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A Newly Identified Passive Hyperaccumulator Eucalyptus grandis × E. urophylla under Manganese Stress.

Xie Q, Li Z, Yang L, Lv J, Jobe TO, Wang Q - PLoS ONE (2015)

Bottom Line: These species are excellent candidates for developing a cost-effective remediation strategy for Mn-polluted soils.Our results from Scanning Electron Microscope (SEM) X-ray microanalysis indicate that Mn is distributed in the entire leaf and stem cross-section, especially in photosynthetic palisade, spongy mesophyll tissue, and stem xylem vessels.Moreover, the Mn-speciation profile obtained for the first time in different cellular organelles of Eucalyptus grandis × E. urophylla suggested that different organelles have differential accumulating abilities and unique mechanisms for Mn-detoxification.

View Article: PubMed Central - PubMed

Affiliation: Department of Chemistry, the MOE Key Laboratory of Spectrochemical Analysis & Instrumentation, College of Chemistry and Chemical Engineering, Xiamen University, Xiamen 361005, China.

ABSTRACT
Manganese (Mn) is an essential micronutrient needed for plant growth and development, but can be toxic to plants in excess amounts. However, some plant species have detoxification mechanisms that allow them to accumulate Mn to levels that are normally toxic, a phenomenon known as hyperaccumulation. These species are excellent candidates for developing a cost-effective remediation strategy for Mn-polluted soils. In this study, we identified a new passive Mn-hyperaccumulator Eucalyptus grandis × E. urophylla during a field survey in southern China in July 2010. This hybrid can accumulate as much as 13,549 mg/kg DW Mn in its leaves. Our results from Scanning Electron Microscope (SEM) X-ray microanalysis indicate that Mn is distributed in the entire leaf and stem cross-section, especially in photosynthetic palisade, spongy mesophyll tissue, and stem xylem vessels. Results from size-exclusion chromatography coupled with ICP-MS (Inductively coupled plasma mass spectrometry) lead us to speculate that Mn associates with relatively high molecular weight proteins and low molecular weight organic acids, including tartaric acid, to avoid Mn toxicity. Our results provide experimental evidence that both proteins and organic acids play important roles in Mn detoxification in Eucalyptus grandis × E. urophylla. The key characteristics of Eucalyptus grandis × E. urophylla are an increased Mn translocation facilitated by transpiration through the xylem to the leaves and further distribution throughout the leaf tissues. Moreover, the Mn-speciation profile obtained for the first time in different cellular organelles of Eucalyptus grandis × E. urophylla suggested that different organelles have differential accumulating abilities and unique mechanisms for Mn-detoxification.

No MeSH data available.


Related in: MedlinePlus

Concentrations of organic acids in leaves (A) and stems (B).The empty bar represents samples from the control area (CA) and the filled gray bar represents samples from the Mn site of the mine tailing area. Data represents mean ± SE. (n = 3). The asterisks on the bars indicate significant differences after t-test statistical analyses, *p < 0.05.
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pone.0136606.g008: Concentrations of organic acids in leaves (A) and stems (B).The empty bar represents samples from the control area (CA) and the filled gray bar represents samples from the Mn site of the mine tailing area. Data represents mean ± SE. (n = 3). The asterisks on the bars indicate significant differences after t-test statistical analyses, *p < 0.05.

Mentions: We extracted organic acids from the leaf and stem samples from both the control and Mn site with liquid nitrogen and dilute HCl. The acid-extractable fractions, which were believed to contain organic acids, were subjected to RP-HPLC. The results obtained (Fig 8A) indicate that leaf samples from the control area contain higher amounts of malic acid (15.19 ± 1.36 mg/g FW), maleic acid (11.4 ± 1.91), tartaric acid (8.57 ± 0.96), and succinic acid (5.98 ± 1.46), but lower fumaric (1.46 ± 1.12), formic (1.56 ± 0.77 mg/g FW) and oxalic acids (0.60 ± 0.37 mg/g FW). Compared with leaf samples from the control site, a greater than three fold increase in succinic acid (19.65 ± 0.38 mg/g FW) was found in leaf samples from the Mn site along with a slight increase in other organic acids. Surprisingly, we observed a decrease in maleic acid from (11.4 ± 1.91 mg/g FW) in the control to undetectable levels in samples collected from the Mn site along with a small decrease in malic acid. It should be noted that both acetic acid and citric acid were found at very low levels in not only the control leaves but also leaves from the Mn site. Unlike in the leaf samples, tartaric acid was the most abundant organic acid found in the stem sample extracts (Fig 8B). It increased significantly by about 2 fold in the Mn site stem samples (31.55 ± 1.69 mg/g FW) compared to the control area samples (14.76 ± 2.39 mg/g FW). However, malic and succinic acid concentrations decreased to (7.32 ± 1.92) and (6.03 ± 1.11 mg/g FW) in the leaf samples. Oxalic (0.57 ± 0.16 mg/g FW), formic (1.88 ± 1.73 mg/g FW), lactic (2.48 ± 0.36 mg/g FW), acetic (0.04 ± 0.001 mg/g FW), maleic (0.13 ± 0.10 mg/g FW) and citric acid (0.08 ± 0.001 mg/g FW) in stems from the Mn site were all lower than in samples from the control site. These results indicated that Mn exposure caused a dramatic decrease in maleic acid and an increase in succinic acid in the leaves but had smaller affects on other organic acids; however, tartaric acid did increase significantly in the stems.


