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Proton-transfer-reaction mass spectrometry as a new tool for real time analysis of root-secreted volatile organic compounds in Arabidopsis

Plant roots release about 5% to 20% of all photosynthetically-fixed carbon, and as a result create a carbon-rich environment for numerous rhizosphere organisms, including plant pathogens and symbiotic microbes. Although some characterization of root exudates has been achieved, especially of secondar...

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Published in:Plant physiology (Bethesda) 2004-05, Vol.135 (1), p.47-58
Main Authors: Steeghs, M, Bais, H.P, De Gouw, J, Goldan, P, Kuster, W, Northway, M, Fall, R, Vivanco, J.M
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De Gouw, J
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Fall, R
Vivanco, J.M
description Plant roots release about 5% to 20% of all photosynthetically-fixed carbon, and as a result create a carbon-rich environment for numerous rhizosphere organisms, including plant pathogens and symbiotic microbes. Although some characterization of root exudates has been achieved, especially of secondary metabolites and proteins, much less is known about volatile organic compounds (VOCs) released by roots. In this communication, we describe a novel approach to exploring these rhizosphere VOCs and their induction by biotic stresses. The VOC formation of Arabidopsis roots was analyzed using proton-transfer-reaction mass spectrometry (PTR-MS), a new technology that allows rapid and real time analysis of most biogenic VOCs without preconcentration or chromatography. Our studies revealed that the major VOCs released and identified by both PTR-MS and gas chromatography-mass spectrometry were either simple metabolites, ethanol, acetaldehyde, acetic acid, ethyl acetate, 2-butanone, 2,3,-butanedione, and acetone, or the monoterpene, 1,8-cineole. Some VOCs were found to be produced constitutively regardless of the treatment; other VOCs were induced specifically as a result of different compatible and noncompatible interactions between microbes and insects and Arabidopsis roots. Compatible interactions of Pseudomonas syringae DC3000 and Diuraphis noxia with Arabidopsis roots resulted in the rapid release of 1,8-cineole, a monoterpene that has not been previously reported in Arabidopsis. Mechanical injuries to Arabidopsis roots did not produce 1,8-cineole nor any C6 wound-VOCs; compatible interactions between Arabidopsis roots and Diuraphis noxia did not produce any wound compounds. This suggests that Arabidopsis roots respond to wounding differently from above-ground plant organs. Trials with incompatible interactions did not reveal a set of compounds that was significantly different compared to the noninfected roots. The PTR-MS method may open the way for functional root VOC analysis that will complement genomic investigations in Arabidopsis.
doi_str_mv 10.1104/pp.104.038703
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Although some characterization of root exudates has been achieved, especially of secondary metabolites and proteins, much less is known about volatile organic compounds (VOCs) released by roots. In this communication, we describe a novel approach to exploring these rhizosphere VOCs and their induction by biotic stresses. The VOC formation of Arabidopsis roots was analyzed using proton-transfer-reaction mass spectrometry (PTR-MS), a new technology that allows rapid and real time analysis of most biogenic VOCs without preconcentration or chromatography. Our studies revealed that the major VOCs released and identified by both PTR-MS and gas chromatography-mass spectrometry were either simple metabolites, ethanol, acetaldehyde, acetic acid, ethyl acetate, 2-butanone, 2,3,-butanedione, and acetone, or the monoterpene, 1,8-cineole. 