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Interaction of nickel and manganese in accumulation and localization in leaves of the Ni hyperaccumulators Alyssum murale and Alyssum corsicum

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Abstract

The genus Alyssum contains >50 Ni hyperaccumulator species; many can achieve >2.5% Ni in dry leaf. In soils with normal Mn levels, Alyssum trichome bases were previously observed to accumulate Ni and Mn to high levels. Here we report concentration and localization patterns in A. murale and A. corsicum grown in soils with nonphytotoxic factorial additions of Ni and Mn salts. Four leaf type subsets based on size and age accumulated Ni and Mn similarly. The greatest Mn accumulation (10 times control) was observed in A. corsicum with 40 mmol Mn kg−1 and 40 mmol Ni kg−1 added to potting soil. Whole leaf Ni concentrations decreased as Mn increased. Synchrotron X-ray fluorescence mapping of whole fresh leaves showed localized in distinct high-concentration Mn spots associated with trichomes, Ni and Mn distributions were strongly spatially correlated. Standard X-ray fluorescence point analysis/mapping of cryofractured and freeze-dried samples found that Ni and Mn were co-located and strongly concentrated only in trichome bases and in cells adjacent to trichomes. Nickel concentration was also strongly spatially correlated with sulfur. Results indicate that maximum Ni phytoextraction by Alyssum may be reduced in soils with higher phytoavailable Mn, and suggest that Ni hyperaccumulation in Alyssum species may have developed from a Mn handling system.

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Acknowledgements

We greatly appreciate the assistance of USDA-ARS personnel Carrie Green for ICP analyses and Christopher Pooley for computer graphics.

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Authors and Affiliations

  1. US Department of Agriculture Henry A. Wallace Agricultural Research Center, Environmental Management and Byproduct Utilization Laboratory, Animal and Natural Resources Institute, Bldg. 007, Beltsville, MD, 20705, USA

    C. Leigh Broadhurst & Rufus L. Chaney

  2. Plant and Soil Sciences Department, University of Delaware, Newark, DE, USA

    Ryan V. Tappero & Donald L. Sparks

  3. Laboratory for Biological Ultrastructure, Department of Biology, University of Maryland, College Park, USA

    Timothy K. Maugel

  4. Electron Microscopy Unit, Soybean Genomics and Improvement Laboratory, Plant Sciences Institute, USDA Beltsville, Beltsville, MD, USA

    Eric F. Erbe

Authors
  1. C. Leigh Broadhurst
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  2. Ryan V. Tappero
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  3. Timothy K. Maugel
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  4. Eric F. Erbe
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  5. Donald L. Sparks
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  6. Rufus L. Chaney
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Corresponding author

Correspondence to C. Leigh Broadhurst.

Additional information

Responsible editor: Fangjie J. Zhao.

Use of trade or proprietary names or trademarks herein is for informational purposes only and does not imply any advertisement or endorsement by the US Department of Agriculture, University of Maryland, or University of Delaware.

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Figure S1.

Alyssum corsicum trichome and adjacent cells (a) upper epidermis; (b) lower epidermis. The trichome basal compartment is roughly tear-drop shaped and lies directly beneath the trichome pedicle (PDF 63 KB).

Figure S2.

Ni μ-XANES spectra of generalized leaf epidermis, demonstrating the Ni absorption edge is similar to the Ni II standard (PDF 37 KB).

Figure S3.

Whole fresh leaf SXRF map for Ni10/Mn10 plant. Left panel shows Ni, Mn, Ca maps plus the tricolor map. Right panel shows the correlation for Ni Kα vs. Mn Kα counts for a selected trichome (masked on left) and the correlation for the whole leaf area (inset graph). The linear high Ni concentration feature parallel to the leaf margin in corresponds to the leaf margin curling away from the mounting tape and thus increasing the relative X-ray cross section—there is no pattern of very high Ni concentration associated with the leaf margin or tip. Due to the extensive network of trichomes, Ca signal covers nearly 100% of the image, so for presentation purposes a very high threshold of Ca signal intensity was set (PDF 36 KB).

Figure S4.

SEM guide photo of A. corsicum Ni10/Mn40 plant (7a). Leaf cross section, general upper epidermis and palisade mesophyll. X-ray maps (20 KeV) show Ni Kα (7b), Ni Lα (7c) Mn Kα (7d), Ca Kα (7e) and S Kα (7f) distribution. High Ca concentrations correspond to intact trichomes. The central concavity corresponds to the projection of the tip of trichome base in the complement fracture. Some material from the trichome base has been retained, yielding dispersed Ni and S signal (PDF 62 KB).

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Leigh Broadhurst, C., Tappero, R.V., Maugel, T.K. et al. Interaction of nickel and manganese in accumulation and localization in leaves of the Ni hyperaccumulators Alyssum murale and Alyssum corsicum . Plant Soil 314, 35–48 (2009). https://doi.org/10.1007/s11104-008-9703-4

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