Metal uptake, oxidative metabolism, and mycorrhization in pigeonpeaand pea under arsenic and cadmium stress

Presence of arsenic (As) and cadmium (Cd) at elevated levels in the soils is threatening agricultural productivity. Arbuscular mycorrhizae (AM) enhance plant resistance to metal(loid)s by sequestering them into roots, thus restricting their translocation into leaves. The present study evaluated differential responses of AM-colonized Cajanus cajan and Pisum sativum plants to As and Cd uptake and oxidative metabolism under As and Cd stress (0, 30, and 60 mg kg-1). Arsenic uptake was significantly higher than Cd uptake, which caused greater growth inhibitions and induced oxidative stress. Pea was more sensitive, with higher toxicity symptoms in roots than leaves. Mycorrhizae were tolerant to metal toxicity and formed stronger association with the roots of pigeonpea than pea. However, mycorrhization arrested metal(loid) uptake, reduced oxidative stress, and strengthened antioxidant enzyme activities. Stronger antioxidant enzyme activity and mycorrhizal symbiosis in pigeonpea when compared with pea could explain the differences in their metal(loid) tolerance.

Metal uptake, oxidative metabolism, and mycorrhization in pigeonpeaand pea under arsenic and cadmium stress

Presence of arsenic (As) and cadmium (Cd) at elevated levels in the soils is threatening agricultural productivity. Arbuscular mycorrhizae (AM) enhance plant resistance to metal(loid)s by sequestering them into roots, thus restricting their translocation into leaves. The present study evaluated differential responses of AM-colonized Cajanus cajan and Pisum sativum plants to As and Cd uptake and oxidative metabolism under As and Cd stress (0, 30, and 60 mg kg-1). Arsenic uptake was significantly higher than Cd uptake, which caused greater growth inhibitions and induced oxidative stress. Pea was more sensitive, with higher toxicity symptoms in roots than leaves. Mycorrhizae were tolerant to metal toxicity and formed stronger association with the roots of pigeonpea than pea. However, mycorrhization arrested metal(loid) uptake, reduced oxidative stress, and strengthened antioxidant enzyme activities. Stronger antioxidant enzyme activity and mycorrhizal symbiosis in pigeonpea when compared with pea could explain the differences in their metal(loid) tolerance.

___

Aebi H (1984). Catalase in vitro. In: Packer L, editor. Methods in Enzymology. Orlando, FL, USA: Academic Press, pp. 121–126.

Aibibu N, Liu Y, Zeng G, Wang X, Chen B, Song H, Xu L (2010). Cadmium accumulation in Vetiveria zizanioides and its effects on growth, physiological and biochemical parameters. Biores Technol 101: 6297–6303.

Al-Ghamdi AAM, Jais HM (2012). Interaction between arbuscular mycorrhiza and heavy metals in the rhizosphere and roots of Juniperus procera. Int J Agric Biol 14: 69–74.

Andrade SAL, Silveira APD, Jorge RA, de Abreu MF (2008). Cadmium accumulation in sunflower plants influenced by arbuscular mycorrhiza. Int J Phytoremed 10: 1–13.

AOAC (1990). Official Methods of Analysis of the Association of Official Analytical Chemists. Rockville, MD, USA: AOAC.

ATSDR (2007). U.S. Toxicological Profile for Cadmium. Atlanta, GA, USA: Centers for Disease Control and Prevention.

Azcón R, Peralvarez MDC, Biro B, Roldan A, Lozano JMR (2009). Antioxidant activities and metal acquisition in mycorrhizal plants growing in a heavy-metal multicontaminated soil amended with treated lignocellulosic agrowaste. Appl Soil Ecol 41: 168-177.

Bai JF, Lin XG, Yin R, Zhang HY, Wang JH, Chen XM, Luo YM (2008). The influence of arbuscular mycorrhizal fungi on As and P uptake by maize (Zea mays L.) from As contaminated soils. Appl Soil Ecol 38: 137–145.

Baker AJM, Ewart K, Hendry GAF, Thrope PC, Walker PL (1990). The evolutionary basis of cadmium tolerance in higher plants. In: 4th International Conference on Environmental Contamination. Barcelona, Spain, pp. 23–29.

Baroni F, Boscagli A, Di Lella LA, Protano G, Riccobono F (2004). Arsenic in soil and vegetation of contaminated areas in southern Tuscany (Italy). J Geochem Explor 81: 1–14.