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Psychology ; Fungi - growth &amp; development ; gas chromatography ; Gas Chromatography-Mass Spectrometry ; Genes. Genome ; Immunity, Innate ; Infections ; insect pests ; Insecta - growth &amp; development ; Ions ; kinetics ; mass spectrometry ; Mass Spectrometry - instrumentation ; Mass Spectrometry - methods ; Mass spectroscopy ; mechanical damage ; Molecular and cellular biology ; Molecular genetics ; Monoterpenes - metabolism ; Net assimilation, photosynthesis, carbon metabolism. Photorespiration, respiration, fermentation (anoxia, hypoxia) ; Nutrition. Photosynthesis. Respiration. Metabolism ; Organic Chemicals - metabolism ; Pathogens ; plant damage ; Plant Diseases - microbiology ; Plant Diseases - parasitology ; Plant interaction ; plant pathogenic bacteria ; plant pathogenic fungi ; plant pests ; plant response ; Plant roots ; Plant Roots - metabolism ; Plant Roots - microbiology ; Plant Roots - parasitology ; Plants ; proton-transfer-reaction mass spectrometry ; Protons ; Pseudomonas syringae ; rhizosphere ; root exudates ; roots ; Stress, Mechanical ; Volatile organic compounds ; Volatilization</subject><ispartof>Plant physiology (Bethesda), 2004-05, Vol.135 (1), p.47-58</ispartof><rights>Copyright 2004 American Society of Plant Biologists</rights><rights>2004 INIST-CNRS</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c438t-e94d6be89b3260e5d0c2c9426d6f7bd7aa61680c5d62ac998920ee6f87ad40573</citedby><cites>FETCH-LOGICAL-c438t-e94d6be89b3260e5d0c2c9426d6f7bd7aa61680c5d62ac998920ee6f87ad40573</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.jstor.org/stable/pdf/4281724$$EPDF$$P50$$Gjstor$$H</linktopdf><linktohtml>$$Uhttps://www.jstor.org/stable/4281724$$EHTML$$P50$$Gjstor$$H</linktohtml><link.rule.ids>314,780,784,27924,27925,58238,58471</link.rule.ids><backlink>$$Uhttp://pascal-francis.inist.fr/vibad/index.php?action=getRecordDetail&amp;idt=15764900$$DView record in Pascal Francis$$Hfree_for_read</backlink><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/15141066$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Steeghs, M</creatorcontrib><creatorcontrib>Bais, H.P</creatorcontrib><creatorcontrib>De Gouw, J</creatorcontrib><creatorcontrib>Goldan, P</creatorcontrib><creatorcontrib>Kuster, W</creatorcontrib><creatorcontrib>Northway, M</creatorcontrib><creatorcontrib>Fall, R</creatorcontrib><creatorcontrib>Vivanco, J.M</creatorcontrib><title>Proton-transfer-reaction mass spectrometry as a new tool for real time analysis of root-secreted volatile organic compounds in Arabidopsis</title><title>Plant physiology (Bethesda)</title><addtitle>Plant Physiol</addtitle><description>Plant roots release about 5% to 20% of all photosynthetically-fixed carbon, and as a result create a carbon-rich environment for numerous rhizosphere organisms, including plant pathogens and symbiotic microbes. Although some characterization of root exudates has been achieved, especially of secondary metabolites and proteins, much less is known about volatile organic compounds (VOCs) released by roots. In this communication, we describe a novel approach to exploring these rhizosphere VOCs and their induction by biotic stresses. The VOC formation of Arabidopsis roots was analyzed using proton-transfer-reaction mass spectrometry (PTR-MS), a new technology that allows rapid and real time analysis of most biogenic VOCs without preconcentration or chromatography. Our studies revealed that the major VOCs released and identified by both PTR-MS and gas chromatography-mass spectrometry were either simple metabolites, ethanol, acetaldehyde, acetic acid, ethyl acetate, 2-butanone, 2,3,-butanedione, and acetone, or the monoterpene, 1,8-cineole. Some VOCs were found to be produced constitutively regardless of the treatment; other VOCs were induced specifically as a result of different compatible