Abstract
Heavy metal (HM) toxicity is an imperative abiotic stress component of the environment that is negatively influencing the agricultural productivity throughout the world. Due to the unprecedented population explosion mainly in developing countries, land resources that are shrinking and therefore utilizing any and every space for cultivation have become a necessity to meet the expanding demands for food, fuel, and fodder. Accumulation of HMs in soil inflicts detrimental effect on various morphological, physiological, and metabolic pathways leading to various other stresses and anomalies in plants. However, plants are equipped with a range of inherent mechanisms to neutralize HM toxicity. Additionally, the phytomicrobiome-microorganisms that colonize plants can allow them to better tolerate soil pollutants. Considering that even contaminated soils are a potential asset for agricultural production, it is crucial to develop remediation techniques involving plants and associated microbiota for sustainable cleanup of defiled land resources so as to avoid biomagnification of toxic trace elements in the food chain. Fungi, both symbiotic and nonsymbiotic, are an important component of soil microbiota. Vesicular arbuscular mycorrhizal fungi (VAMF) are known to enhance nutrient acquisition from soil, promote growth and development, boost reproductive success, modulate secondary metabolic pathways, and confer biotic and abiotic stress tolerance to its host plants. In this chapter, we present the discussion on fungal symbionts and role of VAMF in combating HM stress that interferes with plant development and affects crop productivity. A detailed update on recent research has also been covered which contributes to a better understanding of the potential of this unique mutualistic relationship that can be engaged in the sustainable production of agricultural and other economically important plants in a changing world.
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References
Akiyama K, Matsuzaki K, Hayashi H (2005) Plant sesquiterpenes induce hyphal branching in arbuscular mycorrhizal fungi. Nature 435:824–827
Ali H, Khan E, Sajad MA (2013) Phytoremediation of heavy metals—concepts and applications. Chemosphere 91:869–881
Aloui A, Recorbet G, Robert F et al (2011) Arbuscular mycorrhizal symbiosis elicits shoot proteome changes that are modified during cadmium stress alleviation in Medicago truncatula. BMC Plant Biol. https://doi.org/10.1186/1471-2229-11-75
Anderson TA, Guthrie EA, Walton BT (1993) Bioremediation in the rhizosphere. Environ Sci Technol 27:2630–2636
Auge RM (2001) Water relations, drought and vesicular-arbuscular mycorrhizal symbiosis. Mycorrhiza 11:3–42
Austruy A, Shahid M, Xiong T et al (2014) Mechanisms of metal-phosphates formation in the rhizosphere soils of pea and tomato: environmental and sanitary consequences. J Soils Sediments 14:666–678
Azcón-Aguilar C, Palenzuela J, Roldán A et al (2003) Analysis of the mycorrhizal potential in the rhizosphere of representative plant species from desertification- threatened Mediterranean shrublands. Appl Soil Ecol 22:29–37
Barrow JR, Lucero ME, Reyes-Vera I et al (2008) Do symbiotic microbes have a role in plant evolution, performance and response to stress? Commun Integr Biol 1:69–73
Bécard G, Pfeffer PE (1993) Status of nuclear division in arbuscular mycorrhizal fungi during in-vitro development. Protoplasma 174:62–68
