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Functional Plant Biology Functional Plant Biology Society
Plant function and evolutionary biology
RESEARCH ARTICLE

Novel pattern of foliar metal distribution in a manganese hyperaccumulator

Denise R. Fernando A E , Alan T. Marshall B , Barbara Gouget C , Marie Carrière C , Richard N. Collins D , Ian E. Woodrow A and Alan J. Baker A
+ Author Affiliations
- Author Affiliations

A School of Botany, The University of Melbourne, Parkville, Vic. 3010, Australia.

B Analytical Electron Microscopy Laboratory, Faculty of Science and Technology and Engineering, La Trobe University, Melbourne, Vic. 3086, Australia.

C Laboratoire Pierre Süe, CEA-CNRS, CEA/Saclay, F-91191 Gif-sur-Yvette, France.

D Center for Water and Waste Technology, School of Civil and Environmental Engineering, The University of New South Wales, Sydney, NSW 2052, Australia.

E Corresponding author. Email: d.fernando3@pgrad.unimelb.edu.au

Functional Plant Biology 35(3) 193-200 https://doi.org/10.1071/FP07272
Submitted: 19 November 2007  Accepted: 20 February 2008   Published: 23 April 2008

Abstract

The primary sequestration of foliar manganese (Mn) in Mn-hyperaccumulating plants can occur in either their photosynthetic or non-photosynthetic tissues, depending on the species. To date, only non-photosynthetic tissues have been found to be the major sinks in other hyperaccumulators. Here, electron (SEM) and proton (PIXE) microprobes were used to generate qualitative energy dispersive (EDS) X-ray maps of leaf cross sections. Two Mn hyperaccumulators, Garcinia amplexicaulis Vieill. (Clusiaceae) and Maytenus fournieri (Panch. and Sebert) Loesn. (Celastraceae), and the Mn accumulator Grevillea exul Lindley (Proteaceae) were studied. PIXE/EDS data obtained here for M. fournieri were in agreement with existing SEM/EDS data showing that the highest localised foliar Mn concentrations were in the epidermal tissues. However, this is the first in situ microprobe investigation of G. amplexicaulis and G. exul. The Mn X-ray maps of G. amplexicaulis revealed a previously undescribed third spatial distribution pattern among Mn-hyperaccumulating species. Manganese was relatively evenly distributed throughout the leaf photosynthetic and non-photosynthetic tissues, while in G. exul it was most highly concentrated in the epidermal cells.

Additional keywords: Garcinia amplexicaulis, Grevillea exul, localisation studies, Mn sequestration, PIXE/EDS, SEM/EDS.


Acknowledgements

The authors are extremely grateful to Vincent Dumontet and Alexandre Lagrange (IRD, Nouméa) for their help with identification of plants in the field, and to the late Nicolas Perrier (IRD, Nouméa) for his invaluable assistance in organising field collections. The use of the nuclear microprobe facility at the Laboratoire Pierre Süe, Commisariat à l’Energie Atomique (CEA), Saclay, France, and the help of Dr Hicham Khodja (CEA) are gratefully acknowledged.


References


Baker AJM, Brooks RR (1989) Terrestrial higher plants which hyperaccumulate metallic elements – a review of their distribution, ecology and phytochemistry. Biorecovery 1, 81–126. open url image1

Baker AJM, Whiting SN (2002) In search of the holy grail – a further step in understanding metal hyperaccumulation? The New Phytologist 155, 1–7.
Crossref | GoogleScholarGoogle Scholar | open url image1

Baker AJM , Proctor J , Reeves RD (1992) ‘The vegetation of ultramafic (serpentine) soils.’ (Intercept: University of California, Davis, CA)

Baker AJM, Reeves RD, Hajar ASM (1994) Heavy metal accumulation and tolerance in British populations of the metallophyte Thlaspi caerulescens J. & C. Presl (Brassicaceae). The New Phytologist 127, 61–68.
Crossref | GoogleScholarGoogle Scholar | open url image1

Baker AJM , McGrath SP , Reeves RD , Smith JAC (2000) Metal hyperaccumulator plants: a review of the ecology and physiology of a biological resource for phytoremediation of metal-polluted soils. In ‘Phytoremediation of contaminated soil and water’. (Eds N Terry, G Bañuelos) pp. 85–108. (CRC Press: Boca Raton, FL)

Bidwell SD, Woodrow IE, Batianoff GN, Sommer-Knusden J (2002) Hyperaccumulation of manganese in the rainforest tree Austromyrtus bidwillii (Myrtaceae) from Queensland, Australia. Functional Plant Biology 29, 899–905.
Crossref | GoogleScholarGoogle Scholar | open url image1

