Abstract
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 MnCl2 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.
Highlights
Manganese (Mn) is an essential micronutrient that plays important roles in many plant physiological processes [1]
Xylem bleeding rates were similar in plants treated with excess Mn and in the controls (0.52 and 0.56 mL g−1 DW h−1, respectively) whereas the protein concentration in the xylem was on average 3-fold higher in plants grown in the presence of high Mn compared to the controls (27 and 9 ng protein μL−1, respectively)
Excess Mn caused statistically significant and biologically relevant changes in the relative abundance of 322 proteins, with more decreasing than increasing, suggesting that this metal stress causes an overall deactivation of metabolic pathways
Summary
Manganese (Mn) is an essential micronutrient that plays important roles in many plant physiological processes [1]. When in excess, Mn can be toxic to plants [3]. Manganese occurs in soils largely in oxide forms, and is taken up by plants as Mn2+, with its availability being influenced by soil parameters such as soil structure and composition, water content, microbial activity and especially pH. Plant-available Mn can increase considerably in acidic soils, and this may lead to Mn toxicity [1,5]. Increases in soil acidity are driven by the use of intensive horticulture and acidifying fertilizers [3,6,7], as well as by climate events such as elevated ozone levels, increased ambient temperatures and emission of acidic gases [8,9,10]
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