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Arbuscular Mycorrhiza, Heavy Metal,and Salt Tolerance

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Soil Heavy Metals

Part of the book series: Soil Biology ((SOILBIOL,volume 19))

Abstract

More than 80% of all higher plants are colonized by arbuscular mycorrhizal fungi (AMF) under diverse stress conditions. The extent of mycorrhizal colonization in plants that grow in heavy metal soils (metallophytes) or salt marshes (halophytes) is species dependent. Specially adapted AMF have repeatedly been reported to alleviate the toxicity of heavy metals to plants. Factors governing the heavy metal tolerance conferred by AMF have been elucidated. Compared to this, the current state of knowledge regarding AMF and salt tolerance appears to be underdeveloped, despite the enormous potential applications of this field. This article summarizes heavy metal and salt toxicity to plants and the potential impacts of AMF in both of these forms of toxicity. Currently, the main constraint on applications of AMF is the inability to grow them without the need for a symbiotic partner.

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References

  • Anderson CWN, Brooks RR, Chiarucci A, La Coste CJ, Leblanc M, Robinson BH, Simcock R, Stewart RB (1999) Phytomining for nickel, thalium and gold. J Geochemical Exploration 67:407–415

    Article  CAS  Google Scholar 

  • Apse MP, Blumwald E (2007) Na+ transport in plants. FEBS Lett 581:247–254

    Article  Google Scholar 

  • Bécard G, Fortin JA (1988) Early events of vesicular-arbuscular mycorrhiza formation on Ri T-DNA-transformed roots. New Phytol 108:211–218

    Article  Google Scholar 

  • Bennett LE, Burkhead JL, Hale KL, Terry N, Pilon M, Pilon-Smits EAH (2003) Analysis of transgenic Indian Mustard plants for phytoremediation of metal-contaminated tailings. J Environ Qual 32:432–440

    Article  PubMed  CAS  Google Scholar 

  • Boominathan R, Saha-Chaudhury NM, Sahajwall V, Doran PM (2004) Production of nickel bio-ore from hyperaccumulator plant biomass: applications in phytomining. Biotechnol Bioeng 86:243–250

    Article  PubMed  CAS  Google Scholar 

  • Börstler B, Renker C, Kahmen A, Buscot F (2006) Species composition of arbuscular mycorrhizal fungi in two mountain meadows with differing management types and levels of plant biodiversity. Biol Fertil Soils 42:286–298

    Article  Google Scholar 

  • Brewer EP, Saunders JA, Angle JS, Chaney RL, McIntosh MS (1999) Somatic hybridization between the zinc accumulator Thlaspi caerulenscens and Brassica napus. Theor Appl Genet 99:761–771

    Article  CAS  Google Scholar 

  • Brooks RR (1998) Plants that hyperaccumulate heavy metals. CABI Publishing, Wallingford

    Google Scholar 

  • Brooks RR, Yang X-H (1984) Elemental levels and relationships in the endemic serpentine flora of the Great Dyke, Zimbabwe, and their significance as controlling factors for the flora. Taxon 33:392–399

    Article  Google Scholar 

  • Carvalho LM, Caçador I, Martins-Loução MA (2001) Temporal and spatial variation of arbuscular mycorrhizas in salt marsh plants of the Tagus estuary (Portugal). Mycorrhiza 11:303–309

    Article  Google Scholar 

  • Carvalho LM, Correia PM, Martins- Loução MA (2004) Arbuscular mycorrhizal fungal propagules in a salt marsh. Mycorrhiza 14:165–170

    Article  PubMed  Google Scholar 

  • Dahmani-Muller H, van Ort F, Gelie B, Balabane M (2000) Strategies of heavy metal uptake by three plant species growing near a metal smelter. Environmental Pollution 109:231–238

    Article  PubMed  CAS  Google Scholar 

  • De Mars BG, Boerner REJ (1996) Vesicular arbuscular mycorrhizal development in the Brassicaceae in relation to plant life span. Flora 191:179–189

    Google Scholar 

  • Elstner EF (1990) Der Sauerstoff, Biochemie, Biologie. Medizin, vol. BI- Wissenschaftsverlag, Mannheim, Wien Zürich

    Google Scholar 

  • Ernst WHO (2005) Phytoextraction of mine wastes-options and impossibilities. Chemie der Erde 65:29–42

    Article  CAS  Google Scholar 

  • Ernst WHO, Krauss GJ, Verkleij JAC, Wesenberg D (2008) Interaction of heavy metals with sulphur metabolism in angiosperms from an ecological point of view. Plant Cell Environ 31:123–143