Bidwell SD, Crawford SA, Woodrow IE, Sommer-Knusden J, Marshall AT (2004) Sub-cellular localization of Ni in the hyperaccumulator Hybanthus floribundus (Lindley) F. Muell. Plant, Cell & Environment 27, 705–716.
Crossref | GoogleScholarGoogle Scholar | open url image1

Blamey FPC, Joyce DC, Edwards DG, Asher CJ (1986) Role of trichomes in sunflower tolerance to manganese toxicity. Plant and Soil 91, 171–180.
Crossref | GoogleScholarGoogle Scholar | open url image1

Broadhurst CL, Chaney RL, Angle JS, Maucel TK, Erbe EF, Murphy CA (2004) Simultaneous hyperaccumulation of nickel, manganese and calcium in Alyssum leaf trichomes. Environmental Science & Technology 38, 5797–5802.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Brooks RR (1998) ‘Plants that hyperaccumulate heavy metals.’ (CAB International: New York)

Daudin L, Khodja H, Gallien JP (2003) Development of “position-charge-time” tagged spectrometry for ion beam microanalysis. Nuclear Instruments & Methods in Physics Research. Section B, Beam Interactions with Materials and Atoms 210, 153–158.
Crossref | GoogleScholarGoogle Scholar | open url image1

Esau K (1965) ‘Plant Anatomy.’ (John Wiley & Sons: New York)

Fernando DR, Bakkaus EJ, Perrier N, Baker AJM, Woodrow IE, Batianoff GN, Collins RN (2006a) Manganese accumulation in the leaf mesophyll of four tree species: a PIXE/EDAX localization study. The New Phytologist 171, 751–758.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Fernando DR, Batianoff GN, Baker AJ, Woodrow IE (2006b) In vivo localisation of manganese in the hyperaccumulator Gossia bidwillii (Benth.) N. Snow & Guymer (Myrtaceae) by cryo-SEM/EDAX. Plant, Cell & Environment 29, 1012–1020.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Fernando DR, Baker AJM, Woodrow IE, Batianoff GN, Bakkaus EJ, Collins RN (2007a) Variability of Mn hyperaccumulation in the Australian rainforest tree Gossia bidwillii (Myrtaceae). Plant and Soil 293, 145–152.
Crossref | GoogleScholarGoogle Scholar | open url image1

Fernando DR, Woodrow IE, Jaffre T, Dumontet V, Marshall AT, Baker AJM (2007b) Foliar Mn accumulation by Maytenus fournieri (Celastraceae) in its native New Caledonian habitats: populational variation and localisation by X-ray microanalysis. The New Phytologist 177, 178–185.
PubMed |
open url image1

Foulds W (2003) Nutrient concentrations of foliage and soil in south-western Australia. The New Phytologist 125, 529–546. open url image1

Graham RD , Hannam RJ , Uren NC (1988) Manganese in Soils and Plants. In ‘International Symposium on Manganese in Soils and Plants, Glen Osmond, South Australia’. (Eds RD Graham, RJ Hannam, NC Uren) pp. 125–127. (Kluwer Academic Press: Dordrecht, The Netherlands)

Krämer U, Cotter-Howells JD, Charnock JM, Baker AJM, Smith JAC (1996) Free histidine as a metal chelator in plants that accumulate nickel. Nature 379, 635–638.
Crossref | GoogleScholarGoogle Scholar | open url image1

Krämer U, Grime GW, Smith JAC, Hawes CR, Baker AJM (1997) Micro-PIXE as a technique for studying nickel localization in leaves of the hyperaccumulator Alyssum lesbiacum. Nuclear Instruments and Methods in Physics Research B – Beam Interactions with Materials and Atoms 130, 346–350.
Crossref | GoogleScholarGoogle Scholar | open url image1

Küpper H, Lombi E, Zhao F, McGrath SP (2000) Cellular compartmentation of cadmium and zinc in relation to other elements in the hyperaccumulator Arabidopsis halleri. Planta 212, 75–84.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Küpper H, Lombi E, Zhao F, Wieshammer G, McGrath SP (2001) Cellular compartmentation of nickel in the hyperaccumulators Alyssum lesbiacum, Alyssum bertolonii and Thlaspi goesingense. Journal of Experimental Botany 52, 2291–2300.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Lombi E, Zhao FJ, Fuhrmann M, Ma LQ, McGrath SP (2002) Arsenic distribution and speciation in the fronds of the hyperaccumulator Pteris vittata. The New Phytologist 156, 195–203.
Crossref | GoogleScholarGoogle Scholar | open url image1

