Abstract
Arsenic (As) is a nonessential element, and its uptake and accumulation in plants can produce several negative effects including disturbance in metabolism and physiological disorders or, in extreme cases, cause plant death. However, some microorganisms have the capacity to tolerate those unfavorable effects and to improve plant development under As-enriched environments. Among them, arbuscular mycorrhizal fungi (AMF) are able to alleviate the harmful effects of the metalloid. AMF have been found to occur in contaminated environments, possibly due to several physiological and biochemical mechanisms that fungi display to tolerate As presence. Mycorrhizal plants show more tolerance to As toxicity since (i) AMF inoculation increases plant biomass and promotes a dilution effect in the As concentration in plant; (ii) sequester As in intraradical hyphae, and reducing the metal intake by roots; (iii) mycorrhizal symbiosis immobilizes As, reducing its translocation to different plant tissues; (iv) AMF can reduce arsenic absorption by repressing the arsenate/phosphate transporters; (v) AMF promote the biotransformation of As and (vi) can protect its plant host reducing oxidative damage. This chapter summarizes current knowledge about the effect of As contamination on plants and the role of arbuscular mycorrhizal symbiosis and its contribution to the phytoremediation of polluted soil.
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Abbas MHH, Meharg AA (2008) Arsenate, arsenite and dimethyl arsinic acid (DMA) uptake and tolerance in maize (Zea mays L.). Plant Soil 304:277–289
Adriano DC (2001) Trace elements in terrestrial environments. Springer, New York
Benabdellah K, Merlos MA, Azcón-Aguilar C et al (2009a) GintGRX1, the first characterized glomeromycotan glutaredoxin, is a multifunctional enzyme that responds to oxidative stress. Fungal Genet Biol 46:94–103
Benabdellah K, Azcón-aguilar C, Valderas A et al (2009b) GintPDX1 encodes a protein involved in vitamin B6 biosynthesis that is up-regulated by oxidative stress in the arbuscular mycorrhizal fungus Glomus irregularis. New Phytol 184:682–693
Bleeker PM, Hakvoort HW, Bliek M et al (2006) Enhanced arsenate reduction by a CDC25-like tyrosine phosphatase explains increased phytochelatin accumulation in arsenate-tolerant Holcus lanatus. Plant J 45:917–929
Bona E, Marsanoa F, Massaa N et al (2011) Proteomic analysis as a tool for investigating arsenic stress in Pteris vittata roots colonized or not by arbuscular mycorrhizal symbiosis. J Proteome 7:1338–1350
Bustingorri C, Balestrasse K, Lavado RS (2015) Effects of high arsenic and fluoride soil concentrations on soybean plants. Phyton 84:407–415
Calonne M, Fontaine J, Debiane D et al (2010) Propiconazole toxicity on the non-target organism, the arbuscular mycorrhizal fungus Glomus irregulare. In: Carisse O (ed) Fungicides. InTech, Rijeka, pp 23–39
Carey AM, Norton GJ, Deacon C et al (2011) Phloem transport of arsenic species from flag leaf to grain during grain filling. New Phytol 192:87–98
Catarecha P, Segura MD, Franco-Zorrilla JM et al (2007) A mutant of the Arabidopsis phosphate transporter PHT1;1 displays enhanced arsenic accumulation. Plant Cell 19:1123–1133
Chakrabarty D, Trivedi PK, Misra P et al (2009) Comparative transcriptome analysis of arsenate and arsenite stresses in rice seedlings. Chemosphere 74:688–702
Chen BD, Xiao XY, Zhu YG et al (2007) The arbuscular mycorrhizal fungus Glomus mosseae gives contradictory effects on phosphorus and arsenic acquisition by Medicago sativa Linn. Sci Total Environ 379:226–234
Chen LH, Hu XW, Yang WQ et al (2015) The effects of arbuscular mycorrhizal fungi on sex-specific responses to Pb pollution in Populus cathayana. Ecotoxicol Environ Saf 113:460–468