    PubMed  CAS  Google Scholar 

  • Füzy A, Biro B, Toth T, Hildebrandt U, Bothe H (2008) Drought, but not salinity determines the apparent effectiveness of halophytes colonized by arbuscular mycorrhizal fungi. J Plant Physiology 165:1181–1192

    Google Scholar 

  • Gonzales-Guerrero M, Azcon-Aguilar C, Mooney M, Valderas A, MacDarmid CW, Eide DJ, Ferrol N (2005) Characterization of a Glomus intraradices gene encoding a putative Zn transporter of the cation diffusion facilitator family. Fungal Genet Biol 42:130–140

    Article  Google Scholar 

  • Gonzales-Guerrero M, Cano C, Azcon-Aguilar C, Ferrol N (2007) GintMT1 encodes a functional metallothionein in Glomus intraradices that responds to oxidative stress. Mycorrhiza 17:327–335

    Article  Google Scholar 

  • Hall JL (2002) Cellular mechanisms for heavy metal detoxification and tolerance. J Exper Botany 53:1–11

    Article  CAS  Google Scholar 

  • Hildebrandt U, Kaldorf M, Bothe H (1999) The zinc violet and its colonisation by arbuscular mycorrhizal fungi. J Plant Physiol 154:709–717

    CAS  Google Scholar 

  • Hildebrandt U, Janetta K, Ouziad F, Renne B, Nawrath K, Bothe H (2001) Arbuscular mycorrhizal colonization of halophytes in Central European salt marshes. Mycorrhiza 10:175–183

    Article  CAS  Google Scholar 

  • Hildebrandt U, Hoef-Emden K, Backhausen S, Bothe H, Bozek M, Siuta A, Kuta E (2006a) The rare endemic zinc violets of Central Europe originate from Viola lutea Huds. Plant Syst Evol 257:205–222

    Article  Google Scholar 

  • Hildebrandt U, Ouziad F, Marner FJ, Bothe H (2006b) The bacterium Paenibacillus validus stimulates growth of the arbuscular mycorrhizal fungus Glomus intraradices up to the formation of fertile spores. FEMS Microbiol Lett 254:258–267

    Article  PubMed  CAS  Google Scholar 

  • Hildebrandt U, Regvar M, Bothe H (2007) Arbuscular mycorrhiza and heavy metal tolerance. Phytochemistry 68:139–146

    Article  PubMed  CAS  Google Scholar 

  • Jeffries P, Gianinazzi S, Perotto S, Turnau K, Barea JM (2003) The contribution of arbuscular mycorrhizal fungi in sustainable maintenance of plant health and soil fertility. Biol Fert Soils 37:1–16

    Google Scholar 

  • Jentschke G, Godbold DL (2000) Metal toxicity and ectomycorrhizas. Physiol Plant 109:107–116

    Article  CAS  Google Scholar 

  • Juniper S, Abbott LK (1993) Vesicular-arbuscular mycorrhizas and soil salinity. Mycorrhiza 4:45–47

    Article  Google Scholar 

  • Juniper S, Abbott LK (2006) Soil salinity delays germination and limits growth of hyphae from propagules of arbuscular mycorrhizal fungi. Mycorrhiza 16:371–379

    Article  PubMed  CAS  Google Scholar 

  • Kaldorf MO, Kuhn AJ, Schröder WH, Hildebrandt U, Bothe H (1999) Selective element deposits in maize colonized by a heavy metal tolerance conferring arbuscular mycorrhizal fungus. J Plant Physiol 154:718–728

    CAS  Google Scholar 

  • Klingner A, Bothe H, Wray V, Marner FJ (1995) Identification of a yellow pigment formed in maize roots upon mycorrhizal colonization. Phytochemistry 38:53–55

    Article  CAS  Google Scholar 

  • Landwehr M, Hildebrandt U, Wilde P, Nawrath K, Tóth T, Biro B, Bothe H (2002) The arbuscular mycorrhizal fungus Glomus geosporum in European saline, sodic and gypsum soils. Mycorrhiza 12:199–211

    Article  PubMed  CAS  Google Scholar 

  • Lanfranco L, Bolchi A, Ros EC, Ottonello S, Bonfante P (2002) Differential expression of a metallothionein gene during the presymbiotic versus the symbiotic phase of an arbuscular mycorrhizal fungus. Plant Physiol 130:58–67