Bhaduri AM, Fulekar MH (2012). Assessment of arbuscular mycorrhizal fungi on the phytoremediation potential of Ipomoea aquatica on cadmium uptake. Biotech 2: 193–198.

Bhattacharya S, Gupta K, Debnath S, Ghosh UC, Chattopadhyay D, Mukhopadhyay A (2012). Arsenic bioaccumulation in rice and edible plants and subsequent transmission through food chain in Bengal basin: a review of the perspectives for environmental health. Toxicol Environ Chem 94: 429–441.

Bolan N, Kunhikrishnan A, Thangarajan R, Kumpiene J, Park J, Makino T, Kirkham MB, Scheckel K (2014). Remediation of heavy metal(loid)s contaminated soils - To mobilize or to immobilize? J Hazard Mater 266: 141–166.

Bona E, Marsano F, Massa N, Cattaneo C, Cesaro P, Argese E, di Toppi LS, Cavaletto M, Berta G (2011). Proteomic analysis as a tool for investigating arsenic stress in Pteris vittata roots colonized or not by arbuscular mycorrhizal symbiosis. J Proteomics 74: 1338–1350.

Campos NV, Loureiro ME, Azevedo AA (2014). Differences in phosphorus translocation contributes to differential arsenic tolerance between plants of Borreria verticillata (Rubiaceae) from mine and non-mine sites. Environ Sci Pollut Res 24: 5586–5896.

Cao Q, Hu QH, Khan S, Wang ZJ, Lin AJ, Du X, Zhu YG (2007). Wheat phytotoxicity from arsenic and cadmium separately and together in solution culture and in a calcareous soil. J Hazard Mat 148: 377–382.

Castillo FI, Penel I, Greppin H (1984). Peroxidase release induced by ozone in Sedum album leaves. Plant Physiol 74: 846–851.

Chan WF, Li H, Wu FY, Wu SC, Wong MH (2013). Arsenic uptake in upland rice inoculated with a combination or single arbuscular mycorrhizal fungi. J Hazard Mater 262: 1116–1122.

Chapman HD, Pratt PF (1961). Methods of Analysis for Soil, Plant and Waters. Berkeley, CA, USA: University of California Division of Agriculture Science.

Chen B, Xiao X, Zhu YG, Smith FA, Xie ZM, Smith SE (2007). The arbuscular mycorrhizal fungus Glomus mosseae gives contradictory effects on phosphorus and arsenic acquisition by Medicago sativa Linn. Sci Total Environ 39: 226–234.

Chen XW, Wu FY, Li H, Chan WF, Wu C, Wu SC, Wong MH (2013). Phosphate transporters expression in rice (Oryza sativa L.) associated with arbuscular mycorrhizal fungi (AMF) colonization under different levels of arsenate stress. Environ Exp Bot 87: 92–99.

Cho SH, Chao YY, Hong CY, Kao CH (2012). The role of hydrogen peroxide in cadmium-inhibited root growth of rice seedlings. Plant Growth Regul 66: 27–35.

Clemens S (2006). Toxic metal accumulation, responses to exposure and mechanisms of tolerance in plants. Biochimie 88: 1707– 1719.

Christophersen HM, Smith FA, Smith SE (2009). Arbuscular mycorrhizal colonization reduces arsenate uptake in barley via downregulation of transporters in the direct epidermal phosphate uptake pathway. New Phytol 184: 962–974.

Christophersen HM, Smith FA, Smith SE (2012). Unraveling the influence of arbuscular mycorrhizal colonization on arsenic tolerance in Medicago: Glomus mosseae is more effective than G. intraradices, associated with lower expression of root epidermal Pi transporter genes. Front Physiol 3: 1–13.

DalCorso G, Farinati S, Furini A (2010). Regulatory networks of cadmium stress in plants. Plant Signal Behav 5: 663–667.

DalCorso G, Farinati S, Maistri S, Furini A (2008). How plants cope with cadmium: staking all on metabolism and gene expression. J Integ Plant Biol 50: 1268–1280.

Dalpé Y, Monreal M (2004). Arbuscular mycorrhiza inoculum to support sustainable cropping systems. Crop Manag 3: 1.

Danesh YR, Tajbakhsh M, Goltapeh EM, Varma A (2013) Mycoremediation of heavy metals. In: Goltapeh EM, Danesh YR, Varma A, editors. Fungi as Bioremediators. Soil Biology, Vol. 32. Berlin, Germany: Springer, pp. 245–267.