and noncompatible interactions between microbes and insects and Arabidopsis roots. Compatible interactions of Pseudomonas syringae DC3000 and Diuraphis noxia with Arabidopsis roots resulted in the rapid release of 1,8-cineole, a monoterpene that has not been previously reported in Arabidopsis. Mechanical injuries to Arabidopsis roots did not produce 1,8-cineole nor any C6 wound-VOCs; compatible interactions between Arabidopsis roots and Diuraphis noxia did not produce any wound compounds. This suggests that Arabidopsis roots respond to wounding differently from above-ground plant organs. Trials with incompatible interactions did not reveal a set of compounds that was significantly different compared to the noninfected roots. 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Psychology</subject><subject>Fungi - growth &amp; development</subject><subject>gas chromatography</subject><subject>Gas Chromatography-Mass Spectrometry</subject><subject>Genes. Genome</subject><subject>Immunity, Innate</subject><subject>Infections</subject><subject>insect pests</subject><subject>Insecta - growth &amp; development</subject><subject>Ions</subject><subject>kinetics</subject><subject>mass spectrometry</subject><subject>Mass Spectrometry - instrumentation</subject><subject>Mass Spectrometry - methods</subject><subject>Mass spectroscopy</subject><subject>mechanical damage</subject><subject>Molecular and cellular biology</subject><subject>Molecular genetics</subject><subject>Monoterpenes - metabolism</subject><subject>Net assimilation, photosynthesis, carbon metabolism. Photorespiration, respiration, fermentation (anoxia, hypoxia)</subject><subject>Nutrition. Photosynthesis. Respiration. Metabolism</subject><subject>Organic Chemicals - metabolism</subject><subject>Pathogens</subject><subject>plant damage</subject><subject>Plant Diseases - microbiology</subject><subject>Plant Diseases - parasitology</subject><subject>Plant interaction</subject><subject>plant pathogenic bacteria</subject><subject>plant pathogenic fungi</subject><subject>plant pests</subject><subject>plant response</subject><subject>Plant roots</subject><subject>Plant Roots - metabolism</subject><subject>Plant Roots - microbiology</subject><subject>Plant Roots - parasitology</subject><subject>Plants</subject><subject>proton-transfer-reaction mass spectrometry</subject><subject>Protons</subject><subject>Pseudomonas syringae</subject><subject>rhizosphere</subject><subject>root exudates</subject><subject>roots</subject><subject>Stress, Mechanical</subject><subject>Volatile organic compounds</subject><subject>Volatilization</subject><issn>0032-0889</issn><issn>1532-2548</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2004</creationdate><recordtype>article</recordtype><recordid>eNpNkc2O1DAQhC0EYoeBIzcEvsAtg-04jnNcrfiTVgIJ9hx17M7KqyQObs-ieQWeGq8yAk7VUn1dhyrGXkpxkFLo9-t6KHIQtW1F_YjtZFOrSjXaPmY7IcotrO0u2DOiOyGErKV-yi5kI7UUxuzY728p5rhUOcFCI6YqIbgc4sJnIOK0osspzpjTiQNx4Av-4jnGiY8x8QJPPIcZOSwwnSgQjyNPMeaK0CXM6Pl9nCCHCXlMt7AEx12c13hcPPGw8MsEQ_BxLa_P2ZMRJsIXZ92zm48fflx9rq6_fvpydXldOV3bXGGnvRnQdkOtjMDGC6dcp5XxZmwH3wIYaaxwjTcKXNfZTglEM9oWvBZNW-_Zuy13TfHnESn3cyCH0wQLxiP1reyUNNoWsNpAlyJRwrFfU5ghnXop-ofy-3XtH2Qrv_Cvz8HHYUb_jz63XYC3ZwDIwTSWzl2g_7jW6K6MtmevNu6Ockx_fa2sbJUu9pvNHiH2cJtKxM13VbYVoqsbIW39B7hXogI</recordid><startdate>20040501</startdate><enddate>20040501</enddate><creator>Steeghs, M</creator><creator>Bais, H.P</creator><creator>De Gouw, J</creator><creator>Goldan, P</creator><creator>Kuster, W</creator><creator>Northway, M</creator><creator>Fall, R</creator><creator>Vivanco, J.M</creator><general>American Society of Plant Biologists</general><general>American Society of Plant Physiologists</general><scope>FBQ</scope><scope>IQODW</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>7X8</scope></search><sort><creationdate>20040501</creationdate><title>Proton-transfer-reaction