Skip to main content
SpringerLink
Log in

Mechanisms of trichome-specific Mn accumulation and toxicity in the Ni hyperaccumulator Alyssum murale

  • Regular Article
  • Published:
Plant and Soil Aims and scope Submit manuscript

Abstract

Background and aims

Mechanisms of Mn accumulation and toxicity in and around trichomes on the Ni hyperaccumulator Alyssum murale were investigated.

Methods

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.

Results

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.

Conclusions

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+.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9

Similar content being viewed by others

References

  • Ågren J, Schemske DW (1994) Evolution of trichome number in a naturalized population of Brassica rapa. American Naturalist 143:1–13

    Article  Google Scholar 

  • Beilstein MA, Al-Shehbaz IA, Kellogg EA (2006) Brassicaceae phylogeny and trichome evolution. American Journal of Botany 93(4):607–619

    Article  PubMed  CAS  Google Scholar 

  • Beilstein MA, Al-Shehbaz IA, Mathews S, Kellogg EA (2008) Brassicaceae phylogeny inferred from phytochome A and NDHF sequence data: tribes and trichomes revisited. American Journal of Botany 95(10):1307–1327

    Article  PubMed  CAS  Google Scholar 

  • 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):3–14

    Google Scholar 

  • Barnese K, Gralla EB, Valentine JS, Cabelli DE (2012) Biologically relevant mechanisms for catalytic superoxide removal by simple manganese compounds. PNAS 109(18):6892–6897

    Article  PubMed Central  PubMed  Google Scholar 

  • Benz BW, Martin CE (2006) Foliar trichomes, boundary layers, and gas exchange in the species of epiphytic Tillandsia (Bromeliaceae). J Plant Physiol 163:648–656

    Article  PubMed  CAS  Google Scholar 

  • Blamey FPC, Joyce DC, Edwards DG, Asher CJ (1986) Role of trichomes in sunflower tolerance to manganese toxicity. Plant and Soil 91(2):171–180

    Article  CAS  Google 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 158

    Google Scholar 

  • Broadhurst CL, Chaney RL, Angle JS, Erbe EF, Maugel TK (2004a) Nickel localization and response to increasing Ni soil levels in leaves of the Ni hyperaccumulator Alyssum murale. Plant and Soil 265(1–2):225–242

    Article  CAS  Google Scholar 

  • Broadhurst CL, Chaney RL, Angle JS, Maugel TK, Erbe EF, Murphy CA (2004b) Simultaneous hyperaccumulation of nickel, manganese, and calcium in Alyssum leaf trichomes. Environmental Science & Technology 38(21):5797–5802

    Article  CAS  Google Scholar 

  • Broadhurst LC, Tappero R, Maugel T, Erbe E, Sparks D, Chaney R (2009) Interaction of nickel and manganese in accumulation and localization in leaves of the Ni hyperaccumulators Alyssum murale and Alyssum corsicum. Plant and Soil 314(1–2):35–48

    Article  CAS  Google Scholar 

  • Braodhurst LC, Bauchan GR, Murphy CA, Tang Y-T, Pooley C, Davis AP, Chaney RL (2013) Accumulation of zinc and cadmium and localization of zinc in Picris divaricata Vant. Environmental and Experimental Botany 87:1–9

    Article  CAS  Google Scholar 

  • Chaney RL (1988) Recent progress and needed research in plant Fe nutrition. Journal of Plant Nutrition 11(6–11):1589–1603

    Article  Google Scholar 

  • Ducic T, Thieme J, Polle A (2012) Phosphorus compartmentlazliation on the cellular level of Douglas Fir root as affected by Mn toxicity: a synchtrotron-based FTIR approach. Spectroscopy 27(5–6):265–272

    Article  CAS  Google Scholar 

  • Ducic T, Polle A (2007) Manangese toxicity in two varieties of Douglas fir (Pseudotsuga menziesii var. viridis and glauca) seedlings as afected by phosphours supply. Functional Plant Biology 34:31–40

    Article  CAS  Google Scholar 

  • Choi YE, Harada E, Kim GH, Yoon ES, Sano H (2004) Distribution of elements on tobacco trichomes and leaves under cadmium and sodium stresses. Journal of Plant Biology 47(2):75–82

    Article  CAS  Google Scholar 

  • Choi YE, Harada E, Wada M, Tsuboi H, Morita Y, Kusano T, Sano H (2001) Detoxification of cadmium in tobacco plants: formation and active excretion of crystals containing cadmium and calcium through trichomes. Planta 213(1):45–50