Choudhury B, Chowdhury S, Biswas AK (2011) Regulation of growth and metabolism in rice (Oryza sativa L.) by arsenic and its possible reversal by phosphate. J Plant Interact 6:15–24
Christophersen HM, Smith FA, Smith SE (2009) Arbuscular mycorrhizal colonization reduces arsenate uptake in barley via down regulation of transporters in the direct epidermal phosphate uptake pathway. New Phytol 184:962–974
Codling EE, Chaney RL, Green CE (2016) Accumulation of lead and arsenic by potato grown on lead-arsenate-contaminated orchard soils. Commun Soil Sci Plant Anal 47:799–807
Czech V, Czövek P, Fodor J et al (2008) Investigation of arsenate phytotoxicity in cucumber plants. Acta Biol Szeged 52:79–80
Das HK, Mitra AK, Sengupta PK et al (2004) Arsenic concentrations in rice, vegetables, andfish in Bangladesh: a preliminary study. Environ Int 30:383–387
Emamverdian A, Ding Y, Mokhberdoran F, Xie Y (2015) Heavy metal stress and some mechanisms of plant defense response. Sci World J 2015:1
Farooq MA, Li L, Ali B et al (2015) Oxidative injury and antioxidant enzymes regulation in arsenic-exposed seedlings of four Brassica napus L. cultivars. Environ Sci Pollut Res 22:10699–10712
Farooq MA, Gill RA, Ali B et al (2016) Subcellular distribution, modulation of antioxidant and stress-related genes response to arsenic in Brassica napus L. Ecotoxicology 25:350–366
Finnegan P, Chen W (2012) Arsenic toxicity: the effects on plant metabolism. Front Physiol 3:1–18
Fuentes A, Almonacid L, Ocampo JA et al (2016) Synergistic interactions between a saprophytic fungal consortium and Rhizophagus irregularis alleviate oxidative stress in plants grown in heavy metal contaminated soil. Plant Soil 407:355–366
Garg N, Singla P (2011) Arsenic toxicity in crop plants, physiological effects and tolerance mechanisms. Environ Chem Lett 9:303–321
Garg N, Singla P (2012) The role of Glomus mosseae on key physiological and biochemical parameters of pea plants grown in arsenic contaminated soil. Sci Hortic 143:92–101
Garg N, Singla P, Bhandari P (2015) Metal uptake, oxidative metabolism, and mycorrhization on pigeonpea and pea under arsenic and cadmium stress. Turk J Agric For 39:234–250
Giovannetti M, Tolosano M, Volpe V et al (2014) Identification and functional characterization of a sulfate transporter induced by both sulfur starvation and mycorrhiza formation in Lotus japonicus. New Phytol 204:609–619
Gonzalez-Chavez C, Harris PJ, Dodd J et al (2002) Arbuscular mycorrhizal fungi confer enhanced arsenate resistance on Holcus lanatus. New Phytol 155:163–171
Gonzalez-Chavez MDA, Ortega-Larrocea MD, Carrillo-Gonzalez R et al (2011) Arsenate induces the expression of fungal genes involved in as transport in arbuscular mycorrhiza. Fungal Biol 115:1197–1209
González-Guerrero M, Benabdellah K, Valderas A et al (2010) GintABC1 encodes a putative ABC transporter of the MRP subfamily induced by cu, cd, and oxidative stress in Glomus irregularis. Mycorrhiza 20:137–146
Goupil P, Souguir D, Ferjani E et al (2009) Expression of stress-related genes in tomato plants exposed to arsenic and chromium in nutrient solution. J Plant Physiol 166:1446–1452
Gulz PA, Gupta SK, Schulin R (2005) Arsenic accumulation of common plants from contaminated soils. Plant Soil 272:337–347
Gusman GS, Oliveira JA, Farnese FS et al (2013) Arsenate and arsenite, the toxic effects on photosynthesis and growth of lettuce plants. Acta Physiol Plant 35:1201–1209
Hartley-Whitaker J, Ainsworth G, Meharg A (2001) Copperand-arsenic induced oxidative stress in Holcus lanatus L. cloned with differential sensitivity. Plant Cell Environ 24:713–722