Macnair M (2003) The hyperaccumulation of metals by plants. Advances in Botanical Research 40, 63–105.
Crossref | GoogleScholarGoogle Scholar | open url image1

McGrath SP (2000) Phytoextraction for soil remediation. In ‘Plants that hyperaccumulate heavy metals’. (Ed. RR Brooks) pp. 261–287. (CAB International: New York)

McNear DH, Peltier E, Everhart J, Chaney RL, Sutton S, Newville M, Rivers M, Sparks DL (2005) Application of quantitative fluorescence and absorption-edge computed microtomography to image metal compartmentalization in Alyssum murale. Environmental Science & Technology 39, 2210–2218.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Memon AR, Yatazawa M (1980) Distribution of manganese in leaf tissues of manganese accumulator: Acanthopanax sciadophylliodes as revealed by electronprobe X-ray microanalyzer. Journal of Plant Nutrition 2, 457–476. open url image1

Memon AR, Chino M, Hara K, Yatazawa M (1981) Microdistribution of manganese in the leaf tissues of different plant species as revealed by X-ray microanalyzer. Physiologia Plantarum 53, 225–232.
Crossref | GoogleScholarGoogle Scholar | open url image1

Mesjasz-Przybylowicz J, Przybylowicz WJ (2002) Micro-PIXE in plant sciences: present status and perspectives. Nuclear Instruments & Methods in Physics Research. Section B, Beam Interactions with Materials and Atoms 189, 470–481.
Crossref | GoogleScholarGoogle Scholar | open url image1

Mesjasz-Przybylowicz J, Przybylowicz WJ, Pineda CA (2001) Nuclear microprobe studies of elemental distribution in apical leaves of the Ni hyperaccumulator Berkheya coddii. South African Journal of Science 97, 591–593. open url image1

Min Y, Boqing T, Meizhen T, Aoyama I (2007) Accumulation and uptake of manganese in a hyperaccumulator Phytolacca americana. Minerals Engineering 20, 188–190.
Crossref | GoogleScholarGoogle Scholar | open url image1

Pollard AJ, Powell KD, Harper FA, Smith JA (2002) The genetic basis of metal hyperaccumulation in plants. Critical Reviews in Plant Sciences 21, 539–566.
Crossref | GoogleScholarGoogle Scholar | open url image1

Reeves RD , Baker AJM (2000) Metal-accumulating plants. In ‘Phytoremediation of toxic metals: using plants to clean up the environment’. (Eds I Raskin, BD Ensley) pp. 193–221. (John Wiley and Sons: New York)

Robinson BH, Lombi E, Zhao FJ, McGrath SP (2003) Uptake and distribution of nickel and other metals in the hyperaccumulator Berkheya coddii. The New Phytologist 158, 279–285.
Crossref | GoogleScholarGoogle Scholar | open url image1

Vázquez MD, Barceló J, Poschenrieder C, Mádico J, Hatton P, Baker AJM, Cope GH (1992) Localisation of zinc and cadmium in Thlaspi caerulescins (Brassicaceae), a metallophyte that can hyperaccumulate both metals. Journal of Plant Physiology 140, 350–355. open url image1

Xu X, Shi J, Chen Y, Chen X, Wang H, Perera A (2006a) Distribution and mobility of manganese in the hyperaccumulator plant Phytolacca acinosa Roxb. (Phytolaccaceae). Plant and Soil 285, 323–331.
Crossref | GoogleScholarGoogle Scholar | open url image1

Xu XH, Shi JY, Chen YX, Xue SG, Wu WB, Huang Y (2006b) An investigation of cellular manganese in hyperaccumulator plant Phytolacca acinosa Roxb. using SRXRF analysis. Journal of Environmental Sciences (China) 18, 746–751.
PubMed |
open url image1

Xue SG, Chen YX, Reeves RD, Baker AJM, Lin Q, Fernando DR (2004) Manganese uptake and accumulation by the hyperaccumulator plant Phytolacca acinosa Roxb. (Phytolaccaceae). Environmental Pollution (Barking, Essex: 1987) 131, 393–399.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Xue SG, Chen YX, Baker AJM (2005) Manganese uptake and accumulation by two populations of Phytolacca acinosa Roxb. (Phytolaccaceae). Water, Air, and Soil Pollution 160, 3–14.
Crossref | GoogleScholarGoogle Scholar | open url image1