    Article  PubMed  CAS  Google Scholar 

  • Choinski JS, Wise RR (1999) Leaf growth and development in relation to gas exchange in Quercus marilandica Muenchh. J Plant Physiol 154:302–309

    Article  CAS  Google Scholar 

  • De Silva DLR, Hetherington AM, Mansfield TA (1996) Where does all the calcium go? Evidence of an important regulatory role for trichomes in two calcicoles. Plant, Cell and Environment 19:880–886

    Article  Google Scholar 

  • Dou C, Fu X, Chen X, Shi J, Chen Y (2009) Accumulation and interaction of calcium and manganese in Phytolacca americana. Plant Science 177(6):601–606

    Article  CAS  Google 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 113–132

    Google Scholar 

  • El-Jaoual T, Cox DA (1998) Manganese toxicity in plants. Journal of Plant Nutrition 21(2):353–386

    Article  CAS  Google Scholar 

  • Fecht-Christoffers MM, Braun HP, Lemaitre-Guillier C, VanDorsselaer A, Horst WJ (2003) Effect of manganese toxicity on the proteome of the leaf apoplast in cowpea. Plant Physiology 133(4):1935–1946

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Fecht-Christoffers MM, Fuhrs H, Braun HP, Horst WJ (2006) The role of hydrogen peroxide-producing and hydrogen peroxide-consuming peroxidases in the leaf apoplast of cowpea in manganese tolerance. Plant Physiology 140(4):1451–1463

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Fecht-Christoffers MM, Horst WJ (2005) Does apoplastic ascorbic acid enhance manganese tolerance of Vigna unguiculata and Phaseolus vulgaris? Journal of Plant Nutrition and Soil Science-Zeitschrift Fur Pflanzenernahrung Und Bodenkunde 168(4):590–599

    Article  CAS  Google Scholar 

  • Fernando DR, Mizuno T, Woodrow IE, Baker AJM, Collins RN (2010) Characterization of foliar manganese (Mn) in Mn (hyper)accumulators using X-ray absorption spectroscopy. New Phytologist 188(4):1014–1027

    Article  PubMed  CAS  Google Scholar 

  • Fernando DR, Mizuno T, Woodrow IE, Baker AJM, Marshall AT (2012) Plant homeostasis of foliar manganese sinks: Specific variation in hyperaccumulators. Planta 236(5):1459–1470

    Article  PubMed  CAS  Google Scholar 

  • Foreman J, Demidchik V, Bothwell JHF, Mylona P, Miedema H, Torres MA, Linstead P, Costa S, Brownlee C, Jones JDG, Davies JM, Dolan L (2003) Reactive oxygen species produced by NADPH oxidase regulate plant cell growth. Nature 422(6930):442–446

    Article  PubMed  CAS  Google Scholar 

  • Freeman JL, Lindblom SD, Quinn CF, Fakra S, Marcus MA, Pilon-Smits EAH (2007) Selenium accumulation protects plants from herbivory by orthoptera due to toxicity and deterrence. New Phytologist 175:490–500

    Article  PubMed  CAS  Google Scholar 

  • Galvez L, Clark RB, Gourley LM, Maranville JW (1989) Effects of silicon on mineral-composition of sorghum grown with excess manganese. Journal of Plant Nutrition 12(5):547–561

    Article  CAS  Google Scholar 

  • Ghasemi R, Ghaderian SM, Kramer U (2009) Accumulation of nickel in trichomes of a nickel hyperaccumulator plant, Alyssum inflatum. Northeastern Naturalist 16:81–92

    Article  Google Scholar 

  • Hansard SP, Easter HD, Voelker BM (2011) Rapid reaction of nanomolar Mn(II) with superoxide radical in seawater and simulated freshwater. Environmental Science & Technology 45(7):2811–2817

    Article  CAS  Google 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 109:12621–12625

    Google Scholar 

  • Harada E, Choi YE (2008) Investigation of metal exudates from tobacco glandular trichomes under heavy metal stresses using a variable pressure scanning electron microscopy system. Plant Biotechnology 25(4):407–411

    Article  CAS  Google Scholar 

  • Herndon EM, Jin LX, Brantley SL (2011) Soils reveal widespread manganese enrichment from industrial inputs. Environmental Science & Technology 45(1):241–247