Berg G, Grube M, Schloter M (2014) Unraveling the plant microbiome: looking back and future perspectives. Front Microbiol 5:148–152
Berti WR, Cunningham SD (2000) Phytostabilization of metals. In: Raskin I, Ensley BD (eds) Phytoremediation of toxic metals: using plants to clean-up the environment. Wiley, New York, pp 71–88
Bittman S, Hunt D, Kowalenko CG et al (2004) Early phosphorus nutrition in corn and the role of mycorrhizae. In: Bittman S, Kowalenko CG (eds) Advanced silage corn management: a production guide for coastal British Columbia and the Pacific Northwest
Brundrett MC (1991) Mycorrhizas in natural ecosystems. In: Macfayden A, Begon M, Fitter AH (eds) Advances in ecological research, vol 21. Academic, London, pp 171–313
Bucher M (2007) Functional biology of plant phosphate uptake at root and mycorrhiza interfaces. New Phytol 173(1):11–26
Cambrolle J, Mateos-Naranjo E, Redondo-Gomez S et al (2011) Growth, reproductive and photosynthetic responses to copper in the yellow-horned poppy, Glaucium flavum Crantz. Environ Exp Bot 71:57–64
Chaparro JM, Badri VD, Vivanco MJ (2014) Rhizosphere microbiome assemblage is affected by plant development. ISME J 8(4):790–803. https://doi.org/10.1038/ismej.2013.196
Cornejo P, Meier S, Borie G et al (2008) Glomalin-related soil protein in a Mediterranean ecosystem affected by a copper smelter and its contribution to Cu and Zn sequestration. Sci Total Environ 406:154–160
Cornejo P, Pérez-Tienda J, Meier S et al (2013) Copper compartmentalization in spores as a survival strategy of arbuscular mycorrhizal fungi in Cu-polluted environments. Soil Biol Biochem 57:25–928
Dehne HW, Schoenbeck F (1979) The influence of endotrophic mycorrhizae on plant disease. I. Colonization of tomato plants by Fusarium oxysporum f.sp. lycopersici. Phytopatholology 95:105–110
Diaz G, Azcón-Aguilar C, Honrubia M (1996) Influence of arbuscular mycorrhizae on heavy metal (Zn and Pb) uptake and growth of Lygeum spartum and Anthyllis cytisoides. Plant Soil 180:241–249
Dudhane M, Borde M, Jite PK (2012) Effect of aluminium toxicity on growth responses and antioxidant activities in Gmelina arborea Roxb inoculated with AM Fungi. Int J Phytoremediation 14:643–655
Elbon A, Whalen JK (2014) Phosphorus supply to vegetable crops from arbuscular mycorrhizal fungi: a review. Biol Agric Hortic 31:73–90
Emamverdian A, Ding Y, Mokhberdoran F et al (2015) Heavy metal stress and some mechanisms of plant defense response. Sci World J 2015:1–18. https://doi.org/10.1155/2015/756120
Enkhtuya B, Rydlová J, Vosátka M (2002) Effectiveness of indigenous and non-indigenous isolates of arbuscular mycorrhizal fungi in soils from degraded ecosystems and man-made habitats. Appl Soil Ecol 14:201–211
Etim EE (2012) Phytoremediation and its mechanism: a review. Int J Environ Bioener 2:120–136
Feng G, Song YC, Li XL et al (2003) Contribution of arbuscular mycorrhizal fungi to utilization of organic sources of phosphorus by red clover in a calcareous soil. Appl Soil Ecol 22:139–148
Flora SJS, Mittal M, Mehta A (2008) Heavy metal induced oxidative stress and its possible reversal by chelation therapy. Indian J Med Res 128:501–523
Foucault Y, Leveque T, Xiong T et al (2013) Green manure plants for remediation of soils polluted by metals and metalloids: ecotoxicity and human bioavailability assessment. Chemosphere 93:1430–1435