Dave R, Tripathi RD, Dwivedi S, Tripathi P, Dixit G, Sharma YK, Trivedi PK, Corpas FJ, Barroso JB, Chakrabarty D (2013). Arsenate and arsenite exposure modulate antioxidants and amino acids in contrasting arsenic accumulating rice (Oryza sativa L.) genotypes. J Hazard Mater 262: 1123–1131.

de Melo Rangel W, Schneider J, de SouzaCosta ET, Soares CRFS, Guilherme LRG, de Souza Moreira FM (2014). Phytoprotective effect of arbuscular mycorrhizal fungi species against arsenic toxicity in tropical leguminous species. Int J Phytorem 16: 840–858.

Deng X, Xia Y, Hu W, Zhang H, Shen Z (2010). Cadmium-induced oxidative damage and protective effects of N-acetyl-L-cysteine against cadmium toxicity in Solanum nigrum L. J Hazard Mater 180: 722–729.

Dhindsa RS, Plumb-Dhindsa P, Throne TA (1981). Leaf senescence: correlated with increased levels of membrane permeability and lipid peroxidation and decreased levels of superoxide dismutase and catalase. J Exp Bot 32: 93–101.

Dong Y, Zhu YG, Smith A, Wang CB (2008). Arbuscular mycorrhiza enhanced arsenic resistance off both white clover (Trifolium repens Linn.) and rye grass (Lolium perennee L.) plants in arsenic-contaminated soil. Environ Pollut 155: 174–181.

Duquesnoy I, Champeau GM, Evray G, Ledoigt G, Piquet-Pissaloux A (2010). Enzymatic adaptations to arsenic-induced oxidative stress in Zea mays and genotoxic effect of arsenic in root tips of Vicia faba and Zea mays. C R Biol 333: 814–824.

Elahi FE, Mridha MAU, Aminuzzaman FM (2010). Influence of AMF inoculation on growth, nutrient uptake, arsenic toxicity and chlorophyll content of eggplant grown in arsenic amended soil. Adv Natural Appl Sci 4: 184–192.

Engqvist LG, Martensson A, Orlowska E, Turnau K, Belimov AA, Borisov AY, Gianinazzi-Pearson V (2006). For a successful pea production on polluted soils, inoculation with beneficial microbes requires active interaction between the microbial components and the plant. Acta Agr Scand B-S P 56: 9–16.

Esteban E, Carpena RO, Meharg AA (2003). High-affinity phosphate/ arsenate transport in white lupine (Lupinus albus) is relatively insensitive to phosphate status. New Phytol 158: 165–173.

Ezawa T, Smith SE, Smith FA (2002). P metabolism and transport in AM fungi. Plant Soil 244: 221–230.

Garg N, Aggarwal N (2012). Effect of mycorrhizal inoculations on heavy metal uptake and stress alleviation of Cajanus cajan (L.) Millsp. genotypes grown in cadmium and lead contaminated soils. Plant Growth Regul 66: 9–26.

Garg N, Bhandari P (2012). Influence of cadmium stress and arbuscular mycorrhizal fungi on nodule senescence in Cajanus cajan (L.) Millsp. Int J Phytoremed 14: 62–74.

Garg N, Bhandari P (2014). Cadmium toxicity in crop plants and its alleviation by arbuscular mycorrhizal (AM) fungi: an overview. Plant Biosyst 148: 609–621.

Garg N, Chandel S (2012). Role of arbuscular mycorrhizal (AM) fungi on growth, cadmium uptake, osmolyte, and phytochelatin synthesis in Cajanus cajan (L.) Millsp. under NaCl and Cd stresses. J Plant Growth Regul 31: 292–308.

Garg N, Kaur H (2013a). Response of antioxidant enzymes, phytochelatins and glutathione production towards Cd and Zn stresses in Cajanus cajan (L.) Millsp. genotypes colonized by arbuscular mycorrhizal fungi. J Agro Crop Sci 199: 118–133.

Garg N, Kaur H (2013b). Impact of cadmium-zinc interactions on metal uptake, translocation and yield in pigeonpea genotypes colonized by arbuscular mycorrhizal fungi. J Plant Nutr 36: 67–90.

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 Hort 143: 92–101.

Gaur A, Adholeya A (2004). Prospects of arbuscular mycorrhizal fungi in phytoremediation of heavy metal contaminated soils. Curr Sci 86: 528–534.