    Article  CAS  Google Scholar 

  • Horiguchi T (1987) Mechanism of manganese toxicity and tolerance of plants 2. deposition of oxidized manganese in plant-tissues. Soil Science and Plant Nutrition 33(4):595–606

    Article  CAS  Google 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 175–188

  • 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 162:263–274

    Google Scholar 

  • Isaure M, Fayard B, Sarret G, Pairis S, Bourguignon J (2006) Localization and chemical forms of cadmium in plant samples by combining analytical electron microscopy and X-ray spectromicroscopy. Spectrochimica Acta Part B 61:1242–1252

    Article  CAS  Google Scholar 

  • Isaure MP, Sarret G, Harada E, Choi YE, Marcus MA, Fakra SC, Geoffroy N, Pairis S, Susini J, Clemens S, Manceau A (2010) Calcium promotes cadmium elimination as vaterite grains by tobacco trichomes. Geochimica Et Cosmochimica Acta 74(20):5817–5834

    Article  CAS  Google 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 23–64

    Google Scholar 

  • Kamiya T, Akahori T, Maeshima M (2005) Expression profile of the genes for rice cation/H + exchanger family and functional analysis in yeast. Plant and Cell Physiology 46(10):1735–1740

    Article  PubMed  CAS  Google 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–S201

    Google Scholar 

  • Karban R, Baldwin IT (1997) Induced responses to herbivory. The University of Chicago Press, Chicago, p 319

    Book  Google 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):346–350

    Article  Google Scholar 

  • Kukier U, Peters CA, Chaney RL, Angle JS, Roseberg RJ (2004) The effect of pH on metal accumulation in two Alyssum species. Journal of Environmental Quality 33(6):2090–2102

    Article  PubMed  CAS  Google Scholar 

  • Küpper H, Lombi E, Zhao FJ, McGrath SP (2000) Cellular compartmentation of cadmium and zinc in relation to other elements in the hyperaccumulator Arabidopsis halleri. Planta 212(1):75–84

    Article  PubMed  Google Scholar 

  • Küpper H, Lombi E, Zhao FJ, Wieshammer G, McGrath SP (2001) Cellular compartmentation of nickel in the hyperaccumulators Alyssum lesbiacum, Alyssum bertolonii and Thlaspi goesingense. Journal of Experimental Botany 52(365):2291–2300

    Article  PubMed  Google Scholar 

  • Levin DA (1973) The role of trichomes in plant defence. Quarterly Review of Biology 48:3–15

    Article  Google Scholar 

  • Macnicol RD, Beckett PHT (1985) Critical tissue concentrations of potentially toxic elements. Plant and Soil 85:107–129

    Article  CAS  Google Scholar 

  • Marschner P (2012) Marschner’s mineral nutrition of higher plants. Elsevier, London

    Google Scholar 

  • Marcus MA, MacDowell AA, Celestre R, Manceau A, Millter T, Pdmore HA, Sublett RE (2004) Beamline 10.3.2 at ALS: A hard X-ray microprobe for environemtnal and materials sciences. J Synchrotron Radiat 1(11):239–247

    Article  CAS  Google 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):2210–2218

    Article  CAS  Google Scholar 

  • Pittman JK (2005) Managing the manganese: Molecular mechanisms of manganese transport and homeostasis. New Phytologist 167(3):733–742

    Article  PubMed  CAS  Google Scholar 

  • Pittman JK, Shigaki T, Marshall JL, Morris JL, Cheng NH, Hirschi KD (2004) Functional and regulatory analysis of the Arabidopsis thaliana CAX2 cation transporter. Plant Molecular Biology 56(6):959–971

    Article  PubMed  CAS  Google 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–S272

    Google Scholar 

  • Pleith C, Vollbehr S (2012) Calcium promotes actiivty and confers heat stability on plant peroxidases. Plant Signal Bahav 7(6): On-line first.