Garbisu C, Alkorta I (2001) Phytoextraction: a cost-effective plant-based technology for the removal of metals from the environment. Bioresour Technol 77:229–236
Giasson P, Jaouich A, Gagné S et al (2005) Phytoremediation of zinc and cadmium: a study of arbuscular mycorrhizal hyphae. Remediation 15:113–122
Giasson P, Jaouich A, Cayer P et al (2006) Enhanced phytoremediation: a study of heavy mycorrhizoremediation metal–contaminated soil. Remediation 17:97–110
Gill SS, Tuteja N (2010) Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiol Biochem 48:909–930
Göhre V, Paszkowski U (2006) Contribution of the arbuscular mycorrhizal symbiosis to heavy metal phytoremediation. Planta 223:1115–1122
González-Chávez C, Carrillo-González R, Wright SF et al (2004) The role of glomalin, a protein produced by arbuscular mycorrhizal fungi in sequestering potentially toxic elements. Environ Pollut 130:317–323
González-Guerrero M, Azcón-Aguilar C, Mooney M et al (2005) Characterization of a Glomus intraradices gene encoding a putative Zn transporter of the cation diffusion facilitator family. Fungal Genet Biol 42:130–140
González-Guerrero M, Azcón-Aguilar C, Ferrol N (2006) GintABC1 and GintMT1 are involved in Cu and Cd homeostasis in Glomus intraradices. In: Abstracts of the 5th international conference on mycorrhiza, Granada, Spain
Gray LE, Gerdemann JW (1969) Uptake of phosphorus-32 by vesicular-arbuscular mycorrhizae. Plant Soil 30:415–422. https://doi.org/10.1007/BF01881967
Grayston SJ, Wang S, Campbell CD et al (1998) Selective influence of plant species on microbial diversity in the rhizosphere. Soil Biol Biochem 30:369–378
Guimaraes BCM, Arends JBA, van der Ha D et al (2010) Microbial services and their management: recent progresses in soil bioremediation technology. Appl Soil Ecol 46:157–167
Gutjahr C, Parniske M (2013) Cell and developmental biology of arbuscular mycorrhiza symbiosis. Annu Rev Cell Dev Biol 29:593–617
Hall JL (2002) Cellular mechanisms for heavy metal detoxification and tolerance. J Exp Bot 53:1–11
Hardoim PR, van Overbeek LS, Berg G et al (2015) The hidden world within plants: ecological and evolutionary considerations for defining functioning of microbial endophytes. Microbiol Mol Biol Rev 79:293–320. https://doi.org/10.1128/MMBR.00050-14
Harley JL (1971) Fungi in ecosystems. J Appl Ecol 8:627–642
Harley JL (1989) The significance of mycorrhiza. Mycol Res 92:129–139
Harley JL, Smith SE (1983) Mycorrhizal symbiosis. Academic Press, Toronto, pp 112–115
Harrier L (2001) The arbuscular mycorrhizal symbiosis: a molecular review of the fungal dimension. J Exp Bot 52:469–478
Harrison MJ, van Buuren ML (1995) A phosphate transporter from the mycorrhizal fungus Glomus versiforme. Nature 378:626–629
Heggo A, Angle JS, Chaney RL (1990) Effects of vesicular arbuscular mycorrhizal fungi on heavy-metal uptake by soybeans. Soil Biol Biochem 22:865–869
Helber N, Wippel K, Sauer N et al (2011) A versatile monosaccharide transporter that operates in the arbuscular mycorrhizal fungus Glomus sp is crucial for the symbiotic relationship with plants. Plant Cell 23:3812–3823
Hijri M, Sanders IR (2005) Low gene copy number shows that arbuscular mycorrhizal fungi inherit genetically different nuclei. Nature 433:160–163
Hildebrandt U, Ouziad F, Marner FJ, Bothe H (2006) 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
Hildebrandt U, Regvar M, Bothe H (2007) Arbuscular mycorrhiza and heavy metal tolerance. Phytochemistry 681:139–146