Karuppanapandian T, Moo J, Kim C et al (2011) Reactive oxygen species in plants, their generation, signal transduction, and scavenging mechanisms. Aust J Crop Sci 5:709–725
Keshavkant S, Padhan J, Parkhey S et al (2012) Physiological and antioxidant responses of germinating Cicer arietinum seeds to salt stress. Russ J Plant Physiol 59:206–211
Lafuente A, Pajuelo E, Caviedes MA et al (2010) Reduced nodulation in alfalfa induced by arsenic correlates with altered expression of early nodulins. J Plant Physiol 16:286–291
Lafuente A, Perez-Palacios P, Doukkali B et al (2015) Unraveling the effect of arsenic on the model Medicago-Ensifer interaction, a transcriptomic metaanalysis. New Phytol 205:255–272
Lee JT, Yu WC (2012) Evaluation of legume growth in arsenic-polluted acidic soils with various pH values. J Water Sustain 2:13–23
Lenoir I, Fontaine J, Sahraoui ALH (2016) Arbuscular mycorrhizal fungal responses to abiotic stresses: a review. Phytochemistry 123:4–15
Li RY, Ago Y, Liu WJ et al (2009) The rice aquaporin Lsi1 mediates uptake of methylated arsenic species. Plant Physiol 150:2071–2080
Li H, Chen XW, Wong MH (2016) Arbuscular mycorrhizal fungi reduced the ratios of inorganic/ organic arsenic in rice grains. Chemosphere 145:224–230
Lomax C, Liu WJ, Wu LY et al (2012) Methylated arsenic species in plants originate from soil microorganisms. New Phytol 193:665–672
Meharg AA, Hartley-Whitaker J (2002) Arsenic uptake and metabolism in arsenic resistant and non-resistant plant species. New Phytol 154:29–43
Miransari M (2017) Arbuscular mycorrhizal Fungi and heavy metal tolerance in plants. In: Wu QS (ed) Arbuscular mycorrhizas and stress tolerance of plants. Springer, Singapore, pp 147–161
Miteva E, Peycheva S (1999) Arsenic accumulation and effect on peroxidase activity in green bean and tomatoes. Bulg J Agric Sci 5:737–740
Mukhopadhyay R, Shi J, Rosen BP (2000) Purification and characterization of ACR2p, the Saccharomyces cerevisiae arsenate reductase. J Biol Chem 275:21149–21157
Mukhopadhyay R, Rosen BP, Phung LT et al (2002) Microbial arsenic: from geocycles to genes and enzymes. FEMS Microbiol Rev 26:311–325
Mylona PV, Polidoros AN, Scandalios JG (1998) Modulation of antioxidant responses by arsenic in maize. Free Radic Biol Med 25:576–585
Öpik M, Zobel M, Cantero JJ et al (2013) Global sampling of plant roots expands the described molecular diversity of arbuscular mycorrhizal fungi. Mycorrhiza 23:411–430
Pigna M, Cozzolina V, Violante A et al (2009) Influence of phosphate on the arsenic uptake by wheat (Triticum durum L.) irrigated with arsenic solutions at three different concentrations. Water Air Soil Pollut 197:371–380
Pommerrenig B, Diehn TA, Bienert GP (2015) Metalloido-porins: essentiality of Nodulin 26-like intrinsic proteins in metalloid transport. Plant Sci 238:212–227
Pouyu-Rojas E, Siqueira JO, Santos JGD (2006) Compatibilidade simbiótica de fungos micorrízicos arbusculares com espécies arbóreas tropicais. Rev Bras Cienc Solo 30:413–424
Rahman MA, Hasegawa H, Rahman MM et al (2007) Effect of arsenic on photosynthesis, growth and yield of five widely cultivated rice (Oryza sativa L.) varieties in Bangladesh. Chemosphere 67:1072–1079
Rahman MA, Hasegawa H, Rahman MM et al (2008) Straighthead disease of rice (Oryza sativa L.) induced by arsenic toxicity. Environ Exp Bot 62:54–59
Rosas-Castor JM, Guzman-Mar JL, Alfaro-Barbosa JM et al (2014) Evaluation of the transfer of soil arsenic to maize crops in suburban areas of San Luis Potosi, Mexico. Sci Total Environ 497:153–162
Rozpadek P, Wezowicz K, Stojakowska A et al (2014) Mycorrhizal fungi modulate phytochemical production and antioxidant activity of Cichorium intybus L. (Asteraceae) under metal toxicity. Chemosphere 112:217–224
Scandalios JG (2002) The rise of ROS. Trends Biochem Sci 27:483–486