mass spectrometry as a new tool for real time analysis of root-secreted volatile organic compounds in Arabidopsis</title><author>Steeghs, M ; Bais, H.P ; De Gouw, J ; Goldan, P ; Kuster, W ; Northway, M ; Fall, R ; Vivanco, J.M</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c438t-e94d6be89b3260e5d0c2c9426d6f7bd7aa61680c5d62ac998920ee6f87ad40573</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2004</creationdate><topic>Agronomy. Soil science and plant productions</topic><topic>Alternaria brassicicola</topic><topic>Animals</topic><topic>Aphidoidea</topic><topic>Arabidopsis - metabolism</topic><topic>Arabidopsis - microbiology</topic><topic>Arabidopsis - parasitology</topic><topic>Arabidopsis thaliana</topic><topic>Average linear density</topic><topic>Bacteria - growth &amp; development</topic><topic>Biological and medical sciences</topic><topic>Breakthrough Technologies</topic><topic>Computer Systems</topic><topic>Cyclohexanols - metabolism</topic><topic>Diuraphis noxia</topic><topic>Economic plant physiology</topic><topic>emissions</topic><topic>Ethanol</topic><topic>Eucalyptol</topic><topic>Fundamental and applied biological sciences. Psychology</topic><topic>Fungi - growth &amp; development</topic><topic>gas chromatography</topic><topic>Gas Chromatography-Mass Spectrometry</topic><topic>Genes. Genome</topic><topic>Immunity, Innate</topic><topic>Infections</topic><topic>insect pests</topic><topic>Insecta - growth &amp; development</topic><topic>Ions</topic><topic>kinetics</topic><topic>mass spectrometry</topic><topic>Mass Spectrometry - instrumentation</topic><topic>Mass Spectrometry - methods</topic><topic>Mass spectroscopy</topic><topic>mechanical damage</topic><topic>Molecular and cellular biology</topic><topic>Molecular genetics</topic><topic>Monoterpenes - metabolism</topic><topic>Net assimilation, photosynthesis, carbon metabolism. Photorespiration, respiration, fermentation (anoxia, hypoxia)</topic><topic>Nutrition. Photosynthesis. Respiration. Metabolism</topic><topic>Organic Chemicals - metabolism</topic><topic>Pathogens</topic><topic>plant damage</topic><topic>Plant Diseases - microbiology</topic><topic>Plant Diseases - parasitology</topic><topic>Plant interaction</topic><topic>plant pathogenic bacteria</topic><topic>plant pathogenic fungi</topic><topic>plant pests</topic><topic>plant response</topic><topic>Plant roots</topic><topic>Plant Roots - metabolism</topic><topic>Plant Roots - microbiology</topic><topic>Plant Roots - parasitology</topic><topic>Plants</topic><topic>proton-transfer-reaction mass spectrometry</topic><topic>Protons</topic><topic>Pseudomonas syringae</topic><topic>rhizosphere</topic><topic>root exudates</topic><topic>roots</topic><topic>Stress, Mechanical</topic><topic>Volatile organic compounds</topic><topic>Volatilization</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Steeghs, M</creatorcontrib><creatorcontrib>Bais, H.P</creatorcontrib><creatorcontrib>De Gouw, J</creatorcontrib><creatorcontrib>Goldan, P</creatorcontrib><creatorcontrib>Kuster, W</creatorcontrib><creatorcontrib>Northway, M</creatorcontrib><creatorcontrib>Fall, R</creatorcontrib><creatorcontrib>Vivanco, J.M</creatorcontrib><collection>AGRIS</collection><collection>Pascal-Francis</collection><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>MEDLINE - Academic</collection><jtitle>Plant physiology (Bethesda)</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Steeghs, M</au><au>Bais, H.P</au><au>De Gouw, J</au><au>Goldan, P</au><au>Kuster, W</au><au>Northway, M</au><au>Fall, R</au><au>Vivanco, J.M</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Proton-transfer-reaction mass spectrometry as a new tool for real time analysis of root-secreted volatile organic compounds in Arabidopsis</atitle><jtitle>Plant physiology (Bethesda)</jtitle><addtitle>Plant