Benzoxazinoids in root exudates of maize attract Pseudomonas putida to the rhizosphere
Benzoxazinoids, such as 2,4-dihydroxy-7-methoxy-2H-1,4-benzoxazin-3(4H)-one (DIMBOA), are secondary metabolites in grasses. In addition to their function in plant defence against pests and diseases above-ground, benzoxazinoids (BXs) have also been implicated in defence below-ground, where they can e...
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| creator | Neal, Andrew L Ahmad, Shakoor Gordon-Weeks, Ruth Ton, Jurriaan |
| description | Benzoxazinoids, such as 2,4-dihydroxy-7-methoxy-2H-1,4-benzoxazin-3(4H)-one (DIMBOA), are secondary metabolites in grasses. In addition to their function in plant defence against pests and diseases above-ground, benzoxazinoids (BXs) have also been implicated in defence below-ground, where they can exert allelochemical or antimicrobial activities. We have studied the impact of BXs on the interaction between maize and Pseudomonas putida KT2440, a competitive coloniser of the maize rhizosphere with plant-beneficial traits. Chromatographic analyses revealed that DIMBOA is the main BX compound in root exudates of maize. In vitro analysis of DIMBOA stability indicated that KT2440 tolerance of DIMBOA is based on metabolism-dependent breakdown of this BX compound. Transcriptome analysis of DIMBOA-exposed P. putida identified increased transcription of genes controlling benzoate catabolism and chemotaxis. Chemotaxis assays confirmed motility of P. putida towards DIMBOA. Moreover, colonisation essays in soil with Green Fluorescent Protein (GFP)-expressing P. putida showed that DIMBOA-producing roots of wild-type maize attract significantly higher numbers of P. putida cells than roots of the DIMBOA-deficient bx1 mutant. Our results demonstrate a central role for DIMBOA as a below-ground semiochemical for recruitment of plant-beneficial rhizobacteria during the relatively young and vulnerable growth stages of maize. |
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In addition to their function in plant defence against pests and diseases above-ground, benzoxazinoids (BXs) have also been implicated in defence below-ground, where they can exert allelochemical or antimicrobial activities. We have studied the impact of BXs on the interaction between maize and Pseudomonas putida KT2440, a competitive coloniser of the maize rhizosphere with plant-beneficial traits. Chromatographic analyses revealed that DIMBOA is the main BX compound in root exudates of maize. In vitro analysis of DIMBOA stability indicated that KT2440 tolerance of DIMBOA is based on metabolism-dependent breakdown of this BX compound. Transcriptome analysis of DIMBOA-exposed P. putida identified increased transcription of genes controlling benzoate catabolism and chemotaxis. Chemotaxis assays confirmed motility of P. putida towards DIMBOA. Moreover, colonisation essays in soil with Green Fluorescent Protein (GFP)-expressing P. putida showed that DIMBOA-producing roots of wild-type maize attract significantly higher numbers of P. putida cells than roots of the DIMBOA-deficient bx1 mutant. Our results demonstrate a central role for DIMBOA as a below-ground semiochemical for recruitment of plant-beneficial rhizobacteria during the relatively young and vulnerable growth stages of maize.</description><identifier>ISSN: 1932-6203</identifier><identifier>EISSN: 1932-6203</identifier><identifier>DOI: 10.1371/journal.pone.0035498</identifier><identifier>PMID: 22545111</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>Acids ; Agriculture ; Bacteria ; Benzoxazines - chemistry ; Benzoxazines - isolation & purification ; Benzoxazines - metabolism ; Biodegradation ; Biology ; Catabolism ; Chemistry ; Chemotaxis ; Colonization ; Corn ; Defense industry ; Enzymes ; Exudates ; Exudation ; Flowers & plants ; Fluorescence ; Fungi ; Gene expression ; Genomes ; Grasslands ; Green fluorescent protein ; Hypotheses ; Metabolism ; Metabolites ; Pests ; Phosphatase ; Physiological aspects ; Plant diseases ; Plant metabolites ; Plant Roots - chemistry ; Plant Roots - metabolism ; Pseudomonas fluorescens ; Pseudomonas putida ; Pseudomonas putida - genetics ; Pseudomonas putida - physiology ; Rhizosphere ; Roots ; Secondary metabolites ; Stability analysis ; Transcription ; Transcription (Genetics) ; Transcriptome ; Zea mays - chemistry ; Zea mays - metabolism ; Zea mays - microbiology</subject><ispartof>PloS one, 2012-04, Vol.7 (4), p.e35498-e35498</ispartof><rights>COPYRIGHT 2012 Public Library of Science</rights><rights>2012 Neal et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License: https://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. 