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Effects of Excess Manganese on the Xylem Sap Protein Profile of Tomato (Solanum lycopersicum) as Revealed by Shotgun Proteomic Analysis

Metal toxicity is a common problem in crop species worldwide. Some metals are naturally toxic, whereas others such as manganese (Mn) are essential micro-nutrients for plant growth but can become toxic when in excess. Changes in the composition of the xylem sap, which is the main pathway for ion tran...

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Autores principales: Ceballos-Laita, Laura, Gutierrez-Carbonell, Elain, Takahashi, Daisuke, Lonsdale, Andrew, Abadía, Anunciación, Doblin, Monika S., Bacic, Antony, Uemura, Matsuo, Abadía, Javier, López-Millán, Ana Flor
Formato: Online Artículo Texto
Lenguaje:English
Publicado: MDPI 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7700171/
https://www.ncbi.nlm.nih.gov/pubmed/33238539
http://dx.doi.org/10.3390/ijms21228863
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author Ceballos-Laita, Laura
Gutierrez-Carbonell, Elain
Takahashi, Daisuke
Lonsdale, Andrew
Abadía, Anunciación
Doblin, Monika S.
Bacic, Antony
Uemura, Matsuo
Abadía, Javier
López-Millán, Ana Flor
author_facet Ceballos-Laita, Laura
Gutierrez-Carbonell, Elain
Takahashi, Daisuke
Lonsdale, Andrew
Abadía, Anunciación
Doblin, Monika S.
Bacic, Antony
Uemura, Matsuo
Abadía, Javier
López-Millán, Ana Flor
author_sort Ceballos-Laita, Laura
collection PubMed
description Metal toxicity is a common problem in crop species worldwide. Some metals are naturally toxic, whereas others such as manganese (Mn) are essential micro-nutrients for plant growth but can become toxic when in excess. Changes in the composition of the xylem sap, which is the main pathway for ion transport within the plant, is therefore vital to understanding the plant’s response(s) to metal toxicity. In this study we have assessed the effects of exposure of tomato roots to excess Mn on the protein profile of the xylem sap, using a shotgun proteomics approach. Plants were grown in nutrient solution using 4.6 and 300 µM MnCl(2) as control and excess Mn treatments, respectively. This approach yielded 668 proteins reliably identified and quantified. Excess Mn caused statistically significant (at p ≤ 0.05) and biologically relevant changes in relative abundance (≥2-fold increases or ≥50% decreases) in 322 proteins, with 82% of them predicted to be secretory using three different prediction tools, with more decreasing than increasing (181 and 82, respectively), suggesting that this metal stress causes an overall deactivation of metabolic pathways. Processes most affected by excess Mn were in the oxido-reductase, polysaccharide and protein metabolism classes. Excess Mn induced changes in hydrolases and peroxidases involved in cell wall degradation and lignin formation, respectively, consistent with the existence of alterations in the cell wall. Protein turnover was also affected, as indicated by the decrease in proteolytic enzymes and protein synthesis-related proteins. Excess Mn modified the redox environment of the xylem sap, with changes in the abundance of oxido-reductase and defense protein classes indicating a stress scenario. Finally, results indicate that excess Mn decreased the amounts of proteins associated with several signaling pathways, including fasciclin-like arabinogalactan-proteins and lipids, as well as proteases, which may be involved in the release of signaling peptides and protein maturation. The comparison of the proteins changing in abundance in xylem sap and roots indicate the existence of tissue-specific and systemic responses to excess Mn. Data are available via ProteomeXchange with identifier PXD021973.