Hosny M, Gianinazzi-Pearson V, Dulieu H (1998) Nuclear DNA content of 11 fungal species in glomales. Genome 41:422–428
Jarrah M, Ghasemi-Fasaei R, Karimian N et al (2014) Investigation of Arbuscular mycorrhizal fungus and EDTA efficiencies on lead phytoremediation by sunflower in a calcareous soil. Biorem J 18:71–79
Jarup L (2003) Hazards of heavy metal contamination. Br Med Bull 68:167–182
Joachim HJ, Makoi R, Ndakidemi PA (2009) The agronomic potential of vesicular-arbuscular mycorrhiza (VAM) in cereals-legume mixtures in Africa. Afr J Microbiol Res 3:664–675
Joner EJ, Leyval C (1997) Uptake of 109Cd by roots and hyphae of a Glomus mosseae/Trifolium subterraneum mycorrhiza from soil amended with high and low concentrations of cadmium. New Phytol 135:353–360
Joner EJ, Leyval C, Briones R (2000a) Metal binding capacity of arbuscular mycorrhizal mycelium. Biol Fertil Soils 226:227–234
Joner EJ, Ravnskov S, Jakobsen I (2000b) Arbuscular mycorrhizal phosphate transport under monoxenic conditions using radiolabeled inorganic and organic phosphate. Biotechnol Lett 22:1705–1708
Jung SC, Martinez-Medina A, Lopez-Raez JA et al (2012) Mycorrhiza-induced resistance and priming of plant defenses. J Chem Ecol 38(6):651–664
Kaldorf M, Kuhn AJ, Schroder WH et al (1999) Selective element deposits in maize colonized by a heavy metal tolerance conferring arbuscular mycorrhizal fungus. J Plant Physiol 154:718–728
Kendrick B (1985) The fifth kingdom. Mycologue Publications, Waterloo
Khan AG (2006) Mycorrhizoremediation-an enhanced form of phytoremediation. J Zhejiang Univ Sc B 7:503–514
Kim KY, Jordan D, McDonald GA (1997) Effect of phosphate-solubilizing bacteria and vesicular-arbuscular mycorrhizae on tomato growth and soil microbial activity. Biol Fertil Soils 26:79–87
Knack JJ, Wilcox LW, Ané JM et al (2015) Microbiomes of streptophyte algae and bryophytes suggest that a functional suite of microbiota fostered plant colonization of land. Int J Plant Sci 176:405–420. https://doi.org/10.1086/681161
Krings M, Taylor TN, Hass H et al (2007) Fungal endophytes in a 400 million-yr-old land plant: infection pathways, spatial distribution and host responses. New Phytol 174:648–657
Krupa S, Anderson J, Marx DH (1973) Studies on ectomycorrhizae of pine. IV. Volatile organic compounds in mycorrhizal and nonmycorrhizal root systems of Pinus echinata Mill. Eur J For Pathol 3:194–200
Kuhn G, Hijri M, Sanders IR (2001) Evidence for the evolution of multiple genomes in arbuscular mycorrhizal fungi. Nature 414:745–748
Kuiper I, Lagendijk EL, Bloemberg GV et al (2004) Rhizoremediation: a beneficial plant-microbe interaction. Mol Plant Microb Interact 17:6–15
Laheurte F, Leyval C, Berthelin J (1990) Root exudates of maize, pine and beech seedlings influenced by mycorrhizal and bacterial inoculation. Symbiosis 9:111–116
Lanfranco L, Bolchi A, Ros EC et al (2002) Differential expression of a metallothionein gene during the presymbiotic versus the symbiotic phase of an arbuscular mycorrhizal fungus. Plant Physiol 130:58–67
Li XL, Christie P (2001) Changes in soil solution Zn and pH and uptake of Zn by arbuscular mycorrhizal red clover in Zn-contaminated soil. Chemosphere 42:201–207
Li XL, George E, Marschner H (1991) Phosphorus depletion and pH decrease at the root-soil and hyphae-soil interfaces of VA mycorrhizal white clover fertilized with ammonium. New Phytol 119:397–404
