Effects of Excess Manganese on the Xylem Sap Protein Profile of Tomato (<i>Solanum lycopersicum</i>) 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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| Format: | Article |
| Language: | English |
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MDPI AG
2020-11-01
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| Series: | International Journal of Molecular Sciences |
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| Online Access: | https://www.mdpi.com/1422-0067/21/22/8863 |
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| author | Laura Ceballos-Laita Elain Gutierrez-Carbonell Daisuke Takahashi Andrew Lonsdale Anunciación Abadía Monika S. Doblin Antony Bacic Matsuo Uemura Javier Abadía Ana Flor López-Millán |
| author_facet | Laura Ceballos-Laita Elain Gutierrez-Carbonell Daisuke Takahashi Andrew Lonsdale Anunciación Abadía Monika S. Doblin Antony Bacic Matsuo Uemura Javier Abadía Ana Flor López-Millán |
| author_sort | Laura Ceballos-Laita |
| collection | DOAJ |
| 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<sub>2</sub> as control and excess Mn treatments, respectively. This approach yielded 668 proteins reliably identified and quantified. Excess Mn caused statistically significant (at <i>p</i> ≤ 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. |
| first_indexed | 2024-03-10T14:37:53Z |
| format | Article |
| id | doaj.art-62f8829b30a44ff0b8f297fe13fa48c2 |
| institution | Directory Open Access Journal |
| issn | 1661-6596 1422-0067 |
| language | English |
| last_indexed | 2024-03-10T14:37:53Z |
| publishDate | 2020-11-01 |
| publisher | MDPI AG |
| record_format | Article |
| series | International Journal of Molecular Sciences |
| spelling | doaj.art-62f8829b30a44ff0b8f297fe13fa48c22023-11-20T22:00:02ZengMDPI AGInternational Journal of Molecular Sciences1661-65961422-00672020-11-012122886310.3390/ijms21228863Effects of Excess Manganese on the Xylem Sap Protein Profile of Tomato (<i>Solanum lycopersicum</i>) as Revealed by Shotgun Proteomic AnalysisLaura Ceballos-Laita0Elain Gutierrez-Carbonell1Daisuke Takahashi2Andrew Lonsdale3Anunciación Abadía4Monika S. Doblin5Antony Bacic6Matsuo Uemura7Javier Abadía8Ana Flor López-Millán9Plant Stress Physiology Group, Plant Nutrition Department, Aula Dei Experimental Station, CSIC, P.O. Box 13034, 50080 Zaragoza, SpainPlant Stress Physiology Group, Plant Nutrition Department, Aula Dei Experimental Station, CSIC, P.O. Box 13034, 50080 Zaragoza, SpainUnited Graduate School of Agricultural Sciences, Iwate University, Morioka 020-8550, JapanSchool of Biosciences, The University of Melbourne, Parkville, VIC 3052, AustraliaPlant Stress Physiology Group, Plant Nutrition Department, Aula Dei Experimental Station, CSIC, P.O. Box 13034, 50080 Zaragoza, SpainLa Trobe Institute for Agriculture & Food, Department of Animal, Plant & Soil Sciences, AgriBio Building, La Trobe University, Bundoora, VIC 3086, AustraliaLa Trobe Institute for Agriculture & Food, Department of Animal, Plant & Soil Sciences, AgriBio Building, La Trobe University, Bundoora, VIC 3086, AustraliaUnited Graduate School of Agricultural Sciences, Iwate University, Morioka 020-8550, JapanPlant Stress Physiology Group, Plant Nutrition Department, Aula Dei Experimental Station, CSIC, P.O. Box 13034, 50080 Zaragoza, SpainPlant Stress Physiology Group, Plant Nutrition Department, Aula Dei Experimental Station, CSIC, P.O. Box 13034, 50080 Zaragoza, SpainMetal 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<sub>2</sub> as control and excess Mn treatments, respectively. This approach yielded 668 proteins reliably identified and quantified. Excess Mn caused statistically significant (at <i>p</i> ≤ 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.https://www.mdpi.com/1422-0067/21/22/8863xylem sapmanganese toxicityproteometomatoshotgun proteomics |
| spellingShingle | Laura Ceballos-Laita Elain Gutierrez-Carbonell Daisuke Takahashi Andrew Lonsdale Anunciación Abadía Monika S. Doblin Antony Bacic Matsuo Uemura Javier Abadía Ana Flor López-Millán Effects of Excess Manganese on the Xylem Sap Protein Profile of Tomato (<i>Solanum lycopersicum</i>) as Revealed by Shotgun Proteomic Analysis International Journal of Molecular Sciences xylem sap manganese toxicity proteome tomato shotgun proteomics |
| title | Effects of Excess Manganese on the Xylem Sap Protein Profile of Tomato (<i>Solanum lycopersicum</i>) as Revealed by Shotgun Proteomic Analysis |
| title_full | Effects of Excess Manganese on the Xylem Sap Protein Profile of Tomato (<i>Solanum lycopersicum</i>) as Revealed by Shotgun Proteomic Analysis |
| title_fullStr | Effects of Excess Manganese on the Xylem Sap Protein Profile of Tomato (<i>Solanum lycopersicum</i>) as Revealed by Shotgun Proteomic Analysis |
| title_full_unstemmed | Effects of Excess Manganese on the Xylem Sap Protein Profile of Tomato (<i>Solanum lycopersicum</i>) as Revealed by Shotgun Proteomic Analysis |
| title_short | Effects of Excess Manganese on the Xylem Sap Protein Profile of Tomato (<i>Solanum lycopersicum</i>) as Revealed by Shotgun Proteomic Analysis |
| title_sort | effects of excess manganese on the xylem sap protein profile of tomato i solanum lycopersicum i as revealed by shotgun proteomic analysis |
| topic | xylem sap manganese toxicity proteome tomato shotgun proteomics |
| url | https://www.mdpi.com/1422-0067/21/22/8863 |
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