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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

Accumulation of Mn in the roots, stems and leaves of Eucalyptus grandis × E. urophylla.Seedlings were treated with different Mn treatments (5, 500, 104 and 2×104 μM) in hydroponic solution for one week. Mn content in different tissues was measured with ICP-OES. Data represents mean ± SE. (n = 3).
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pone.0136606.g003: Accumulation of Mn in the roots, stems and leaves of Eucalyptus grandis × E. urophylla.Seedlings were treated with different Mn treatments (5, 500, 104 and 2×104 μM) in hydroponic solution for one week. Mn content in different tissues was measured with ICP-OES. Data represents mean ± SE. (n = 3).

Mentions: We measured Mn concentrations in the roots, stems and leaves of Mn-stressed Eucalyptus grandis × E. urophylla using ICP-MS. The Mn distribution in different tissues is shown in (Fig 3). The plant accumulated Mn in all tissues and the accumulation increased with increasing Mn concentration in the culture solution. When exposed to hydroponic solution with 5 μM Mn (corresponding to 0.28 mg Mn/kg), the Mn content in Eucalyptus grandis × E. urophylla tissues were: leaf (595 mg/kg) > stem (157 mg/kg) > root (52 mg/kg). When treated with 500 μM Mn (corresponding to 28 mg/kg), the stems (3662 mg/kg) accumulated a similar amount of Mn as leaves (3792 mg/Kg), and both were approximately 15 times higher than roots (249 mg/Kg). When exposed to elevated Mn levels, especially 10,000 and 20,000 μM (corresponding to 549.4 and 1098.8 mg/Kg), we unexpectedly observed that the stems accumulated much higher Mn (29,018 and 52,540 mg/Kg) than the leaves (5,676 and 11,715 mg/Kg) and roots (1,965 and 8,459 mg/Kg). These observations indicate that young Eucalyptus grandis × E. urophylla plants accumulate more Mn in the stems when exposed to extremely toxic Mn levels to protect the young leaves, which is an important site for photosynthesis. Nevertheless, when the plants mature and have enough leaves to increase their Mn storage capacity and Mn detoxification, the Mn is transported and stored in the leaves, which explain why the leaf Mn concentration (13549 mg/kg) was much higher than that in the stems (5231 mg/kg) of the 1–2 years old Eucalyptus grandis × E. urophylla collected at the mining area. This could imply that the Mn stem-accumulation of Eucalyptus grandis × E. urophylla during its early development is a useful strategy to protect seedlings from Mn stress. However, while our results are suggestive, it is unclear if the development stage has a strong effect on metal accumulation and additional experiments on different plant species are warranted.


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)

Accumulation of Mn in the roots, stems and leaves of Eucalyptus grandis × E. urophylla.Seedlings were treated with different Mn treatments (5, 500, 104 and 2×104 μM) in hydroponic solution for one week. Mn content in different tissues was measured with ICP-OES. Data represents mean ± SE. (n = 3).
© Copyright Policy
Related In: Results  -  Collection

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

pone.0136606.g003: Accumulation of Mn in the roots, stems and leaves of Eucalyptus grandis × E. urophylla.Seedlings were treated with different Mn treatments (5, 500, 104 and 2×104 μM) in hydroponic solution for one week. Mn content in different tissues was measured with ICP-OES. Data represents mean ± SE. (n = 3).
Mentions: We measured Mn concentrations in the roots, stems and leaves of Mn-stressed Eucalyptus grandis × E. urophylla using ICP-MS. The Mn distribution in different tissues is shown in (Fig 3). The plant accumulated Mn in all tissues and the accumulation increased with increasing Mn concentration in the culture solution. When exposed to hydroponic solution with 5 μM Mn (corresponding to 0.28 mg Mn/kg), the Mn content in Eucalyptus grandis × E. urophylla tissues were: leaf (595 mg/kg) > stem (157 mg/kg) > root (52 mg/kg). When treated with 500 μM Mn (corresponding to 28 mg/kg), the stems (3662 mg/kg) accumulated a similar amount of Mn as leaves (3792 mg/Kg), and both were approximately 15 times higher than roots (249 mg/Kg). When exposed to elevated Mn levels, especially 10,000 and 20,000 μM (corresponding to 549.4 and 1098.8 mg/Kg), we unexpectedly observed that the stems accumulated much higher Mn (29,018 and 52,540 mg/Kg) than the leaves (5,676 and 11,715 mg/Kg) and roots (1,965 and 8,459 mg/Kg). These observations indicate that young Eucalyptus grandis × E. urophylla plants accumulate more Mn in the stems when exposed to extremely toxic Mn levels to protect the young leaves, which is an important site for photosynthesis. Nevertheless, when the plants mature and have enough leaves to increase their Mn storage capacity and Mn detoxification, the Mn is transported and stored in the leaves, which explain why the leaf Mn concentration (13549 mg/kg) was much higher than that in the stems (5231 mg/kg) of the 1–2 years old Eucalyptus grandis × E. urophylla collected at the mining area. This could imply that the Mn stem-accumulation of Eucalyptus grandis × E. urophylla during its early development is a useful strategy to protect seedlings from Mn stress. However, while our results are suggestive, it is unclear if the development stage has a strong effect on metal accumulation and additional experiments on different plant species are warranted.

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