Lingua G, Franchin C, Todeschini V et al (2008) Arbuscular mycorrhizal fungi differentially affect the response to high zinc concentrations of two registered poplar clones. Environ Pollut 153:137–147
Liu A, Hamel C, Hamilton RI et al (2000) Acquisition of Cu, Zn, Mn and Fe by mycorrhizal maize (Zea mays L.) grown in soil at different P and micronutrient levels. Mycorrhiza 9:331–336
López-Pedrosa A, González-Guerrero M, Valderas A (2006) GintAMT1 encodes a functional high-affinity ammonium transporter that is expressed in the extraradical mycelium of Glomus intraradices. Fungal Genet Biol 43:102–110
Lugtenberg B, Kamilova F (2009) Plant-growth promoting rhizobacteria. Annu Rev Microbiol 63:541–556. https://doi.org/10.1146/annurev.micro.62.081307.162918
Malbreil M, Tisserant E, Martin F et al (2014) Genomics of arbuscular mycorrhizal fungi: out of the shadows. Adv Bot Res 70:259–290
Malekzadeh E, Aliasgharzad N, Majidi J et al (2016) Cd-induced production of glomalin by arbuscular mycorrhizal fungus (Rhizophagus irregularis) as estimated by monoclonal antibody assay. Environ Sci Pollut Res 23(20):20711–20718. https://doi.org/10.1007/s11356-016-7283-z
Marques AP, Oliveira RS, Samardjieva KA et al (2007) Solanum nigrum grown in contaminated soils. Effects of AMF on zinc accumulation and histolocalisation. Environ Pollut 145:691–699
Martin F, Tuskan GA, DiFazio SP et al (2004) Symbiotic sequencing for the Populus mesocosm. New Phytol 161:330–335
Meier S, Cornejo P, Cartes P et al (2015) Interactive effect between Cu-adapted arbuscular mycorrhizal fungi and biotreated agrowaste residue to improve the nutritional status of Oenothera picensis growing in Cu-polluted soils. J Plant Nutr Soil Sci 178:126–135
Miller MH (2000) Arbuscular mycorrhizae and the phosphorus nutrition of maize: a review of Guelph studies. Can J Plant Pathol Sci 80(1):47–52
Mohammadi K, Khalesro S, Sohrabi Y et al (2011) A review: beneficial effects of the mycorrhizal fungi for plant growth. J Appl Environ Biol Sci 9:310–319
Morton JB (1988) Taxonomy of VA mycorrhizal fungi: classification, nomenclature and identification. Mycotaxon 32:267–324
Morton JB, Benny GL (1990) Revised classification of arbuscular mycorrhizal fungi (Zygomycetes): a new order, Glomales, two new suborders Glomineae and Gigasporineae and two new families Acaulosporaceae and Gigasporaceae with an emendation of Glomaceae. Mycotaxon 37:471–491
Morton JB, Redecker D (2001) Two new families of Glomales, Archaeosporaceae and Paraglomaceae, with two new genera Archaeospora and Paraglomus, based on concordant molecular and morphological characters. Mycologia 93:181–195
Mosse B (1953) Fructifications associated with mycorrhizal strawberry roots. Nature 171:974
Mosse B, Hepper C (1975) Vesicular-arbuscular mycorrhizal infections in root organ cultures. Physiol Plant Pathol 5:215–223
Nagajyoti PC, Lee KD, Sreekanth TVM (2010) Heavy metals, occurrence and toxicity for plants: a review. Environ Chem Lett 8:199–216
Nichols K (2003) Characterization of glomalin-a glycoprotein produced by arbuscular mycorrhizal fungi. Ph. D Dissertation. University of Maryland, College Park, Maryland
Nichols KA, Wright SF (2006) Carbon and nitrogen in operationally defined soil organic matter pools. Biol Fertil Soils 43:215–220
Oehl F, Sieverding E (2004) Pacispora, a new vesicular-arbuscular mycorrhizal fungal genus in the Glomeromycetes. J Appl Bot Food Qual 78:72–82
