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. 2015 Sep 1;10(9):e0136606.
doi: 10.1371/journal.pone.0136606. eCollection 2015.

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

Affiliations

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

Qingqing Xie et al. PLoS One. .

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.

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Conflict of interest statement

Competing Interests: The authors have declared that no competing interests exist.

Figures

Fig 1
Fig 1. Eucalyptus grandis × E. urophylla growing at Liancheng manganese tailings in Southern China.
Fig 2
Fig 2. 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.
Fig 3
Fig 3. 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).
Fig 4
Fig 4. Anatomical structure of the Eucalyptus grandis × E. urophylla:
a leaf from the mining area (A) including the upper epidermis (1), palisade (2), sponge tissue (3), lower epidermis (4), xylem of vein (5), phloem of vein (6) and collenchyma (7); stem from mining area (B) including the periderm (8), phloem (9), cambium (10), xylem near the cambium (11), xylem near the vessel (12), vessel (13). (C) Distribution of Mn in the leaf cross-section. (D) Distribution of Mn in the stem cross-section. The empty bar represented samples from the control area (CA) and the filled gray bar represented samples from the mine tailing area (Mine). Data represents mean ± SE. (n = 3). (The asterisks on the bars indicate significant differences after t-test statistical analyses, *p < 0.05).
Fig 5
Fig 5. Subcellular distribution of Mn.
CA represents samples from the control area, and Mine represents samples from the mine tailing area. Data represents mean ± SE. (n = 3).
Fig 6
Fig 6. SEC/UV/ICPMS chromatograms of the water-soluble fractions from leaves and stems of Eucalyptus grandis × E. urophylla.
The leaves (A) and stems (C) from the control area; the leaves (B) and stems (D) from the mining area; Peak 1, Mn associated with high molecular weight proteins; peak 2, Mn associated with low molecular weight compounds.
Fig 7
Fig 7. Elution profiles of leaf subcellular soluble proteins with Size-exclusion columns coupled to ICP-MS.
(Leaf samples all from the mining area.) Covalently-bound cell wall protein (A) and ionically-bound cell wall protein (B); Chloroplast PSI(C); Chloroplast PSII (D) and Vacuole protein (E). 1, high molecular weight chelate; 2, middle molecular weight chelate; 3, low molecular weight.
Fig 8
Fig 8. 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.
Fig 9
Fig 9. Typical chromatogram of ten organic acid standards by RP-HPLC
(A). a, oxalic acid; b, tartaric acid; c, formic acid; d, malic acid; e, lactic acid; f, acetic acid; g, maleic acid; h, citric acid; i, fumaric acid; j, succinic acid. (B) RP-HPLC of the small molecular-Mn complexes in the leaf sample peak 2 (Fig 6B).

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