitric oxide (NO) produced by plants for the associated microbiota remains elusive.
Using Arabidopsis thaliana isogenic mutants overproducing NO (nox1, NO overexpression) or down‐producing NO (i.e. nia1nia2 impaired in the expression of both nitrate reductases NR1/NIA1 and NR2/NIA2; the 35s::GSNOR1 line overexpressing nitrosoglutathione reductase (GSNOR) and 35s::AHB1 line overexpressing haemoglobin 1 (AHB1)), we investigated how altered NO homeostasis affects microbial communities in the rhizosphere and in the roots, soil microbial activity and soil metabolites.
We show that the rhizosphere microbiome was affected by the mutant genotypes, with the nox1 and nia1nia2 mutants causing opposite shifts in bacterial and fungal communities compared with the wild‐type (WT) Col‐0 in the rhizosphere and roots, respectively. These mutants also exhibited distinctive soil metabolite profiles than those from the other genotypes while soil microbial activity did not differ between the mutants and the WT Col‐0.
Our findings support our hypothesis that changes in NO production by plants can influence the plant microbiome composition with differential effects between fungal and bacterial communities.</abstract><cop>England</cop><pub>Wiley Subscription Services, Inc</pub><pmid>39329426</pmid><doi>10.1111/nph.20159</doi><tpages>16</tpages><orcidid>https://orcid.org/0000-0003-4832-738X</orcidid><orcidid>https://orcid.org/0000-0002-0364-6654</orcidid><orcidid>https://orcid.org/0000-0002-1088-102X</orcidid><orcidid>https://orcid.org/0000-0003-2671-3992</orcidid><orcidid>https://orcid.org/0000-0003-0119-7696</orcidid><orcidid>https://orcid.org/0000-0001-9499-6598</orcidid><orcidid>https://orcid.org/0000-0001-8151-7420</orcidid><orcidid>https://orcid.org/0000-0002-3928-9070</orcidid><orcidid>https://orcid.org/0000-0001-6924-3586</orcidid><orcidid>https://orcid.org/0000-0003-3461-4492</orcidid><orcidid>https://orcid.org/0000-0002-1359-4114</orcidid><orcidid>https://orcid.org/0000-0002-4707-9559</orcidid></addata></record> |
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subjects | Agricultural sciences Arabidopsis - genetics Arabidopsis - microbiology Arabidopsis Proteins - genetics Arabidopsis Proteins - metabolism Arabidopsis thaliana Bacteria - genetics Bacteria - metabolism Biological activity Composition effects endosphere Fungi Genotypes Glutamate receptors Haemoglobin Hemoglobin Homeostasis Life Sciences Metabolites Microbial activity Microbial flora microbiome Microbiomes Microbiota Microbiota - genetics Microorganisms Molecular modelling Mutants Mutation - genetics Nitrate Reductase - genetics Nitrate Reductase - metabolism Nitric oxide Nitric Oxide - metabolism Plant growth Plant layout Plant Roots - genetics Plant Roots - microbiology Plants Reductases Rhizosphere Roots Soil Soil investigations Soil Microbiology Soil microorganisms Soil profiles Soil study Vegetal Biology |
title | Microbiota responses to mutations affecting NO homeostasis in Arabidopsis thaliana |
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