Physiol</addtitle><date>2004-05-01</date><risdate>2004</risdate><volume>135</volume><issue>1</issue><spage>47</spage><epage>58</epage><pages>47-58</pages><issn>0032-0889</issn><eissn>1532-2548</eissn><coden>PPHYA5</coden><abstract>Plant roots release about 5% to 20% of all photosynthetically-fixed carbon, and as a result create a carbon-rich environment for numerous rhizosphere organisms, including plant pathogens and symbiotic microbes. Although some characterization of root exudates has been achieved, especially of secondary metabolites and proteins, much less is known about volatile organic compounds (VOCs) released by roots. In this communication, we describe a novel approach to exploring these rhizosphere VOCs and their induction by biotic stresses. The VOC formation of Arabidopsis roots was analyzed using proton-transfer-reaction mass spectrometry (PTR-MS), a new technology that allows rapid and real time analysis of most biogenic VOCs without preconcentration or chromatography. Our studies revealed that the major VOCs released and identified by both PTR-MS and gas chromatography-mass spectrometry were either simple metabolites, ethanol, acetaldehyde, acetic acid, ethyl acetate, 2-butanone, 2,3,-butanedione, and acetone, or the monoterpene, 1,8-cineole. Some VOCs were found to be produced constitutively regardless of the treatment; other VOCs were induced specifically as a result of different compatible and noncompatible interactions between microbes and insects and Arabidopsis roots. Compatible interactions of Pseudomonas syringae DC3000 and Diuraphis noxia with Arabidopsis roots resulted in the rapid release of 1,8-cineole, a monoterpene that has not been previously reported in Arabidopsis. Mechanical injuries to Arabidopsis roots did not produce 1,8-cineole nor any C6 wound-VOCs; compatible interactions between Arabidopsis roots and Diuraphis noxia did not produce any wound compounds. This suggests that Arabidopsis roots respond to wounding differently from above-ground plant organs. Trials with incompatible interactions did not reveal a set of compounds that was significantly different compared to the noninfected roots. 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subjects Agronomy. Soil science and plant productions
Alternaria brassicicola
Animals
Aphidoidea
Arabidopsis - metabolism
Arabidopsis - microbiology
Arabidopsis - parasitology
Arabidopsis thaliana
Average linear density
Bacteria - growth & development
Biological and medical sciences
Breakthrough Technologies
Computer Systems
Cyclohexanols - metabolism
Diuraphis noxia
Economic plant physiology
emissions
Ethanol
Eucalyptol
Fundamental and applied biological sciences. Psychology
Fungi - growth & development
gas chromatography
Gas Chromatography-Mass Spectrometry
Genes. Genome
Immunity, Innate
Infections
insect pests
Insecta - growth & development
Ions
kinetics
mass spectrometry
Mass Spectrometry - instrumentation
Mass Spectrometry - methods
Mass spectroscopy
mechanical damage
Molecular and cellular biology
Molecular genetics
Monoterpenes - metabolism
Net assimilation, photosynthesis, carbon metabolism. Photorespiration, respiration, fermentation (anoxia, hypoxia)
Nutrition. Photosynthesis. Respiration. Metabolism
Organic Chemicals - metabolism
Pathogens
plant damage
Plant Diseases - microbiology
Plant Diseases - parasitology
Plant interaction
plant pathogenic bacteria
plant pathogenic fungi
plant pests
plant response
Plant roots
Plant Roots - metabolism
Plant Roots - microbiology
Plant Roots - parasitology
Plants
proton-transfer-reaction mass spectrometry
Protons
Pseudomonas syringae
rhizosphere
root exudates
roots
Stress, Mechanical
Volatile organic compounds
Volatilization
title Proton-transfer-reaction mass spectrometry as a new tool for real time analysis of root-secreted volatile organic compounds in Arabidopsis
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