Oehl F, Souza FA, Sieverding E (2008) Revision of Scutellospora and description of five new genera and three new families in the arbuscular mycorrhizal-forming Glomeromycetes. Mycotaxon 106:311–360
Oehl F, Silva GA, Goto BT et al (2011a) Glomeromycetes: three new genera and glomoid species reorganized. Mycotaxon 116:75–120
Oehl F, Silva DKA, Maia LC et al (2011b) Orbispora gen. nov., ancestral in the Scutellosporaceae (Glomeromycetes). Mycotaxon 116:161–169
Oehl F, Silva GA, Goto BT et al (2011c) Glomeromycota: two new classes and a new order. Mycotaxon 116:365–379
Oehl F, Silva GA, Sanchez-Castro I et al (2011d) Revision of Glomeromycetes with entrophosporoid and glomoid spore formation with three new genera. Mycotaxon 117:297–316
Oehl F, Sieverding E, Palenzuela J et al (2011e) Advances in Glomeromycota taxonomy and classification. IMA Fungus: The Global Mycological Journal 2(2):191–199
Olsson PA, Francis R, Read DJ et al (1998) Growth of arbuscular mycorrhizal mycelium in calcareous dune sand and its interaction with other soil microorganisms as estimated by measurement of specific fatty acids. Plant Soil 201:9–16
Palenzuela J, Ferrol N, Boller T et al (2008) Otospora bareai, a new fungal species in the Glomeromycetes from a dolomitic shrub land in Sierra de Baza National Park (Granada, Spain). Mycologia 100(2):296–305
Partida-Martínez LP, Heil M (2011) The microbe-free plant: factor artifact? Front Plant Sci 2:100. https://doi.org/10.3389/fpls.2011.00100
Pawlowska TE (2005) Genetic processes in arbuscular mycorrhizal fungi. FEMS Microbiol Lett 251:85–192
Pérez-Tienda J, Testillano PS, Balestrini R et al (2011) GintAMT2, a new member of the ammonium transporter family in the arbuscular mycorrhizal fungus Glomus intraradices. Fungal Genet Biol 48:1044–1055
Petrini O (1991) Fungal endophytes of tree leaves. In: Andrews JH, Hirano SS (eds) Microbial ecology of leaves. Springer, New York, pp 179–197. https://doi.org/10.1007/978-1-4612-3168-4_9
Pilon-Smits E (2005) Phytoremediation. Annu Rev Plant Biol 56:15–39
Pirozynski KA, Dalpé Y (1989) Geological history of the Glomaceae with particular reference to mycorrhizal symbiosis. Symbiosis 7:1–36
Pirozynski KA, Malloch DW (1975) The origin of land plants a matter of mycotrophism. Biosystems 6:153–164
Pourrut B, Jean S, Silvestre J et al (2011) Lead-induced DNA damage in Vicia faba root cells: potential involvement of oxidative stress. Mutat Res 726:123–128
Pourrut B, Shahid M, Douay F et al (2013) Molecular mechanisms involved in lead uptake, toxicity and detoxification in higher plants. In: Gupta DK, Corpas FJ, Palma JM (eds) Heavy metal stress in plants. Springer, Berlin, pp 121–147
Rascio N, Navari-Izzo F (2011) Heavy metal hyperaccumulating plants: how and why do they do it? And what makes them so interesting? Plant Sci 180:169–181
Redecker D, Kodner R, Graham LE (2000) Glomalean fungi from the Ordovician. Science 289(5486):1920–1921
Redecker D, Schussler A, Stockinger H et al (2013) An evidence-based consensus for the classification of arbuscular mycorrhizal fungi (Glomeromycota). Mycorrhiza 23:515–531
Reid CPP (1990) Mycorrhizas. In: Lynch JM (ed) The rhizosphere. Wiley, Chichester, pp 281–315
Remy W, Taylor TN, Hass H et al (1994) Four hundred-million-year-old vesicular arbuscular mycorrhizae. Proc Natl Acad Sci U S A 91(25):11841–11843