Geng CN, Zhu YG, Hu Y, Williams P, Meharg AA (2006). Arsenate causes differential acute toxicity to two P-derived genotypes of rice seedlings (Oryza sativa L.). Plant Soil 279: 297–306.

Giasson P, Karam A, Jaouich A (2008). Arbuscular mycorrhizae and alleviation of soil stresses on plant growth. In: Siddiqui ZA, Akhtar MS, Futai K, editors. Mycorrhizae: Sustainable Agriculture and Forestry. London, UK: Springer, pp. 99–134.

Gomes MP, Carvalho M, Sáe Melo Marques TCLL, Duarte DM, de Oliveira Gonçalves Nogueira C, Soares AM, de Souza Garcia Q (2012). Arsenic-sensitivity in Anadenanthera peregrina due to arsenic-induced lipid peroxidation. Int J App Sci Technol 2: 55–63.

González-Chávez MC, Carrillo-Gonzalez R, Gutierrez-Castorena MC (2009). Natural attenuation in a slag heap contaminated with cadmium: the role of plants and arbuscular mycorrhizal fungi. J Hazard Mater 161: 1288–1298.

González-Chávez MDCA, Miller B, Maldonado-Mendoza IE, Scheckel K, Carrillo-González R (2014). Localization and speciation of arsenic in Glomus intraradices by synchrotron radiation spectroscopic analysis. Fungal Biol 118: 444–452.

Gresser MJ (1981). ADP-arsenate formation by sub-mitochondrial particles under phosphorylating conditions. J Biol Chem 256: 5981–5983.

Grİnlund M, Albrechtsen M, Johansen IE, Hammer EC, Nielsen TH, Jakobsen I (2013). The interplay between P uptake pathways in mycorrhizal peas: a combined physiological and gene-silencing approach. Physiol Plant 149: 234–248.

Gunes A, Pilbeam DJ, Inal A (2009). Effect of arsenic-phosphorous interaction on arsenic-induced oxidative stress in chickpea plants. Plant Soil 314: 211–220.

Harrison MJ, Dewbre GR, Liu J (2002). A phosphate transporter from Medicago truncatula involved in the acquisition of phosphate released by arbuscular mycorrhizal fungi. Plant Cell 14: 2413–2429.

Hatata MH, Abdel-Aal EA (2008) Oxidative stress and antioxidant defense mechanisms in response to cadmium treatments. Am- Euras J Agric Environ Sci 4: 655–669.

Heath RL Packer I (1968). Photoperoxidation in isolated chloroplast: I. Kinetics and stoichiometry of fatty acid peroxidation. Arch Biochem Biophys 125: 189–198.

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

Ishtiaq S, Mahmood S (2011). Phytotoxicity of nickel and its accumulation in tissues of three Vigna species at their early growth stages. J App Bot Food Qual 84: 223–228.

Jankong P, Visoottiviseth P (2008). Effects of arbuscular mycorrhizal inoculation on plants growing on arsenic contaminated soil. Chemosphere 72: 1092–1097.

Janoušková M, Vosatka M, Rossi L, Lugon-Moulin, N (2007). Effects of arbuscular mycorrhizal inoculation on cadmium accumulation by different tobacco (Nicotiana tabacum L.) types. Appl Soil Ecol 35: 502–510.

Jia Y, Huang H, Sun G, Zhao FJ (2012). Pathways and relative contributions to arsenic volatilization from rice plants and paddy soil. Environ Sci Technol 46: 8090–8096.

Joner EJ, Briones R, Levyal C (2000). Metal-binding capacity of arbuscular mycorrhizal mycelium. Plant Soil 226: 227–234.

Kapoor R, Bhatnagar AK (2007). Attenuation of cadmium toxicity in mycorrhizal celery (Apium graveolens L.). World J Microbiol Biotechnol 23: 1083–1089.

Khade SW, Adholeya A (2009). Arbuscular mycorrhizal association in plants growing on metal-contaminated and non-contaminated soils adjoining Kanpur tanneries, Uttar Pradesh, India. Water Air Soil Pollut 202: 45–56.

Krüger C (2013). Arbuscular mycorrhizal fungi for reforestation of native tropical trees in the Andes of South Ecuador. PhD, Ludwig Maximilian University of Munich, Munich, Germany.

Lee DA, Chen A, Schroeder JI (2003). Ars1, an Arabidopsis mutant exhibiting increased tolerance to arsenate and increased phosphate uptake. Plant J 35: 637–646.

