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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

Observed Mn toxicity in Eucalyptus grandis × E. urophylla.Seedlings were treated in hydroponic solution with different levels of Mn for one week. A, the control Hoagland solution plus (5 μM); B, 500 μM; C, 5×103 μM; D, 10×103 μM; E, 20×103 μM Mn. The white arrow in D indicated young leaves which turned purple, curled and crinkling symptoms under 10×103 μM Mn treatment.
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pone.0136606.g002: Observed Mn toxicity in Eucalyptus grandis × E. urophylla.Seedlings were treated in hydroponic solution with different levels of Mn for one week. A, the control Hoagland solution plus (5 μM); B, 500 μM; C, 5×103 μM; D, 10×103 μM; E, 20×103 μM Mn. The white arrow in D indicated young leaves which turned purple, curled and crinkling symptoms under 10×103 μM Mn treatment.

Mentions: Seeds of Eucalyptus grandis × E.urophylla were surface sterilized and grown in a hydroponic system. Two-month-old seedlings were treated with different Mn concentrations for one week. The seedlings grew normally in Hogaland solutions containing 5 to 5,000 μM Mn without showing toxicity symptoms (Fig 2A, 2B and 2C); however, when exposed to 10,000 μM Mn, toxicity was observed in the seedlings. More specifically, only one or two young leaves turned purple, curled and crinkling symptoms were observed but the other leaves seemed normal and the whole seedling did not show impaired growth compared to lower Mn treatments (Fig 2D). When exposed to 20, 000 μM Mn (corresponding to 1,098.8 mg/kg), all the leaves showed strong symptoms of Mn toxicity with most of them turning purple and curling (Fig 2E). The critical concentration for Mn toxicity varies between plant species, but most plants show toxicity symptoms at Mn concentrations of 160–200 mg/kg [43]. Our results suggest that Eucalyptus grandis × E. urophylla can tolerate up to 10, 000 μM Mn (corresponding to 549.4 mg/kg) making its Mn tolerance ability similar to another Mn hyper-accumulator previously found in China, Phytolacca acinosa Roxb [29]. In a previous report, the acid-extractable Mn in soil from the Liancheng mining area accounts for 0.46 to 1.3% (wt/wt) [44]. Based on the total Mn concentration in the soils collected near Eucalyptus grandis × E. urophylla plants, the acid-extractable Mn ranged from 63.2 to 178.6 mg/kg. We are aware that the acid-extractable Mn in soil is much higher than the bioavailable Mn. However, if the threshold Mn concentration is 10,000 μM (corresponding to 549.4 mg/kg) based on the results of the hydroponic exposure experiments, the maximum Mn tolerance capacity of Eucalyptus grandis × E. urophylla has not yet been reached in the soil. Based on these findings, Eucalyptus grandis × E. urophylla should be a good candidate for remediating soils with extremely toxic amounts of Mn and may also be a good candidate for phyto-mining of Mn.


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)

Observed Mn toxicity in Eucalyptus grandis × E. urophylla.Seedlings were treated in hydroponic solution with different levels of Mn for one week. A, the control Hoagland solution plus (5 μM); B, 500 μM; C, 5×103 μM; D, 10×103 μM; E, 20×103 μM Mn. The white arrow in D indicated young leaves which turned purple, curled and crinkling symptoms under 10×103 μM Mn treatment.
© Copyright Policy
Related In: Results  -  Collection

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

pone.0136606.g002: Observed Mn toxicity in Eucalyptus grandis × E. urophylla.Seedlings were treated in hydroponic solution with different levels of Mn for one week. A, the control Hoagland solution plus (5 μM); B, 500 μM; C, 5×103 μM; D, 10×103 μM; E, 20×103 μM Mn. The white arrow in D indicated young leaves which turned purple, curled and crinkling symptoms under 10×103 μM Mn treatment.
Mentions: Seeds of Eucalyptus grandis × E.urophylla were surface sterilized and grown in a hydroponic system. Two-month-old seedlings were treated with different Mn concentrations for one week. The seedlings grew normally in Hogaland solutions containing 5 to 5,000 μM Mn without showing toxicity symptoms (Fig 2A, 2B and 2C); however, when exposed to 10,000 μM Mn, toxicity was observed in the seedlings. More specifically, only one or two young leaves turned purple, curled and crinkling symptoms were observed but the other leaves seemed normal and the whole seedling did not show impaired growth compared to lower Mn treatments (Fig 2D). When exposed to 20, 000 μM Mn (corresponding to 1,098.8 mg/kg), all the leaves showed strong symptoms of Mn toxicity with most of them turning purple and curling (Fig 2E). The critical concentration for Mn toxicity varies between plant species, but most plants show toxicity symptoms at Mn concentrations of 160–200 mg/kg [43]. Our results suggest that Eucalyptus grandis × E. urophylla can tolerate up to 10, 000 μM Mn (corresponding to 549.4 mg/kg) making its Mn tolerance ability similar to another Mn hyper-accumulator previously found in China, Phytolacca acinosa Roxb [29]. In a previous report, the acid-extractable Mn in soil from the Liancheng mining area accounts for 0.46 to 1.3% (wt/wt) [44]. Based on the total Mn concentration in the soils collected near Eucalyptus grandis × E. urophylla plants, the acid-extractable Mn ranged from 63.2 to 178.6 mg/kg. We are aware that the acid-extractable Mn in soil is much higher than the bioavailable Mn. However, if the threshold Mn concentration is 10,000 μM (corresponding to 549.4 mg/kg) based on the results of the hydroponic exposure experiments, the maximum Mn tolerance capacity of Eucalyptus grandis × E. urophylla has not yet been reached in the soil. Based on these findings, Eucalyptus grandis × E. urophylla should be a good candidate for remediating soils with extremely toxic amounts of Mn and may also be a good candidate for phyto-mining of Mn.

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