Repetto O, Bestel-Corre G, Dumas-Gaudot E et al (2003) Targeted proteomics to identify cadmium-induced protein modifications in Glomus mosseae-inoculated pea roots. New Phytol 157:555–567
Rillig MC (2004) Arbuscular mycorrhizae, glomalin, and soil aggregation. Can J Soil Sci 84:355–363
Rillig MC, Steinberg PD (2002) Glomalin production by an arbuscular mycorrhizal fungus: a mechanism of habitat modification. Soil Biol Biochem 34:1371–1374
Rivera-Becerril F, van Tuinen D, Martin-Laurent F et al (2005) Molecular changes in Pisum sativum L. roots during arbuscular mycorrhiza buffering of cadmium stress. Mycorrhiza 16:51–60
Rodriguez RJ, Redman RS, Henson JM (2004) The role of fungal symbioses in the adaptation of plants to high stress environments. Mitig Adapt Strateg Glob Chang 9:261–272
Sampangi RK (1989) Some recent advances in the study of fungal root diseases. Ind Phytopth 22:1–17
Schüßler A, Schwarzott D, Walker C (2001) A new fungal phylum the Glomeromycota: phylogeny and evolution. Mycol Res 105:1413–1142
Schwab AP, Banks MK (1994) Biologically mediated dissipation of polyaromatic hydrocarbons in the root zone. In: Anderson TA, Coats JR (eds) Bioremediation through rhizosphere technology. American Chemical Society, Washington, DC, pp 132–141
Shahid M, Khalid S, Abbas G et al (2015) Heavy metal stress and crop productivity. In: Hakeem K (ed) Crop production and global environmental issues. Springer, Cham, pp 1–25
Sharma P, Jha AB, Dubey RS et al (2012) Reactive oxygen species, oxidative damage, and antioxidative defense mechanism in plants under stressful conditions. J Bot. Article ID 217037
Shivakumar CK, Hemavani C, Thippeswamy B et al (2011) Effect of inoculation with arbuscular mycorrhizal fungi on green gram grown in soil containing heavy metal zinc. Journal of Experimental Sciences 2:17–21
Sieverding E, Oehl F (2006) Revision of Entrophospora and description of Kuklospora and Intraspora, two new genera in the arbuscular mycorrhizal Glomeromycetes. J Appl Bot Food Qual 80:69–81
Singh R, Tripathi RD, Dwivedi S et al (2010) Lead bioaccumulation potential of an aquatic macrophyte Najas indica are related to antioxidant system. Bioresour Technol 101:3025–3032
Spain JL, Sieverding E, Oehl F (2006) Appendicispora, a new genus in the arbuscular mycorrhizal-forming Glomeromycetes, with a discussion of the genus Archaeospora. Mycotaxon 97:163–182
Strobel NE, Sinclair WA (1991) Role of flavonolic wall infusions in the resistance induced by Laccaria bicolor to Fusarium oxysporum in primary roots of Douglas fir. Phytopathology 81:420–425
Sytar O, Kumar A, Latowski D et al (2013) Heavy metal-induced oxidative damage, defense reactions, and detoxification mechanisms in plants. Acta Physiol Plant 35:985–999
Takács T, Birơ B, Vörös I (2001) Arbuscular mycorrhizal effect on heavy metal uptake of ryegrass (Lolium perenne L.) in pot culture with polluted soil. In: Horst WWJ, Scheck MK, Bürkert A et al (eds) Plant nutrition: food security and sustainability of agro-ecosystems through basic and applied research, developments in plant and soil sciences. Kluwer Academic, Dordrecht, pp 480–481
Tamayo E, Gómez-Gallego T, Azcón-Aguilar C et al (2014) Genome-wide analysis of copper, iron and zinc transporters in the arbuscular mycorrhizal fungus Rhizophagus irregularis. Plant Traffic Transp 5:1–13
Tao HQ (1997) Effect of arbuscular mycorrhiza on resistance of red clover to heavy metal Zn and Cd pollution. MS thesis, China Agricultural University, Beijing