    Article  PubMed  CAS  Google Scholar 

  • Leyval C, Turnau K, Haselwandter K (1997) The effect of heavy metal pollution on mycorrhizal colonization and function, physiological, ecological and applied aspects. Mycorrhiza 7:159–163

    Article  Google Scholar 

  • Ma LQ, KK M, Tu C, Zhang W, Cai Y, Kennelly ED (2001) A fern that hyperaccumulates arsenic. Nature 409:579–579

    Article  PubMed  CAS  Google Scholar 

  • Marschner H (1995) Mineral nutrition of higher plants, 2nd edn. Academic Press, London

    Google Scholar 

  • Megharaj M, Ragusa SR, Naidu R (2002) Metal-algae interactions: implications of bioavailability. In: Naidu R et al (eds) Bioavailability, toxicity and risk relationships in ecosystems. Science Publishers, Inc., Enfield, USA

    Google Scholar 

  • Nauenburg JD (1986) Untersuchungen zur Variabilität, Ökologie und Systematik der Viola tricolor -Gruppe in Mitteleuropa, Thesis, The University of Göttingen, Germany, p. 126

    Google Scholar 

  • Orłowska E, Zubek S, Jurkiewicz A, Szarek-Lukaszewska G, Turnau K (2002) Influence of restoration on arbuscular mycorrhiza of Biscutella laevigata L. (Brassicaceae) and Plantago lanceolata L. (Plantaginaceae) from calamine spoil mounds. Mycorrhiza 12:153–160

    Article  PubMed  Google Scholar 

  • Orłowska E, Ryszka P, Jurkiewicz A, Turnau K (2005) Effectiveness of arbuscularmycorrhizal fungal (AMF) strains in colonisation of plants involved in phytostabilization of zinc wastes. Geoderma 129:92–98

    Article  Google Scholar 

  • Orłowska E, Mesjasz-Przybylowicz J, Przybylowicz W, Turnau K (2008) Nuclear microprobe studies of elemental distribution in mycorrhizal and nonmycorrhizal roots of Ni-hyperaccumulator Berkheya coddii. X-Ray Spectrom 37:129–132

    Article  Google Scholar 

  • Ouziad F, Hildebrandt U, Schmelzer E, Bothe H (2005) Differential gene expressions in arbuscular mycorrhizal-colonized tomato grown under heavy metal stress. J Plant Physiol 162:634–649

    Article  PubMed  CAS  Google Scholar 

  • Ouziad F, Wilde P, Schmelzer E, Hildebrandt U, Bothe H (2006) Analysis of expression of aquaporins and Na+/H+ transporters in tomato colonized by arbuscular mycorrhizal fungi and affected by salt stress. Envir Exp Bot 57:177–186

    Article  CAS  Google Scholar 

  • Patzke W, Brown G (1990) Festua aequisgranensis sp. nova ein neuer Vertreter der Kollektivart Festuca ovina L. Decheniana 143:194–195

    Google Scholar 

  • Pongrac P, Vogel-Mikuš K, Kump P, Necemer M, Tolra R, Poschenrieder C, Barcelo J, Regvar M (2007) Changes in elemental uptake and arbuscular mycorrhizal colonization during the life cycle of Thlaspi praecox Wulfen. Chemosphere 69:1602–1609

    Article  PubMed  CAS  Google Scholar 

  • Prasad MNV, de Oliveira-Freitas HM (1999) Feasible biotechnological and bioremediation strategies for serpentine soils and mine spoils. Electron J Biotechnol 15th April 1999 http://www.ejbiotechnology.info/content/vol2/issue1/index.html

  • Prasad MNV, Hagemeyer JE (1999) Heavy metal stress in plants-from molecules to ecosystems. New York, Berlin

    Google Scholar 

  • Redecker D, Kodner R, Graham LE (2000) Glomalean fungi from the Ordovician. Science 289:1920–1921

    Article  PubMed  CAS  Google Scholar 

  • Regvar M, Vogel-Mikuš K (2008) Recent advances in understanding of plant responses to excess metals: exposure, accumulation and tolerance. In: Kahn NA, Singh S, Umar S (eds) Sulphur assimilation and abiotic stress in plants. Springer, New York

    Google Scholar 

  • Regvar M, Vogel-Mikuš K, Kugonic N, Turk B, Batic F (2006) Vegetational and mycorrhizal successions at a metal polluted site: Indications for the direction of phytostabilisation? Environ Pollut 144:976–984