Lee JT, Yu WC (2012). Evaluation of legume growth in arsenic- polluted acidic soils with various pH values. J Water Sustain 2: 13–23.

Lindner RC (1944). Rapid analytical method for some of the more in organic constituents of plants tissue. Plant Physiol 19: 76–89.

Lingua G, Franchin C, Todeschini V, Castiglione S, Biondi S, Burlando B, Parravicini V, Torrigiani P, Berta G (2008). Arbuscular mycorrhizal fungi differentially affect the response to high zinc concentrations of two registered poplar clones. Environ Pollut 153: 137–147.

Liu LZ, Gong ZQ, Zhang YL, Li PJ (2011). Growth, cadmium accumulation and physiology of marigold (Tagetes erecta L.) as affected by arbuscular mycorrhizal fungi. Pedosphere 21: 319-327.

Liu Y, Li M, Han C, Wu F, Tu B, Yang P (2013) Comparative proteomic analysis of rice shoots exposed to high arsenate. J Integr Plant Biol 55: 1–14.

Liu YT, Chen ZS, Hong CY (2011). Cadmium-induced physiological response and antioxidant enzyme changes in the novel cadmium accumulator, Tagetes patula. J Hazard Mater 189: 724–731.

Luan ZQ, Cao HC, Yan BX (2008). Individual and combined phytotoxic effects of cadmium, lead and arsenic on soybean in Phaeozem. Plant Soil Environ 54: 403–411.

McGonigle TP, Millers MH, Evans DG, Fairchild GL, Swan JA (1990). A new method which gives an objective measure of colonization of roots by vesicular-arbuscular mycorrhizal fungi. New Phytol 115: 495–501.

Meharg AA (2005). Mechanisms of plant resistance to metal and metalloid ions and potential biotechnological applications. Plant Soil 274: 163–174.

Mehlich A (1953). Determination of P, Ca, Mg, K, Na and NH4. Short Test Methods Used in Soil Testing Division. Raleigh, NC, USA: North Carolina State University Department of Agriculture.

Metwally A, Safronova VI, Belimov AA, Dietz KJ (2005). Genotypic variation of the response to cadmium toxicity in Pisum sativum L. J Exp Bot 56: 167–178.

Miransari M (2010). Contribution of arbuscular mycorrhizal symbiosis to plant growth under different types of soil stress. Plant Biol 12: 563–569.

Miransari M (2011). Hyperaccumulators, arbuscular mycorrhizal fungi and stress of heavy metals. Biotechnol Advan 29: 645– 653.

Miyasaka SC, Habte M, Friday JB, Johnson EV (2003). Manual on Arbuscular Mycorrhizal Fungus Production and Inoculation Techniques. Honolulu, HI, USA: University of Hawaii.

Mukhopadhyay R, Rosen BP, Phung LT, Siver S (2002). Microbial arsenic: from geocycle to gene and enzymes. FEMS Microbiol Rev 26: 311–325.

Muleta D, Woyessa D (2012). Importance of arbuscular mycorrhizal fungi in legume production under heavy metal-contaminated soils. In: Zaidi A, Wani PA, Khan MS, editors. Toxicity of Heavy Metals to Legumes and Bioremediation. London, UK: Springer, pp. 219–241.

Nelson DW, Sommers LE (1973). Determination of total nitrogen in plant material. Agron J 65: 109–112.

Nguyen QTT, Huang TL, Huang HJ (2014). Identification of genes related to arsenic detoxification in rice roots using microarray analysis. Int J Biosci Biochem Bioinfor 4: 22–27.

Olsen SR, Sommers LE (1982). Phosphorus. In: Page AL, editor. Methods of Soil Analysis, No. 9, Part 2 - Chemical and Microbiological Properties. 2nd ed. Madison, WI, USA: American Society of Agronomy, pp. 403–430.

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.

Ouzounidou G, Eleftheriou EF, Karataglis S (1992). Ecophysiological and ultrastructural effects of copper in Thlaspi ochroleucum (Cruciferae). Can J Bot 70: 947–957.

Ovečka M, Takáč T (2014). Managing heavy metal toxicity stress in plants: biological and biotechnological tools. Biotech Adv 32: 73–86.

