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The biocontrol agent Pseudomonas chlororaphis PA23 primes Brassica napus defenses through distinct gene networks

BACKGROUND: The biological control agent Pseudomonas chlororaphis PA23 is capable of protecting Brassica napus (canola) from the necrotrophic fungus Sclerotinia sclerotiorum via direct antagonism. While we have elucidated bacterial genes and gene products responsible biocontrol, little is known abou...

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Autores principales: Duke, Kelly A., Becker, Michael G., Girard, Ian J., Millar, Jenna L., Dilantha Fernando, W. G., Belmonte, Mark F., de Kievit, Teresa R.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2017
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5477169/
https://www.ncbi.nlm.nih.gov/pubmed/28629321
http://dx.doi.org/10.1186/s12864-017-3848-6
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author Duke, Kelly A.
Becker, Michael G.
Girard, Ian J.
Millar, Jenna L.
Dilantha Fernando, W. G.
Belmonte, Mark F.
de Kievit, Teresa R.
author_facet Duke, Kelly A.
Becker, Michael G.
Girard, Ian J.
Millar, Jenna L.
Dilantha Fernando, W. G.
Belmonte, Mark F.
de Kievit, Teresa R.
author_sort Duke, Kelly A.
collection PubMed
description BACKGROUND: The biological control agent Pseudomonas chlororaphis PA23 is capable of protecting Brassica napus (canola) from the necrotrophic fungus Sclerotinia sclerotiorum via direct antagonism. While we have elucidated bacterial genes and gene products responsible biocontrol, little is known about how the host plant responds to bacterial priming on the leaf surface, including global changes in gene activity in the presence and absence of S. sclerotiorum. RESULTS: Application of PA23 to the aerial surfaces of canola plants reduced the number of S. sclerotiorum lesion-forming petals by 91.1%. RNA sequencing of the host pathogen interface showed that pretreatment with PA23 reduced the number of genes upregulated in response to S. sclerotiorum by 16-fold. By itself, PA23 activated unique defense networks indicative of defense priming. Genes encoding MAMP-triggered immunity receptors detecting flagellin and peptidoglycan were downregulated in PA23 only-treated plants, consistent with post-stimulus desensitization. Downstream, we observed reactive oxygen species (ROS) production involving low levels of H(2)O(2) and overexpression of genes associated with glycerol-3-phosphate (G3P)-mediated systemic acquired resistance (SAR). Leaf chloroplasts exhibited increased thylakoid membrane structures and chlorophyll content, while lipid metabolic processes were upregulated. CONCLUSION: In addition to directly antagonizing S. sclerotiorum, PA23 primes the plant defense response through induction of unique local and systemic defense networks. This study provides novel insight into the effects of biocontrol agents applied to the plant phyllosphere. Understanding these interactions will aid in the development of biocontrol systems as an alternative to chemical pesticides for protection of important crop systems. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s12864-017-3848-6) contains supplementary material, which is available to authorized users.
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spelling pubmed-54771692017-06-23 The biocontrol agent Pseudomonas chlororaphis PA23 primes Brassica napus defenses through distinct gene networks Duke, Kelly A. Becker, Michael G. Girard, Ian J. Millar, Jenna L. Dilantha Fernando, W. G. Belmonte, Mark F. de Kievit, Teresa R. BMC Genomics Research Article BACKGROUND: The biological control agent Pseudomonas chlororaphis PA23 is capable of protecting Brassica napus (canola) from the necrotrophic fungus Sclerotinia sclerotiorum via direct antagonism. While we have elucidated bacterial genes and gene products responsible biocontrol, little is known about how the host plant responds to bacterial priming on the leaf surface, including global changes in gene activity in the presence and absence of S. sclerotiorum. RESULTS: Application of PA23 to the aerial surfaces of canola plants reduced the number of S. sclerotiorum lesion-forming petals by 91.1%. RNA sequencing of the host pathogen interface showed that pretreatment with PA23 reduced the number of genes upregulated in response to S. sclerotiorum by 16-fold. By itself, PA23 activated unique defense networks indicative of defense priming. Genes encoding MAMP-triggered immunity receptors detecting flagellin and peptidoglycan were downregulated in PA23 only-treated plants, consistent with post-stimulus desensitization. Downstream, we observed reactive oxygen species (ROS) production involving low levels of H(2)O(2) and overexpression of genes associated with glycerol-3-phosphate (G3P)-mediated systemic acquired resistance (SAR). Leaf chloroplasts exhibited increased thylakoid membrane structures and chlorophyll content, while lipid metabolic processes were upregulated. CONCLUSION: In addition to directly antagonizing S. sclerotiorum, PA23 primes the plant defense response through induction of unique local and systemic defense networks. This study provides novel insight into the effects of biocontrol agents applied to the plant phyllosphere. Understanding these interactions will aid in the development of biocontrol systems as an alternative to chemical pesticides for protection of important crop systems. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s12864-017-3848-6) contains supplementary material, which is available to authorized users. BioMed Central 2017-06-19 /pmc/articles/PMC5477169/ /pubmed/28629321 http://dx.doi.org/10.1186/s12864-017-3848-6 Text en © The Author(s). 2017 Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.
spellingShingle Research Article
Duke, Kelly A.
Becker, Michael G.
Girard, Ian J.
Millar, Jenna L.
Dilantha Fernando, W. G.
Belmonte, Mark F.
de Kievit, Teresa R.
The biocontrol agent Pseudomonas chlororaphis PA23 primes Brassica napus defenses through distinct gene networks
title The biocontrol agent Pseudomonas chlororaphis PA23 primes Brassica napus defenses through distinct gene networks
title_full The biocontrol agent Pseudomonas chlororaphis PA23 primes Brassica napus defenses through distinct gene networks
title_fullStr The biocontrol agent Pseudomonas chlororaphis PA23 primes Brassica napus defenses through distinct gene networks
title_full_unstemmed The biocontrol agent Pseudomonas chlororaphis PA23 primes Brassica napus defenses through distinct gene networks
title_short The biocontrol agent Pseudomonas chlororaphis PA23 primes Brassica napus defenses through distinct gene networks
title_sort biocontrol agent pseudomonas chlororaphis pa23 primes brassica napus defenses through distinct gene networks
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5477169/
https://www.ncbi.nlm.nih.gov/pubmed/28629321
http://dx.doi.org/10.1186/s12864-017-3848-6
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