    Article  PubMed  CAS  Google Scholar 

  • Rivera-Becerril F, Calantzis F, Turnau K, Caussanel J-P, Belimov AA, Gianinazzi S, Strasser RJ, Gianinazzi-Pearson V (2002) Cadmium accumulation and buffering of cadmium-induced stress by arbuscular mycorrhiza in three Pisum sativum L. genotypes. J Exp Bot 53:177–1185

    Article  Google Scholar 

  • Robinson RH, Lombi E, Zhao FJ, McGrath SP (2003) Uptake and distribution of nickel and other metals in the hyperaccumulator Berkeya coddii. New Phytologist 158:279–285

    Article  CAS  Google Scholar 

  • Ryszka P, Turnau K (2007) Arbuscular mycorrhiza of introduced and native grasses colonizing zinc wastes: Implications for restoration practices. Plant and Soil 298:219–229

    Article  CAS  Google Scholar 

  • Salt D (2001) Responses and adaptations of plants to metal stress. In: Hawkesford MJ, Buchner P (eds) Molecular analysis of plant adaptation to the environment. Kluyer Academic Publishers, Dordrecht, The Netherlands

    Google Scholar 

  • Sanità di Toppi L, Prasad MNV, Ottonello S (2002) Metal chelating peptides and proteins in plants. In: Prasad MNV, Strzalka K (eds) Physiology and biochemistry of metal toxicity in plants. Kluyver Academic Publishers, Dordrecht, NL

    Google Scholar 

  • Scheloske S, Maetz M, Schneider T, Hildebrandt U, Bothe H, Povh H (2004) Element distribution in mycorrhizal and nonmycorrhizal roots of the halophyte Aster tripolium determined by proton induced X-ray emission. Protoplasma 223:183–189

    Article  PubMed  CAS  Google Scholar 

  • Schüßler A, Schwarzott D, Walker C (2001) A new fungal phylum, the Glomeromycota:phylogeny and evolution. Mycol Res 105:1413–1421

    Article  Google Scholar 

  • Smith SE, Read DJ (1997) Mycorrhizal symbiosis, vol Academic Press. San Diego, USA

    Google Scholar 

  • Stocker O (1928) Das Halophytenproblem. Springer, Berlin

    Google Scholar 

  • Strzyszcz Z (2003) Some problems of the reclamation of waste heaps of zinc and lead ore exploitation in southern Poland. Z Geol Wissenschaft 32:167–173

    Google Scholar 

  • Sudova R, Jurkiewicz A, Turnau K, Vosatka M (2007) Persistence of heavy metal tolerance of the arbuscular mycorrhizal fungus Glomus intraradices under different cultivation regimes. Symbiosis 43:71–81

    CAS  Google Scholar 

  • Sutcliffe JF, Baker DA (1974) Plants and mineral salts. Studies in Biology. vol 48, Edward Arnold, Southampton

    Google Scholar 

  • Tonin C, Vandenkoornhuyse P, Joner EJ, Strczek J, Leyval C (2001) Assessment of arbuscular mycorrhizal fungi diversity in the rhizosphere of Viola calaminaria and effect of these fungi on heavy metal uptake by clover. Mycorrhiza 10:161–168

    Article  CAS  Google Scholar 

  • Trouvelot A, Kough JL, GianinazziV (1986) Mesure du taux de mycorhization VA d’un système radiculaire. Recherche de méthodes d’estimation ayant une signification fonctionelle. In: Gianinazzi-Pearson V, Gianinazzi S (eds) Physiological and genetical aspects of mycorrhizae, vol INRA, ISBN:2-85340-774-8, Paris, p 217-221

    Google Scholar 

  • Turnau K, Mesjasz-Przybylowicz J (2003) Arbuscular mycorrhiza of Berkheya coddii and other Ni-hyperaccumulating members of Asteraceae from ultarmafic soils in South Africa. Mycorrhiza 13:185–190

    Article  PubMed  Google Scholar 

  • Turnau K, Jurkiewicz A, Lingua JM, Barea JM, Gianinazzi-Pearson V (2006a) Role of arbuscular mycorrhiza and associated microorganisms in phytoremediation of heavy metal polluted sites. In: Prasad MNV, Sajwan KS, Naidu R (eds) Trace elements in the environment: biogeochemistry, biotechnology, and bioremediation. CRC Press, Baton Rouge, pp 235–252