Pajuelo E, Rodriguez-Llorente ID, Lafuente A, Caviedes MA (2011). Legume-Rhizobium symbiosis as a tool for bioremediation of heavy metal polluted soils. In: Khan MS, Zaidi A, Goel R, Musarrat J, editors. Biomanagement of Metal-Contaminated Soils. London, UK: Springer, pp. 95–123.

Pant PP, Tripathi AK, Dwivedi V (2011). Effect of heavy metals on some biochemical parameters of Sal (Shorea robusta) seedling at nursery level, Doon Valley, India. J Agri Sci 2: 45–51.

Peralta-Videaa JR, Lopeza ML, Narayana M, Saupea G, Gardea- Torresdey J (2009). The biochemistry of environmental heavy metal uptake by plants: Implications for the food chain. Int J Biochem Cell Biol 41: 1665–1677.

Phillips JM, Hayman DS (1970). Improved procedures for clearing and staining parasitic and vesicular-arbuscular mycorrhizal fungi for rapid assessment of infection. T Brit Mycol Soc 55: 158–161.

Pichardo ST, Su Y, Han FX (2012). The potential effects of arbuscular mycorrhizae (AM) on the uptake of heavy metals by plants from contaminated soils. J Bioremed Biodeg 3: 10.

Pigna M, Cozzolino V, Giandonato Caporale A, Mora ML, Di Meo V, Jara AA, Violante A (2010). Effects of phosphorus fertilization on arsenic uptake by wheat grown in polluted soils. J Soil Sci Plant Nutr 10: 428–442.

Piršelová B, Kuna R, Libantová J, Moravčíková J, Matušíková I (2011). Biochemical and physiological comparison of heavy metal-triggered defense responses in the monocot maize and dicot soybean roots. Mol Biol Rep 38: 3437–3446.

Ramos I, Esteban E, Lucena JJ, Garate A (2002). Cadmium uptake and subcellular distribution in plants of Lactica sp. Cd-Mn interaction. Plant Sci 162: 761–767.

Redon PO, Beguiristain T, Leyval C (2009). Differential effects of AM fungal isolates on Medicago truncatula and metal uptake in a multimetallic (Cd, Zn, Pb) contaminated agricultural soil. Mycorrhiza 19: 187–195.

Rellán-Álvarez R, Ortega-Villasante C, Álvarez-Fernández A, del Campo FF, Hernández LE (2006). Stress responses of Zea mays to cadmium and mercury. Plant Soil 279: 41–50.

Repetto O, Massa N, Gianinazzi-Pearson V, Dumas-Gaudot E, Berta G (2007). Cadmium effects on populations of root nuclei in two pea genotypes inoculated or not with the arbuscular mycorrhizal fungus Glomus mosseae. Mycorrhiza 17: 111–120.

Rivera-Becerril F, Calantzis C, Turnau K, Caussanel J, 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: 1177–1185.

Romero-Puertas MC, Palma JM, Gomez LA, del Rio LA, Sandalio LM (2002). Cadmium causes oxidative modification of proteins in plants. Plant Cell Environ 25: 677–686.

Saraswat S, Rai JPN (2011). Mechanism of metal tolerance and detoxification in mycorrhizal fungi. In: Khan MS, Zaidi A, Goel R, Musarrat J, editors. Biomanagement of Metal-Contaminated Soils. London, UK: Springer, pp. 225–240.

Schmidt AC, Mattusch J, Reisser W, Wennrich R (2004). Uptake and accumulation behavior of angiosperms irrigated with solution of different arsenic species. Chemosphere 56: 305–331.

Schneider J, Stürmer SL, Guilherme LRG, de Souza Moreira FM, de Sousa Soares CRF (2013). Arbuscular mycorrhizal fungi in arsenic-contaminated areas in Brazil. J Hazard Mater 262: 1105–1115.

Schützendübel A, Schwanz P, Teichmann T, Gross K, Langenfeld- Heyser R, Godbold DL, Polle A (2001). Cadmium-induced changes in antioxidative systems, hydrogen peroxide content, and differentiation in Scots pine roots. Plant Physiol 127: 887– 898.

Shao Y, Jiang LN, Zhang DJ, Ma LJ, Li CX (2011). Effects of arsenic, cadmium and lead on growth and respiratory enzymes activity in wheat seedlings. Afr J Agric Res 6: 4505–4512.

Sharma I (2013) Arsenic stress in plants: an inside story. In: Hakeem KR, Ahmad P, Ozturk M, editors. Crop Improvement. Berlin, Germany: Springer Science + Business Media, pp. 379–400.