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In addition to their function in plant defence against pests and diseases above-ground, benzoxazinoids (BXs) have also been implicated in defence below-ground, where they can exert allelochemical or antimicrobial activities. We have studied the impact of BXs on the interaction between maize and Pseudomonas putida KT2440, a competitive coloniser of the maize rhizosphere with plant-beneficial traits. Chromatographic analyses revealed that DIMBOA is the main BX compound in root exudates of maize. In vitro analysis of DIMBOA stability indicated that KT2440 tolerance of DIMBOA is based on metabolism-dependent breakdown of this BX compound. Transcriptome analysis of DIMBOA-exposed P. putida identified increased transcription of genes controlling benzoate catabolism and chemotaxis. Chemotaxis assays confirmed motility of P. putida towards DIMBOA. Moreover, colonisation essays in soil with Green Fluorescent Protein (GFP)-expressing P. putida showed that DIMBOA-producing roots of wild-type maize attract significantly higher numbers of P. putida cells than roots of the DIMBOA-deficient bx1 mutant. Our results demonstrate a central role for DIMBOA as a below-ground semiochemical for recruitment of plant-beneficial rhizobacteria during the relatively young and vulnerable growth stages of maize.</description><subject>Acids</subject><subject>Agriculture</subject><subject>Bacteria</subject><subject>Benzoxazines - chemistry</subject><subject>Benzoxazines - isolation & purification</subject><subject>Benzoxazines - metabolism</subject><subject>Biodegradation</subject><subject>Biology</subject><subject>Catabolism</subject><subject>Chemistry</subject><subject>Chemotaxis</subject><subject>Colonization</subject><subject>Corn</subject><subject>Defense industry</subject><subject>Enzymes</subject><subject>Exudates</subject><subject>Exudation</subject><subject>Flowers & plants</subject><subject>Fluorescence</subject><subject>Fungi</subject><subject>Gene expression</subject><subject>Genomes</subject><subject>Grasslands</subject><subject>Green fluorescent protein</subject><subject>Hypotheses</subject><subject>Metabolism</subject><subject>Metabolites</subject><subject>Pests</subject><subject>Phosphatase</subject><subject>Physiological aspects</subject><subject>Plant diseases</subject><subject>Plant metabolites</subject><subject>Plant Roots - 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Academic</collection><collection>PubMed Central (Full Participant titles)</collection><collection>DOAJ Directory of Open Access Journals</collection><jtitle>PloS one</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Neal, Andrew L</au><au>Ahmad, Shakoor</au><au>Gordon-Weeks, Ruth</au><au>Ton, Jurriaan</au><au>Yang, Ching-Hong</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Benzoxazinoids in root exudates of maize attract Pseudomonas putida to the rhizosphere</atitle><jtitle>PloS one</jtitle><addtitle>PLoS One</addtitle><date>2012-04-24</date><risdate>2012</risdate><volume>7</volume><issue>4</issue><spage>e35498</spage><epage>e35498</epage><pages>e35498-e35498</pages><issn>1932-6203</issn><eissn>1932-6203</eissn><abstract>Benzoxazinoids, such as 2,4-dihydroxy-7-methoxy-2H-1,4-benzoxazin-3(4H)-one (DIMBOA), are secondary metabolites in grasses. In addition to their function in plant defence against pests and diseases above-ground, benzoxazinoids (BXs) have also been implicated in defence below-ground, where they can exert allelochemical or antimicrobial activities. We have studied the impact of BXs on the interaction between maize and Pseudomonas putida KT2440, a competitive coloniser of the maize rhizosphere with plant-beneficial traits. Chromatographic analyses revealed that DIMBOA is the main BX compound in root exudates of maize. In vitro analysis of DIMBOA stability indicated that KT2440 tolerance of DIMBOA is based on metabolism-dependent breakdown of this BX compound. Transcriptome analysis of DIMBOA-exposed P. putida identified increased transcription of genes controlling benzoate catabolism and chemotaxis. Chemotaxis assays confirmed motility of P. putida towards DIMBOA. Moreover, colonisation essays in soil with Green Fluorescent Protein (GFP)-expressing P. putida showed that DIMBOA-producing roots of wild-type maize attract significantly higher numbers of P. putida cells than roots of the DIMBOA-deficient bx1 mutant. Our results demonstrate a central role for DIMBOA as a below-ground semiochemical for recruitment of plant-beneficial rhizobacteria during the relatively young and vulnerable growth stages of maize.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>22545111</pmid><doi>10.1371/journal.pone.0035498</doi><tpages>e35498</tpages><oa>free_for_read</oa></addata></record> |
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| subjects | Acids Agriculture Bacteria Benzoxazines - chemistry Benzoxazines - isolation & purification Benzoxazines - metabolism Biodegradation Biology Catabolism Chemistry Chemotaxis Colonization Corn Defense industry Enzymes Exudates Exudation Flowers & plants Fluorescence Fungi Gene expression Genomes Grasslands Green fluorescent protein Hypotheses Metabolism Metabolites Pests Phosphatase Physiological aspects Plant diseases Plant metabolites Plant Roots - chemistry Plant Roots - metabolism Pseudomonas fluorescens Pseudomonas putida Pseudomonas putida - genetics Pseudomonas putida - physiology Rhizosphere Roots Secondary metabolites Stability analysis Transcription Transcription (Genetics) Transcriptome Zea mays - chemistry Zea mays - metabolism Zea mays - microbiology |
| title | Benzoxazinoids in root exudates of maize attract Pseudomonas putida to the rhizosphere |
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