    Google Scholar 

  • Turnau K, Orłowska E, Ryszka P, Zubek SZ, Anielska T, Gawroński S, Jurkiewicz A (2006b) Role of mycorrhizal fungi in phytoremediation and toxicity monitoring of heavy metal rich industrial wastes in southern Poland. In: Twardowska I, Allen HE, Häggblom MM (eds) Soil and water pollution monitoring, protection and remediation. Springer, New York, pp 533–551

    Chapter  Google Scholar 

  • Turnau K, Henriques FS, Anieska T, Renker C, Buscot F (2007) Metal uptake and detoxification mechanisms in Erica andevalensis growing in a pyrite mine tailing. Envir Exper Botany 61:117–123

    Article  CAS  Google Scholar 

  • Turnau K, Anielska T, Ryszka P, Gawroński S, Ostachowicz B, Jurkiewicz A (2008) Establishment of arbuscular mycorrhizal plants originating from xerothermic grasslands on heavy metal rich industrial wastes - new solution for waste revegetation. Plant and Soil 305:267–280

    Article  CAS  Google Scholar 

  • Vogel-Mikuš K, Regvar M (2006) Arbuscular mycorrhiza as a tolerance strategy in metal contaminated soils:prospects in phytoremediation. In: Rodes D (ed) New topics in environmental research. Nova Science Publishers, Hauppauge, N.Y

    Google Scholar 

  • Vogel-Mikuš K, Drobne D, Regvar M (2005) Zn, Cd and Pb accumulation and arbuscular mycorrhiza colonization of pennycress Thlaspi praecox Wulf. from the vicinity of a lead mine and smelter in Slovenia. Environ Pollution 133:233–242

    Article  Google Scholar 

  • Vogel-Mikuš K, Pongrac P, Kump P, Necemer M, Regvar M (2006) Colonization of a Zn, Cd and Pb hyperaccumulator Thlaspi praecox Wulfen with indigenous arbuscular mycorrhizal mixture induces changes in heavy metal and nutrient uptake. Environ Pollut 139:362–371

    Article  PubMed  Google Scholar 

  • Vogel-Mikuš K, Pongrac P, Pelicon P, Vapetic P, Povh B, Bothe H, Regvar M (2009) Micro-PIXE analysis for localisation and quantification of elements in roots of mycorrhizal metaltolerant plants. In: Varma A, Kharkwal A (eds) Symbiotic fungus: principles and practice. Springer, New York

    Google Scholar 

  • Weissenhorn I, Leyval C (1993) Cd-tolerant arbuscular mycorrhizal (AM) fungi from heavy- metal polluted soils. Plant Soil 157:247–256

    Article  CAS  Google Scholar 

  • Weissenhorn I, Leyval C (1995) Root colonization of maize by a Cd-sensitive and a Cd- tolerant Glomus mosseae and Cadmium uptake in sand culture. Plant Soil 175:233–238

    Article  CAS  Google Scholar 

  • Wierzbicka M, Panufnik D (1998) The adaptation of Silene vulgaris to growth on a calamine waste heap (S. Poland). Environ Pollution 101:415–426

    Article  CAS  Google Scholar 

  • Wierzbicka M, Pielichowska M (2004) Adaptation of Biscutella laevigata L., a metal hyperaccumulator, to growth on zinc-lead waste heap in southern Poland. Chemosphere 54:1663–1674

    Article  PubMed  CAS  Google Scholar 

  • Wilde P, Manal A, Stodden M, Sieverding E, Hildebrandt U, Bothe H (2009) Biodiversity of arbuscular mycorrhizal fungi in two salt marshes. Environmental Microbiology 11:1548–1561

    Google Scholar 

  • Yamaguchi T, Blumwald E (2005) Developing salt-tolerant plants: challenges and opportunities. Trends Plant Sci 10:615–620

    Article  PubMed  CAS  Google Scholar 

  • Zalẹcka F, Wierzbicka M (2002) The adaptation of Dianthus carthusianorum L. (Caryophyllaceae) to growth on a zinc-lead heap in southern Poland. Plant Soil 246:249–257

    Article  Google Scholar 

  • Zhang J, Shu WS (2006) Mechanisms of heavy metal cadmium tolerance in plants. J Plant Physiol Mol Biol 32:1–8

    Google Scholar 

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Bothe, H., Regvar, M., Turnau, K. (2010). Arbuscular Mycorrhiza, Heavy Metal,and Salt Tolerance. In: Soil Heavy Metals. Soil Biology, vol 19. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-02436-8_5

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