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Phosphite-induced changes of the transcriptome and secretome in Solanum tuberosum leading to resistance against Phytophthora infestans

BACKGROUND: Potato late blight caused by the oomycete pathogen Phytophthora infestans can lead to immense yield loss. We investigated the transcriptome of Solanum tubersoum (cv. Desiree) and characterized the secretome by quantitative proteomics after foliar application of the protective agent phosp...

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Autores principales: Burra, Dharani Dhar, Berkowitz, Oliver, Hedley, Pete E, Morris, Jenny, Resjö, Svante, Levander, Fredrik, Liljeroth, Erland, Andreasson, Erik, Alexandersson, Erik
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2014
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4192290/
https://www.ncbi.nlm.nih.gov/pubmed/25270759
http://dx.doi.org/10.1186/s12870-014-0254-y
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author Burra, Dharani Dhar
Berkowitz, Oliver
Hedley, Pete E
Morris, Jenny
Resjö, Svante
Levander, Fredrik
Liljeroth, Erland
Andreasson, Erik
Alexandersson, Erik
author_facet Burra, Dharani Dhar
Berkowitz, Oliver
Hedley, Pete E
Morris, Jenny
Resjö, Svante
Levander, Fredrik
Liljeroth, Erland
Andreasson, Erik
Alexandersson, Erik
author_sort Burra, Dharani Dhar
collection PubMed
description BACKGROUND: Potato late blight caused by the oomycete pathogen Phytophthora infestans can lead to immense yield loss. We investigated the transcriptome of Solanum tubersoum (cv. Desiree) and characterized the secretome by quantitative proteomics after foliar application of the protective agent phosphite. We also studied the distribution of phosphite in planta after application and tested transgenic potato lines with impaired in salicylic and jasmonic acid signaling. RESULTS: Phosphite had a rapid and transient effect on the transcriptome, with a clear response 3 h after treatment. Strikingly this effect lasted less than 24 h, whereas protection was observed throughout all time points tested. In contrast, 67 secretome proteins predominantly associated with cell-wall processes and defense changed in abundance at 48 h after treatment. Transcripts associated with defense, wounding, and oxidative stress constituted the core of the phosphite response. We also observed changes in primary metabolism and cell wall-related processes. These changes were shown not to be due to phosphate depletion or acidification caused by phosphite treatment. Of the phosphite-regulated transcripts 40% also changed with β-aminobutyric acid (BABA) as an elicitor, while the defence gene PR1 was only up-regulated by BABA. Although phosphite was shown to be distributed in planta to parts not directly exposed to phosphite, no protection in leaves without direct foliar application was observed. Furthermore, the analysis of transgenic potato lines indicated that the phosphite-mediated resistance was independent of the plant hormones salicylic and jasmonic acid. CONCLUSIONS: Our study suggests that a rapid phosphite-triggered response is important to confer long-lasting resistance against P. infestans and gives molecular understanding of its successful field applications. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s12870-014-0254-y) contains supplementary material, which is available to authorized users.
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spelling pubmed-41922902014-10-11 Phosphite-induced changes of the transcriptome and secretome in Solanum tuberosum leading to resistance against Phytophthora infestans Burra, Dharani Dhar Berkowitz, Oliver Hedley, Pete E Morris, Jenny Resjö, Svante Levander, Fredrik Liljeroth, Erland Andreasson, Erik Alexandersson, Erik BMC Plant Biol Research Article BACKGROUND: Potato late blight caused by the oomycete pathogen Phytophthora infestans can lead to immense yield loss. We investigated the transcriptome of Solanum tubersoum (cv. Desiree) and characterized the secretome by quantitative proteomics after foliar application of the protective agent phosphite. We also studied the distribution of phosphite in planta after application and tested transgenic potato lines with impaired in salicylic and jasmonic acid signaling. RESULTS: Phosphite had a rapid and transient effect on the transcriptome, with a clear response 3 h after treatment. Strikingly this effect lasted less than 24 h, whereas protection was observed throughout all time points tested. In contrast, 67 secretome proteins predominantly associated with cell-wall processes and defense changed in abundance at 48 h after treatment. Transcripts associated with defense, wounding, and oxidative stress constituted the core of the phosphite response. We also observed changes in primary metabolism and cell wall-related processes. These changes were shown not to be due to phosphate depletion or acidification caused by phosphite treatment. Of the phosphite-regulated transcripts 40% also changed with β-aminobutyric acid (BABA) as an elicitor, while the defence gene PR1 was only up-regulated by BABA. Although phosphite was shown to be distributed in planta to parts not directly exposed to phosphite, no protection in leaves without direct foliar application was observed. Furthermore, the analysis of transgenic potato lines indicated that the phosphite-mediated resistance was independent of the plant hormones salicylic and jasmonic acid. CONCLUSIONS: Our study suggests that a rapid phosphite-triggered response is important to confer long-lasting resistance against P. infestans and gives molecular understanding of its successful field applications. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s12870-014-0254-y) contains supplementary material, which is available to authorized users. BioMed Central 2014-10-01 /pmc/articles/PMC4192290/ /pubmed/25270759 http://dx.doi.org/10.1186/s12870-014-0254-y Text en © Burra et al.; licensee BioMed Central Ltd. 2014 This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly credited. 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
Burra, Dharani Dhar
Berkowitz, Oliver
Hedley, Pete E
Morris, Jenny
Resjö, Svante
Levander, Fredrik
Liljeroth, Erland
Andreasson, Erik
Alexandersson, Erik
Phosphite-induced changes of the transcriptome and secretome in Solanum tuberosum leading to resistance against Phytophthora infestans
title Phosphite-induced changes of the transcriptome and secretome in Solanum tuberosum leading to resistance against Phytophthora infestans
title_full Phosphite-induced changes of the transcriptome and secretome in Solanum tuberosum leading to resistance against Phytophthora infestans
title_fullStr Phosphite-induced changes of the transcriptome and secretome in Solanum tuberosum leading to resistance against Phytophthora infestans
title_full_unstemmed Phosphite-induced changes of the transcriptome and secretome in Solanum tuberosum leading to resistance against Phytophthora infestans
title_short Phosphite-induced changes of the transcriptome and secretome in Solanum tuberosum leading to resistance against Phytophthora infestans
title_sort phosphite-induced changes of the transcriptome and secretome in solanum tuberosum leading to resistance against phytophthora infestans
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4192290/
https://www.ncbi.nlm.nih.gov/pubmed/25270759
http://dx.doi.org/10.1186/s12870-014-0254-y
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