Taylor J, Harrier LA (2001) A comparison of development and mineral nutrition of micropropagated Fragaria×ananassa cv. Elvira (strawberry) when colonized by nine species of arbuscular mycorrhizal fungi. Appl Soil Ecol 18(3):205–215
Thangavel P, Subhuram CV (2004) Phytoextraction-role of hyper accumulators in metal contaminated soils. Proc Indian Natl Sci Acad 70(1):109–130
Tisserant E, Malbreil M, Kuo A et al (2013) Genome of an arbuscular mycorrhizal fungus provides insight into the oldest plant symbiosis. Proc Natl Acad Sci 110:20117–20122
Tullio M, Pierandrei F, Salerno A et al (2003) Tolerance to cadmium of vesicular arbuscular mycorrhizae spores isolated from a cadmium-polluted and unpolluted soil. Biol Fertil Soils 37:211–214
Turnau K (1998) Heavy metal content and localization in mycorrhizal Euphorbia cyparissias from zinc wastes in southern Poland. Acta Soc Bot Poloniae 67:105–113
Turnau K, Kottke I, Oberwinkler F (1993) Element localization in mycorrhizal roots of Pteridium aquilinum (L.) Kuhn collected from experimental plots treated with cadmium dust. New Phytol 123:313–324
Walker C, Schüßler A (2004) Nomenclature clarifications and new taxa in the Glomeromycota. Mycol Res 108:979–982
Weissenhorn I, Leyval C, Belgy G et al (1995) Arbuscular mycorrhizal contribution to heavy metal uptake by maize (Zea mays L.) in pot culture with contaminated soil. Mycorrhiza 5:245–251
Weller DM, Raaijmakers JM, Gardener BB et al (2002) Microbial populations responsible for specific soil suppressiveness to plant pathogens. Annu Rev Phytopathol 40:309–348. https://doi.org/10.1146/annurev.phyto.40.030402.110010
Whipps JM (2004) Prospects and limitations for mycorrhizas in biocontrol of root pathogens. Can J Bot 1227:1198–1227
Wright SF, Upadhyaya A (1998) A survey of soils for aggregate stability and glomalin, a glycoprotein produced by hyphae of arbuscular mycorrhizal fungi. Plant Soil 198(1):97–107. https://doi.org/10.1023/A:1004347701584
Xiong T, Leveque T, Shahid M et al (2014) Lead and cadmium phytoavailability and human bioaccessibility for vegetables exposed to soil or atmospheric pollution by process ultrafine particles. J Environ Qual 43:1593–1600
Yang J, Kloepper JW, Ryu CM (2009) Rhizosphere bacteria help plants tolerate abiotic stress. Trends Plant Sci 14:1–4
Yang Y, Han X, Liang Y et al (2015) The combined effects of arbuscular mycorrhizal fungi (AMF) and lead (Pb) stress on Pb accumulation, plant growth parameters, photosynthesis, and antioxidant enzymes in Robinia pseudoacacia L. PLoS One 10(12):e0145726
Zhou JL (1999) Zn biosorption by Rhizopus arrhizus and other fungi. Appl Microbiol Biotechnol 51:686–693
Zhu YG, Christie P, Laidlaw AS (2001) Uptake of Zn by arbuscular mycorrhizal white clover from Zn-contaminated soil. Chemosphere 42:193–199
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Chaturvedi, R., Malik, G. (2019). VAM-Assisted Adaptive Response and Tolerance Mechanism of Plants Under Heavy Metal Stress: Prospects for Bioremediation. In: Kumar, M., Muthusamy, A., Kumar, V., Bhalla-Sarin, N. (eds) In vitro Plant Breeding towards Novel Agronomic Traits. Springer, Singapore. https://doi.org/10.1007/978-981-32-9824-8_12
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DOI: https://doi.org/10.1007/978-981-32-9824-8_12
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