A Newly Identified Passive Hyperaccumulator Eucalyptus grandis × E. urophylla under Manganese Stress.

Xie Q, Li Z, Yang L, Lv J, Jobe TO, Wang Q - PLoS ONE (2015)

Concentrations of organic acids in leaves (A) and stems (B).The empty bar represents samples from the control area (CA) and the filled gray bar represents samples from the Mn site of the mine tailing area. Data represents mean ± SE. (n = 3). The asterisks on the bars indicate significant differences after t-test statistical analyses, *p < 0.05.
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4556624&req=5

pone.0136606.g008: Concentrations of organic acids in leaves (A) and stems (B).The empty bar represents samples from the control area (CA) and the filled gray bar represents samples from the Mn site of the mine tailing area. Data represents mean ± SE. (n = 3). The asterisks on the bars indicate significant differences after t-test statistical analyses, *p < 0.05.
Mentions: We extracted organic acids from the leaf and stem samples from both the control and Mn site with liquid nitrogen and dilute HCl. The acid-extractable fractions, which were believed to contain organic acids, were subjected to RP-HPLC. The results obtained (Fig 8A) indicate that leaf samples from the control area contain higher amounts of malic acid (15.19 ± 1.36 mg/g FW), maleic acid (11.4 ± 1.91), tartaric acid (8.57 ± 0.96), and succinic acid (5.98 ± 1.46), but lower fumaric (1.46 ± 1.12), formic (1.56 ± 0.77 mg/g FW) and oxalic acids (0.60 ± 0.37 mg/g FW). Compared with leaf samples from the control site, a greater than three fold increase in succinic acid (19.65 ± 0.38 mg/g FW) was found in leaf samples from the Mn site along with a slight increase in other organic acids. Surprisingly, we observed a decrease in maleic acid from (11.4 ± 1.91 mg/g FW) in the control to undetectable levels in samples collected from the Mn site along with a small decrease in malic acid. It should be noted that both acetic acid and citric acid were found at very low levels in not only the control leaves but also leaves from the Mn site. Unlike in the leaf samples, tartaric acid was the most abundant organic acid found in the stem sample extracts (Fig 8B). It increased significantly by about 2 fold in the Mn site stem samples (31.55 ± 1.69 mg/g FW) compared to the control area samples (14.76 ± 2.39 mg/g FW). However, malic and succinic acid concentrations decreased to (7.32 ± 1.92) and (6.03 ± 1.11 mg/g FW) in the leaf samples. Oxalic (0.57 ± 0.16 mg/g FW), formic (1.88 ± 1.73 mg/g FW), lactic (2.48 ± 0.36 mg/g FW), acetic (0.04 ± 0.001 mg/g FW), maleic (0.13 ± 0.10 mg/g FW) and citric acid (0.08 ± 0.001 mg/g FW) in stems from the Mn site were all lower than in samples from the control site. These results indicated that Mn exposure caused a dramatic decrease in maleic acid and an increase in succinic acid in the leaves but had smaller affects on other organic acids; however, tartaric acid did increase significantly in the stems.

Bottom Line: These species are excellent candidates for developing a cost-effective remediation strategy for Mn-polluted soils.Our results from Scanning Electron Microscope (SEM) X-ray microanalysis indicate that Mn is distributed in the entire leaf and stem cross-section, especially in photosynthetic palisade, spongy mesophyll tissue, and stem xylem vessels.Moreover, the Mn-speciation profile obtained for the first time in different cellular organelles of Eucalyptus grandis × E. urophylla suggested that different organelles have differential accumulating abilities and unique mechanisms for Mn-detoxification.

View Article: PubMed Central - PubMed

Affiliation: Department of Chemistry, the MOE Key Laboratory of Spectrochemical Analysis & Instrumentation, College of Chemistry and Chemical Engineering, Xiamen University, Xiamen 361005, China.

ABSTRACT
Manganese (Mn) is an essential micronutrient needed for plant growth and development, but can be toxic to plants in excess amounts. However, some plant species have detoxification mechanisms that allow them to accumulate Mn to levels that are normally toxic, a phenomenon known as hyperaccumulation. These species are excellent candidates for developing a cost-effective remediation strategy for Mn-polluted soils. In this study, we identified a new passive Mn-hyperaccumulator Eucalyptus grandis × E. urophylla during a field survey in southern China in July 2010. This hybrid can accumulate as much as 13,549 mg/kg DW Mn in its leaves. Our results from Scanning Electron Microscope (SEM) X-ray microanalysis indicate that Mn is distributed in the entire leaf and stem cross-section, especially in photosynthetic palisade, spongy mesophyll tissue, and stem xylem vessels. Results from size-exclusion chromatography coupled with ICP-MS (Inductively coupled plasma mass spectrometry) lead us to speculate that Mn associates with relatively high molecular weight proteins and low molecular weight organic acids, including tartaric acid, to avoid Mn toxicity. Our results provide experimental evidence that both proteins and organic acids play important roles in Mn detoxification in Eucalyptus grandis × E. urophylla. The key characteristics of Eucalyptus grandis × E. urophylla are an increased Mn translocation facilitated by transpiration through the xylem to the leaves and further distribution throughout the leaf tissues. Moreover, the Mn-speciation profile obtained for the first time in different cellular organelles of Eucalyptus grandis × E. urophylla suggested that different organelles have differential accumulating abilities and unique mechanisms for Mn-detoxification.

No MeSH data available.


Related in: MedlinePlus