  • Psaras GK, Constantinidis T, Cotsopoulos B, Manetas Y (2000) Relative abundance of nickel in the leaf epidermis of eight hyperaccumulators: Evidence that the metal is excluded from both guard cells and trichomes. Annals of Botany 86(1):73–78

    Article  CAS  Google Scholar 

  • Quinn CF, Prins CN, Gross AM, Hantzis L, Reynolds RJB, Freeman JL, Yang SI, Covey PA, Bañuelos GS, Pickering IJ, Fakra SF, Marcus MA, Arathi HS, Pilon-Smits EAH (2011) Selenium accumulation in flowers and its effects on pollination. New Phytologist 192:727–737

    Article  PubMed  CAS  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 193–229

    Google Scholar 

  • Sakihama Y, Cohen MF, Grace SC, Yamasaki H (2002) Plant phenolic antioxidant and prooxidant activities: phenolics-induced oxidative damage mediated by metals in plants. Toxicology 177(1):67–80

    Article  PubMed  CAS  Google Scholar 

  • Sarret G, Harada E, Choi YE, Isaure MP, Geoffroy N, Fakra S, Marcus MA, Birschwilks M, Clemens S, Manceau A (2006) Trichomes of tobacco excrete zinc as zinc-substituted calcium carbonate and other zinc-containing compounds. Plant Physiology 141(3):1021–1034

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Sarret G, Isaure MP, Marcus MA, Harada E, Choi YE, Pairis S, Fakra S, Manceau A (2007) Chemical forms of calcium in Ca, Zn- and Ca, Cd-containing grains excreted by tobacco trichomes. Canadian Journal of Chemistry-Revue Canadienne De Chimie 85(10):738–746

    Article  CAS  Google Scholar 

  • Sarret G, Saumitou-Laprade P, Bert V, Proux O, Hazemann JL, Traverse AS, Marcus MA, Manceau A (2002) Forms of zinc accumulated in the hyperaccumulator Arabidopsis halleri. Plant Physiology 130(4):1815–1826

    Article  PubMed Central  PubMed  CAS  Google 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):581–595

    Article  PubMed  CAS  Google Scholar 

  • Schaaf G, Catoni E, Fitz M, Schwacke R, Schneider A, von Wiren N, Frommer WB (2002) A putative role for the vacuolar calcium/manganese proton antiporter AtCAX2 in heavy metal detoxification. Plant Biology 4(5):612–618

    Article  CAS  Google Scholar 

  • Southwood SR (1986) Plant surfaces and insects—an overview. In: Juniper B, Southwood SR (eds) Insects and the plant surface. Arnold, London, pp 1–22

    Google Scholar 

  • Tappero RV (2008) Microspectroscopic study of cobalt speciation and localization in nickel hyperaccumulator Alyssum murale. Ph.D. Dissertation, University of Delaware, Newark

    Google Scholar 

  • Traw BM, Dawson TE (2002) Reduced performance of two specialist herbivores (Lepidoptera: Pieridae, Coleoptera: Chrysomelidae) on new leaves of damaged black mustard plants. Environmental Entomology 31:714–722

    Article  Google 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):1855–1866

    CAS  Google Scholar 

  • Wagner G, Wang E, Shepherd RW (2004) New approaches for studying and exploiting an old protuberance, the plant trichome. Annals of Botany 93:3–11

    Article  PubMed  CAS  Google Scholar 

  • Webb MA (2007) Calcium biominerals in trichomes of the Brassicaceae. Plant Biology Meetings. July 7–12 Chicago, Illinois

  • Werker E (2000) Trichome diversity and development. Advances in Botanical Research Incorporating Advances in Plant Pathology 31:1–35

    Google Scholar 

  • Wissemeier AH, Horst WJ (1992) Effect of light-intensity on manganese toxicity symptoms and callose formation in cowpea (Vigna-Unguiculata (L) Walp). Plant and Soil 143(2):299–309

    Article  CAS  Google Scholar 

Download references

Acknowledgments

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.

Author information

Authors and Affiliations

  1. Rhizosphere Science Laboratory, Department of Plant and Soil Sciences, N122S Agricultural Sciences North Building, University of Kentucky, 1100 Nicholasville Road, Lexington, KY, 40546-0091, USA

    David H. McNear Jr. & Joseph V. Kupper

Authors
  1. David H. McNear Jr.
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Joseph V. Kupper
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to David H. McNear Jr..

Additional information

Responsible Editor: Fangjie Zhao.

Electronic supplementary material

Below is the link to the electronic supplementary material.

ESM 1

(DOCX 170 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

McNear, D.H., Kupper, J.V. Mechanisms of trichome-specific Mn accumulation and toxicity in the Ni hyperaccumulator Alyssum murale . Plant Soil 377, 407–422 (2014). https://doi.org/10.1007/s11104-013-2003-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11104-013-2003-7

Keywords

Search

Navigation