Schneider J, Oliveira LM, Stürmer SL et al (2012) Espécies tropicais de pteridófitas em associação com fungos micorrízicos arbusculares em solo contaminado com arsênio. Quim Nova 35:709–714
Schneider J, Stürmer SL, LRG G et al (2013) Arbuscular mycorrhizal fungi in arsenic-contaminated areas in Brazil. J Hazard Mater 262:1105–1115
Schützendübel A, Polle A (2002) Plant responses to abiotic stresses: heavy metal induced oxidative stress and protection by mycorrhization. J Exp Bot 53:1351–1365
Shalaby AM (2003) Responses of arbuscular mycorrhizal fungal spores isolated from heavy metal-polluted and unpolluted soil to Zn, cd, Pb and their interactions in vitro. Pak J Biol Sci 6:1416–1422
Sharma I (2012) Arsenic induced oxidative stress in plants. Biologia 67:447–453
Shin H, Shin HS, Dewbre GR et al (2004) Phosphate transport in Arabidopsis: Pht1;1 and Pht1;4 play a major role in phosphate acquisition from both low- and high-phosphate environments. Plant J 39:629–642
Shri M, Kumar S, Chakrabarty D et al (2009) Effect of arsenic on growth, oxidative stress, and antioxidant system in rice seedlings. Ecotoxicol Environ Saf 72:1102–1110
Shrivastava M, Ma LQ, Singh N (2005) Antioxidant responses of hyper- accumulator and sensitive fern species to arsenic. J Exp Bot 56:335–1342
Singh N, Ma LQ, Shrivastava M et al (2006) Metabolic adaptation to arsenic-induced oxidative stress in Pteris vittata L and Pteris ensiformis L. Plant Sci 170:274–282
Singh HP, Batish DR, Kohli RK et al (2007) As induced root growth inhibition in mung bean is due to oxidative stress resulting from enhanced lipid peroxidation. Plant Growth Regul 53:65–73
Singh M, Singh VP, Dubey G et al (2015) Exogenous proline application ameliorates toxic effects of arsenate in Solanum melongena L. seedlings. Ecotoxicol Environ Saf 117:164–173
Smedley PL, Kinniburgh DG (2002) A review of the source, behavior and distribution of arsenic in natural waters. Appl Geochem 17:517–568
Smith SE, Read DJ (2008) Mycorrhizal symbiosis, 3rd edn. Academic Press, London
Smith SE, Christophersen HM, Pope S et al (2010) Arsenic uptake and toxicity in plants, integrating mycorrhizal influences. Plant Soil 327:1–21
Spagnoletti F, Lavado RS (2015) The arbuscular mycorrhiza Rhizophagus intraradices reduces the negative effects of arsenic on soybean plants. Agronomy 5:188–199
Spagnoletti FN, Tobar NE, Chiocchio VM et al (2014) The in-vitro and in-vivo influence of arsenic on arbuscular mycorrhizal fungi. In: Litter MI, Nicolli HB, Meichtry JM, Quici N, Bundschuh BP, Naidu R (eds) One century of the discovery of arsenicosis in Latin America (1914–2014) as 2014. CRC Press, London, pp 375–377
Spagnoletti F, Tobar N, Chiocchio V et al (2015) Mycorrhizal inoculation and high arsenic concentrations in the soil increase the survival of soybean plants subjected to strong water stress. Commun Soil Sci Plant Anal 46:2837–2846
Spagnoletti FN, Balestrasse K, Lavado RS et al (2016) Arbuscular mycorrhiza detoxifying response against arsenic and pathogenic fungus in soybean. Ecotoxicol Environ Saf 133:47–56
Spagnoletti F, Carmona M, Gómez NET et al (2017) Arbuscular mycorrhiza reduces the negative effects of M. phaseolina on soybean plants in arsenic-contaminated soils. Appl Soil Ecol 121:41–47
Stoeva N, Berova M, Zlatev Z (2004) Physiological response of maize to arsenic contamination. Biol Plant 47:449–452
Stoeva N, Berova M, Vassilev A et al (2005) Effect of exogenous polyamine diethylenetriamine on oxidative changes and photosynthesis in astreated maize plants (Zea mays L.). J Cent Eur Agric 6:367–374
Summers AO (2009) Damage control: regulating defenses against toxic metals and metalloids. Curr Opin Microbiol 12:138–144