Shri M, Kumar S, Chakrabarty D, Trivedi PK, Mallick S, Misra P, Shukla D, Mishra S, Srivastava S, Tripathi RD et al. (2009). Effect of arsenic on growth, oxidative stress, and antioxidant system in rice seedlings. Ecotoxicol Environ Saf 72: 1102–1110.

Singh N, Ma LQ, Srivastava M, Rathinasabapathi B. (2006). Metabolic adaptations to arsenic induced oxidative stress in Pteris vittata L. and Pteris ensiformis L. Plant Sci. 170: 274–282.

Singh S, Eapen S, D’Souza SF. (2006). Cadmium accumulation and its influence on lipid peroxidation and antioxidative system in an aquatic plant, Bacopa monnieri L. Chemosphere 61: 233-246.

Smeets K, Ruytinx J, Semane B, Belleghem FV, Remans T, Sanden SV, Vangronsveld J, Cuypers A (2008). Cadmium-induced transcriptional and enzymatic alterations related to oxidative stress. Environ Exp Bot 63: 1–8.

Smith SE, Read DJ (2008). Mycorrhizal Symbiosis. New York, NY, USA: Academic Press.

Sobrino-Plata J,  Carrasco-Gil S,  Abadía J,  Escobar C,  Álvarez- Fernández A,  Hernández LE (2014). The role of glutathione in mercury tolerance resembles its function under cadmium stress in Arabidopsis. Metallomics 6: 356–366.

Srivastava S, Sharma YK (2013) Impact of arsenic toxicity on black gram and its amelioration using phosphate. Toxicology 2013: 340925.

Stoeva N, Berova M, Zlatez Z (2005). Effect of arsenic on some physiological parameters in bean plants. Biol Planta 49: 293– 296.

Sun Y, Zhou Q, Diao C (2008). Effects of cadmium and arsenic on growth and metal accumulation of Cd-hyperaccumulator Solanum nigrum L. Biores Technol 99: 1103–1110.

Sun Y, Zhou Q, Liu W, An J, Xu ZQ, Wang L (2009). Joint effects of arsenic and cadmium on plant growth and metal bioaccumulation: a potential Cd-hyperaccumulator and As- excluder Bidens pilosa L. J Hazard Mat 165: 1023–1028.

Talukdar D (2013). Arsenic-induced oxidative stress in the common bean legume, Phaseolus vulgaris L. seedlings and its amelioration by exogenous nitric oxide. Physiol Mol Biol Plants 19: 69–79.

Tang T, Miller DM (1991). Growth and tissue composition of rice grown in soil treated with inorganic copper, nickel and arsenic. Commu Soil Sci Plant Anal 22: 2037–2045.

Tiwari M, Sharma D, Dwivedi S, Singh M, Tripathi RD, Trivedi PK (2014). Expression in Arabidopsis and cellular localization reveal involvement of rice NRAMP, OsNRAMP1, in arsenic transport and tolerance. Plant Cell Environ 37: 140–152.

Tu S, Ma LQ (2003). Effects of arsenate and phosphate on their accumulation by an arsenic-hyperaccumulator Pteris vittata L. Plant Soil 249: 373–382.

Ultra VU Jr, Tanaka S, Sakurai K, Iwasaki K (2007). Effects of arbuscular mycorrhiza and phosphorus application on arsenic toxicity in sunflower (Helianthus annuus L.) and on the transformation of arsenic in the rhizosphere. Plant Soil 290: 29–41.

Upadhyaya H, Panda SK, Bhattacharjee MK, Dutta S (2010). Role of arbuscular mycorrhiza in heavy metal tolerance in plants: prospects for phytoremediation. J Phytol 2: 16–27.

Vallino M, Massa N, Lumini E, Bianciotto V, Berta G, Bonfante P (2006). Assessment of arbuscular mycorrhizal fungi diversity in roots of Solidago gigantean growing in a polluted soil in Northern Italy. Environ Microbiol 8: 971–983.

Velikova V, Yordanov I, Edreva A (2000). Oxidative stress and some antioxidant systems in acid rain-treated bean plants. Plant Sci 151: 59–66.

Verbruggen N, Hermans C, Schat H (2009). Mechanisms to cope with arsenic or cadmium excess in plants. Curr Opin Plant Biol 12: 1–9.