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spelling pubmed-77001712020-11-30 Effects of Excess Manganese on the Xylem Sap Protein Profile of Tomato (Solanum lycopersicum) as Revealed by Shotgun Proteomic Analysis Ceballos-Laita, Laura Gutierrez-Carbonell, Elain Takahashi, Daisuke Lonsdale, Andrew Abadía, Anunciación Doblin, Monika S. Bacic, Antony Uemura, Matsuo Abadía, Javier López-Millán, Ana Flor Int J Mol Sci Article Metal toxicity is a common problem in crop species worldwide. Some metals are naturally toxic, whereas others such as manganese (Mn) are essential micro-nutrients for plant growth but can become toxic when in excess. Changes in the composition of the xylem sap, which is the main pathway for ion transport within the plant, is therefore vital to understanding the plant’s response(s) to metal toxicity. In this study we have assessed the effects of exposure of tomato roots to excess Mn on the protein profile of the xylem sap, using a shotgun proteomics approach. Plants were grown in nutrient solution using 4.6 and 300 µM MnCl(2) as control and excess Mn treatments, respectively. This approach yielded 668 proteins reliably identified and quantified. Excess Mn caused statistically significant (at p ≤ 0.05) and biologically relevant changes in relative abundance (≥2-fold increases or ≥50% decreases) in 322 proteins, with 82% of them predicted to be secretory using three different prediction tools, with more decreasing than increasing (181 and 82, respectively), suggesting that this metal stress causes an overall deactivation of metabolic pathways. Processes most affected by excess Mn were in the oxido-reductase, polysaccharide and protein metabolism classes. Excess Mn induced changes in hydrolases and peroxidases involved in cell wall degradation and lignin formation, respectively, consistent with the existence of alterations in the cell wall. Protein turnover was also affected, as indicated by the decrease in proteolytic enzymes and protein synthesis-related proteins. Excess Mn modified the redox environment of the xylem sap, with changes in the abundance of oxido-reductase and defense protein classes indicating a stress scenario. Finally, results indicate that excess Mn decreased the amounts of proteins associated with several signaling pathways, including fasciclin-like arabinogalactan-proteins and lipids, as well as proteases, which may be involved in the release of signaling peptides and protein maturation. The comparison of the proteins changing in abundance in xylem sap and roots indicate the existence of tissue-specific and systemic responses to excess Mn. Data are available via ProteomeXchange with identifier PXD021973. MDPI 2020-11-23 /pmc/articles/PMC7700171/ /pubmed/33238539 http://dx.doi.org/10.3390/ijms21228863 Text en © 2020 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (http://creativecommons.org/licenses/by/4.0/).
spellingShingle Article
Ceballos-Laita, Laura
Gutierrez-Carbonell, Elain
Takahashi, Daisuke
Lonsdale, Andrew
Abadía, Anunciación
Doblin, Monika S.
Bacic, Antony
Uemura, Matsuo
Abadía, Javier
López-Millán, Ana Flor
Effects of Excess Manganese on the Xylem Sap Protein Profile of Tomato (Solanum lycopersicum) as Revealed by Shotgun Proteomic Analysis
title Effects of Excess Manganese on the Xylem Sap Protein Profile of Tomato (Solanum lycopersicum) as Revealed by Shotgun Proteomic Analysis
title_full Effects of Excess Manganese on the Xylem Sap Protein Profile of Tomato (Solanum lycopersicum) as Revealed by Shotgun Proteomic Analysis
title_fullStr Effects of Excess Manganese on the Xylem Sap Protein Profile of Tomato (Solanum lycopersicum) as Revealed by Shotgun Proteomic Analysis
title_full_unstemmed Effects of Excess Manganese on the Xylem Sap Protein Profile of Tomato (Solanum lycopersicum) as Revealed by Shotgun Proteomic Analysis
title_short Effects of Excess Manganese on the Xylem Sap Protein Profile of Tomato (Solanum lycopersicum) as Revealed by Shotgun Proteomic Analysis
title_sort effects of excess manganese on the xylem sap protein profile of tomato (solanum lycopersicum) as revealed by shotgun proteomic analysis
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7700171/
https://www.ncbi.nlm.nih.gov/pubmed/33238539
http://dx.doi.org/10.3390/ijms21228863
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