Sýkorová Z, Ineichen K, Wiemken A et al (2007) The cultivation bias: different communities of arbuscular mycorrhizal fungi detected in roots from the field, from bait plants transplanted to the field, and from a greenhouse trap experiment. Mycorrhiza 18:1–14
Talano MA, Cejas RB, González PS et al (2013) Arsenic effect on the model crop symbiosis Bradyrhizobium-soybean. Plant Physiol Biochem 63:8–14
Talukdar D (2013) Arsenic induced changes in growth and antioxidant metabolism of fenugreek. Russ J Plant Physiol 60:652–660
Trivedi D, Gill SS, Yadav S et al (2013) Genome-wide analysis of glutathione reductase (GR) genes from rice and Arabidopsis. Plant Signal Behav 8:e23021. https://doi.org/10.4161/psb.23021
Ullrich-Eberius CI, Sanz A, Novacky AJ (1989) Evaluation of arsenate and vanadate-associated changes of electrical membrane potential and phosphate transport in Lemna gibba G1. J Exp Bot 40:119–128
Ultra VU, Tanaka S, Sakurai K et al (2007) Arbuscular mycorrhizal fungus (Glomus aggregatum) influences biotransformation of arsenic in the rhizosphere of sunflower (Helianthus annuus L.). J Soil Sci Plant Nutr 53:499–508
Vodnik D, Grcman H, Macek I, vanElteren JT, Kovacevic M (2008) The contribution of glomalin-related soil protein to Pb and Zn sequestration in polluted soil. Sci Total Environ 392:130–136
Wang S, Mulligan CN (2006) Occurrence of arsenic contamination in Canada: sources, behavior and distribution. Sci Total Environ 366(2–3):701–721
Wu FY, Ye ZH, Wonga MH (2009) Intraspecific differences of arbuscular mycorrhizal fungi in their impacts on arsenic accumulation by Pteris vittata L. Chemosphere 76:1258–1264
Xia YS, Chen BD, Christie P et al (2007) Arsenic uptake by arbuscular mycorrhizal maize (Zea mays L.) grown in an arsenic contaminated soil with added phosphorus. J Environ Sci 19:1245–1251
Xu PL, Christie P, Liu Y et al (2008) The arbuscular mycorrhizal fungus Glomus mosseae can enhance arsenic tolerance in Medicago truncatula by increasing plant phosphorus status and restricting arsenate uptake. Environ Pollut 156:215–220
Ye Y, Yuan J, Zhang SZ et al (2015) The phosphate transporter gene OsPht1;4 is involved in phosphate homeostasis in Rice. PLoS One 10:e0126186 https://doi.org/10.1371/journal.pone.0126186
Yu Y, Huang HL, Luo L et al (2009) Arsenic accumulation and speciation in maize as affected by inoculation with arbuscular mycorrhizal fungus Glomus mosseae. J Agric Food Chem 57:3695–3701
Zangaro W, Rostirola LV, de Souza PB et al (2013) Root colonization and spore abundance of arbuscular mycorrhizal fungi in distinct successional stages from an Atlantic rainforest biome in southern Brazil. Mycorrhiza 23:221–233
Zhang WD, Liu DS, Tian JC et al (2009) Toxicity and accumulation of arsenic in wheat (Triticum aestivum L.) varieties of China Phyton. Int J Exp Bot 78:147–154
Zhao FJ, Ma JF, Meharg AA et al (2009) Arsenic uptake and metabolism in plants. New Phytol 181:777–794
Zhou Y, Yao J, Choi M et al (2009) A combination method to study microbial communities and activities in zinc contaminated soil. J Hazard Mater 169:875–881
Zhu Y, Geng C, Tong Y et al (2006) Phosphate (pi) and arsenate uptake by two wheat (Triticum aestivum L.) cultivars and their doubled haploid lines. Ann Bot 98:631–636
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Spagnoletti, F.N., Lavado, R.S., Giacometti, R. (2018). Interaction of Plants and Arbuscular Mycorrhizal Fungi in Responses to Arsenic Stress: A Collaborative Tale Useful to Manage Contaminated Soils. In: Hasanuzzaman, M., Nahar, K., Fujita, M. (eds) Mechanisms of Arsenic Toxicity and Tolerance in Plants. Springer, Singapore. https://doi.org/10.1007/978-981-13-1292-2_10
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