Vogel-Mikuš K, Regvar M (2006). Arbuscular mycorrhiza as a tolerance strategy in metal contaminated soils: prospects in phytoremediation. In: Rodes D, editor. New Topics in Environmental Research. Hauppauge, NY, USA: Nova Science Publishers, pp. 37–56.

Walkley A (1947). A critical examination of a rapid method for determining organic carbon in soils: effects of variations in digestion conditions and of organic soil constituents. Soil Sci 63: 251–263.

Wang ZH, Zhang JL, Christie P, Li XL (2008). Influence of inoculation with Glomus mosseae or Acaulospora morrowiae on arsenic uptake and translocation by maize. Plant Soil 311: 235–244.

Wu F, Hu J, Wu S, Wong MH (2013). Grain yield and arsenic uptake of upland rice inoculated with arbuscular mycorrhizal fungi in As-spiked soils. Environ Sci Pollut Res (in press).

Xu PL, Christie P, Liu Y, Zhang JL, Li XL (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.

Yu Y, Zhang S, Huang H, Luo L, Wen B (2009). Arsenic accumulation and speciation in maize as affected by inoculation with arbuscular mycorrhizal fungus Glomus mosseae. J Agric Food Chem 57: 3695–3701.

Zaefarian F, Rezvani M, Ardakani MR, Rejali F, Miransari M (2013). Impact of mycorrhizae formation on the phosphorus and heavy-metal uptake of alfalfa. Comm Soil Sci Plant Anal 44: 1340–1352.

Zavala YJ, Duxbury JM (2008). Arsenic in rice: I. Estimating normal levels of total arsenic in rice grain. Environ Sci Technol 42: 3856–3860.

Zhao FJ, McGrath SP, Meharg AA (2010) Arsenic as a food chain contaminant: Mechanisms of plant uptake and metabolism and mitigation strategies. Annu Rev Plant Biol 61: 535–559.

Turkish Journal of Agriculture and Forestry-Cover
  • ISSN: 1300-011X
  • Yayın Aralığı: Yılda 6 Sayı
  • Yayıncı: TÜBİTAK
Sayıdaki Diğer Makaleler

The response to bacterial inoculation is cultivar-related in strawberries

JELENA M. TOMIC, JASMINKA M. MILIVOJEVIC, MARIJANA I. PESAKOVIC

N-acetylcysteine increased rice yield

Mohd NOZULAIDI, Md Sarwar JAHAN, Mohd KHAIRI, Mohammad Moneruzzaman KHANDAKER, Mat NASHRIYAH, Yusop Mohd KHANIF

Species-specifc growth and photosynthetic responses of frst-year seedlings of four coniferous species to open-feld experimental warming

Sun Jeoung LEE, Tae Kyung YOON, Jongyeol LEE, Saerom HAN, Seung Hyun HAN, Seongjun KIM, Jaehong HWANG, Min Seok CHO, Yowhan SON

Emissions of volatile organic compounds from lacquer coatings used in the furniture industry, modified with nanoparticles of inorganic metal compounds

Agata Stachowiak WENCEK, Magdalena ZBOROWSKA, Wlodzimierz PRADZYNSKI, Boguslawa WALISZEWSKA

Assessment of fruit characteristics and genetic variation among naturally growingwild fruit Elaeagnus angustifolia accessions

Aydın UZUN, AYDIN UZUN, BUKET ÇELİK, TURAN KARADENİZ, KADİR UĞURTAN YILMAZ, Kadir Uğurtan YILMAZ, CAFER ALTINTAŞ

Neera GARG, Priyanka SINGLA, Purnima BHANDARI

Auxin-mediated growth of rice in cadmium-contaminated soil

Hussna FAROOQ, Hafiz Naeem ASGHAR, Muhammad Yahya KHAN, Muhammad SALEEM, Zahir Ahmad ZAHIR

Comparative analysis of genetic diversity among Chinese watermelon germplasmsusing SSR and SRAP markers, and implications for future genetic improvement

PANGQIAO WANG, QIONG LI, Jianbin Hu, YAN SU

Genetic variability and relationship studies in new Indian papaya (Carica papaya L.) germplasm using morphological and molecular markers

PARMESHWAR LAL SARAN, RAVISH CHOUDHARY, ISHWAR SINGH SOLANKI, PRAVIN PATIL, SANJAY KUMAR

Genetic variation in wheat germplasm for salinity tolerance atseedling stage: improved statistical inference

Babar HUSSAIN, Abdus Salam KHAN, Zulfiqar ALI