Mechanisms of trichome-specific Mn accumulation and toxicity in the Ni hyperaccumulator Alyssum murale
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Background and aims
Mechanisms of Mn accumulation and toxicity in and around trichomes on the Ni hyperaccumulator Alyssum murale were investigated.
Plants were grown aeroponically with variable amounts of Mn and Ni. Total metals were determined and electron microprobe analysis (EMPA) and synchrotron-based micro x-ray fluorescence (μ-SXRF) spectroscopy were used to evaluate metal distribution. Synchrotron techniques (μ-XANES, μ-EXAFS) along with infrared spectroscopy (DRIFT) were used to determine Mn speciation.
At lower Mn concentrations or when grown together with Ni, Mn is confined to the trichome basal compartment in the +2 oxidation state in a complex with phosphate. At tissue concentrations >1,150 μg g−1 Mn-rich lesions develop around some trichomes in which greater amounts of Mn 3+ is found.
Mn is preferentially stored in trichomes on the plant surface which at higher concentrations enters the cell wall or apoplastic space of neighboring cells resulting in the formation of brown reaction products and oxidized Mn species. We propose a mechanism by which lesion formation and oxidized Mn species around some trichomes is possibly due to induction of the peroxidase system by excess Mn, triggering the accumulation of toxic phenoxy radicals and Mn3+.
KeywordsManganese (Mn) Alyssum murale Trichome Hyperaccumulation Nickel (Ni) Synchrotron x-ray absorption fine structure spectroscopy (XAFS)
The authors would like to thank Dr. Jason Unrine for ICP-MS analysis of total metal concentrations, the environmental soil chemistry research group of Dr. Donald Sparks for the Mn standard spectra and Matthew Marcus at beamline 10.3.2 for advice on Mn fitting. The Advanced Light Source is supported by the Director, Office of Science, Office of Basic Energy Sciences, of the U.S. Department of Energy under Contract No. DE-AC02-05CH11231.
- Bani A, Pavlova D, Echevarria G, Mullaj A, Reeves RD, Morel JL, Sulce S (2010) Nickel hyperaccumulation by species of alyssum and Thlaspi (Brassicaceae) from the ultramafic soils of the Balkans. Botanica Servica 34(1):3–14Google Scholar
- Bray EA, Bailey SJ, Weretilnyk E (2000) Responses to abiotic stresses. In: Gruissem W, Buchannan B, Jones R (eds) Biochemistry and molecular biology of plants. American Society of Plant Biologists, Rockville, p 158Google Scholar
- Ehrlinger J (1984) Ecology and physiology of leaf pubescence in North American desert plants. In: Rodriguez E, Healey PL, Mehta I (eds) Biology and chemistry of plant trichomes. Plenum Press, New York, pp 113–132Google Scholar
- Hansel CM, Zeiner CA, Santelli CM, Webb SM (2012) Mn (II) oxidation by an ascomycete fungus is linked to superoxide production during asexual reproduction. Proc Natl Acad Sci 109:12621–12625Google Scholar
- Horst WJ (1988) The physiology of manganese toxicity. In: Graham RD, Hannam RJ, Uren NJ (eds) Manganese in soil and plants. Kluwer Academic Publishers, Dordrecht, pp 175–188Google Scholar
- Horst W, Fecht M, Naumann A, Wissemeier A, Maier P (1999) Physiology of manganese toxicity and tolerance in Vigna unguiculata (L.) Walp. J Plant Nutr Soil Sci 162:263–274Google Scholar
- Jeffree CE (1986) The cuticle, epicuticular waxes and trichomes of plants, with reference to their structure, function and evolution. In: Juniper B, Southwood SR (eds) Insects and the plant surface. Arnold, London, pp 23–64Google Scholar
- Kamiya T, Akahori T, Maeshima M (2006) Expression profile of the genes for rice cation/H + exchanger family and functional analysis in yeast. Plant and Cell Physiology 47:S201–S201Google Scholar
- Kramer U, Grime GW, Smith JAC, Hawes CR, Baker AJM (1997) Micro-PIXE as a technique for studying nickel localization in leaves of the hyperaccumulator plant Alyssum lesbiacum. Nuclear Instruments & Methods in Physics Research Section B-Beam Interactions with Materials and Atoms 130(1–4):346–350CrossRefGoogle Scholar
- Marschner P (2012) Marschner’s mineral nutrition of higher plants. Elsevier, LondonGoogle Scholar
- 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(7):2210–2218CrossRefGoogle Scholar
- Pittman JK, Shigaki T, Morris JL, Hirschi KD (2005) Functional analysis of CAX2, an Arabidopsis cation/proton transporter with broad specificity. Comparative Biochemistry and Physiology a-Molecular & Integrative Physiology 141(3):S272–S272Google Scholar
- Pleith C, Vollbehr S (2012) Calcium promotes actiivty and confers heat stability on plant peroxidases. Plant Signal Bahav 7(6): On-line first.Google Scholar
- Reeves RD, Baker AJ (2000) Metal-accumulating plants. In: Raskin I, Ensley BD (eds) Phytoremediation of toxic metals: Using plants to clean up the environment. Wiley, New York, pp 193–229Google Scholar
- Sarret G, Willems G, Isaure MP, Marcus MA, Fakra SC, Frerot H, Pairis S, Geoffroy N, Manceau A, Saumitou-Laprade P (2009) Zinc distribution and speciation in Arabidopsis halleri x Arabidopsis lyrata progenies presenting various zinc accumulation capacities. New Phytologist 184(3):581–595PubMedCrossRefGoogle Scholar
- Southwood SR (1986) Plant surfaces and insects—an overview. In: Juniper B, Southwood SR (eds) Insects and the plant surface. Arnold, London, pp 1–22Google Scholar
- Tappero RV (2008) Microspectroscopic study of cobalt speciation and localization in nickel hyperaccumulator Alyssum murale. Ph.D. Dissertation, University of Delaware, NewarkGoogle Scholar
- Tumi AF, Mihailović N, Gajić BA, Niketić M, Tomović G (2012) Comparative study of hyperaccumulation of nickel by Alyssum murale s.l. populations from the ultramafics of Serbia. Pol J Environ Stud 21(6):1855–1866Google Scholar
- Webb MA (2007) Calcium biominerals in trichomes of the Brassicaceae. Plant Biology Meetings. July 7–12 Chicago, IllinoisGoogle Scholar
- Werker E (2000) Trichome diversity and development. Advances in Botanical Research Incorporating Advances in Plant Pathology 31:1–35Google Scholar