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Role of Arbuscular Mycorrhizal (AM) Fungi on Growth, Cadmium Uptake, Osmolyte, and Phytochelatin Synthesis in Cajanus cajan (L.) Millsp. Under NaCl and Cd Stresses

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Abstract

Application of phosphatic (P) fertilizers and biosolids is known to enhance cadmium (Cd) contamination in saline soils. Increased concentration of dissolved chloride (Cl−) in soil solution significantly influences Cd bioavailability in P fertilizer- or biosolid-amended soils. Arbuscular mycorrhizal (AM) fungi have an ability to protect plants against salinity and heavy metals by mediating interactions between toxic ions and plant roots. The effects of Glomus mosseae (AM) and NaCl and Cd stresses on Cd uptake and osmolyte and phytochelatin (PCs) synthesis in Cajanus cajan (L.) Millsp. (pigeonpea) were studied under greenhouse conditions. Two genotypes [Sel 85 N (tolerant) and ICP 13997 (sensitive)] were subjected to NaCl (4 and 6 dS m−1) and Cd (CdCl2, 25 and 50 mg kg−1 dry soil) treatments. NaCl and Cd applied individually as well as in combination caused dramatic reductions in plant biomass and induced membrane peroxidation, ionic perturbations, and metabolite synthesis in both genotypes, although Sel 85 N was less affected than ICP 13997. Cadmium uptake was enhanced when NaCl was added along with Cd. The protection of growth in Sel 85 N was associated with restricted accumulation of Na+, Cl−, and Cd2+ and higher concentrations of stress metabolites (sugars, proteins, free amino acids, proline, glycine betaine). Cd led to a significant increase in biothiols (NP-SH) and glutathione (GSH), with a larger pool of NP-SH which strongly induced accumulation of phytochelatins, whereas no significant effects in their concentrations were detectable under NaCl stress. The interactive effects of NaCl and Cd on all parameters were larger than those of individual treatments. Fungal inoculations improved plant growth and reduced accumulation of toxic ions. Higher stress metabolite synthesis and PCs observed in AM plants of Sel 85 N indicated the role of an efficient AM symbiosis capable of attenuating NaCl and Cd stresses.

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References

  • Anderson ME (1985) Determination of glutathione and glutathione disulfides in biological samples. Methods Enzymol 113:548–570

    Article  PubMed  CAS  Google Scholar 

  • Andrade SAL, Silveira APD (2008) Mycorrhiza influence on maize development under Cd stress and P supply. Braz J Plant Physiol 20(1):39–50

    Article  Google Scholar 

  • Andrade SAL, Gratao PL, Schiavinato SMA, Silveira APD, Azevodo RA, Mazzafera P (2009) Zn uptake, physiological response and stress attenuation in mycorrhizal jack bean growing in soil with increasing concentrations. Chemosphere 75:1363–1370

    Article  PubMed  CAS  Google Scholar 

  • AOAC (1990) Official method of analysis of the association of official analytical chemists, 15th edn, vol 1. Association of Analytical Chemists, Arlington

  • Arnon DI (1949) Copper enzymes in isolated chloroplasts. Polyphenyloxidase in Beta vulgaris. Plant Physiol 24:1–15

    Article  PubMed  CAS  Google Scholar 

  • Aydi S, Sassi S, Abdelly C (2008) Growth, nitrogen fixation and ion distribution in Medicago truncatula subjected to salt stress. Plant Soil 312:59–67

    Article  CAS  Google Scholar 

  • Azcon R, Medina A, Roldan A, Biro B, Vivas A (2009) Significance of treated agrowaste residue and autochthonous inoculates (arbuscular mycorrhizal fungi and Bacillus cereus) on bacterial community structure and phytoextraction to remediate soils contaminated with heavy metals. Chemosphere 75:327–334

    Article  PubMed  CAS  Google Scholar 

  • Azevedo Neto ADA, Prisco JT, Gomes-Filho E (2009) Changes in soluble amino-N, soluble proteins and free amino acids in leaves and roots of salt-stressed maize genotypes. J Plant Interact 4(2):137–144

    Article  CAS  Google Scholar 

  • Bates LS, Waldran RP, Teare ID (1973) Rapid determination of free proline for water studies. Plant Soil 39:205–208

    Article  CAS  Google Scholar 

  • Beltrano J, Ronco MG (2008) Improved tolerance of wheat plants (Triticum aestivum L.) to drought stress and rewatering by the arbuscular mycorrhizal fungus Glomus claroideum: effect on growth and cell membrane stability. Braz J Plant Physiol 20(1):29–37

    Article  CAS  Google Scholar 

  • Bhargava P, Srivastava AK, Urmil S, Rai LC (2005) Phytochelatin plays a role in UV-B tolerance in N2-fixing cyanobacterium Anabaena doliolum. J Plant Physiol 162:1220–1225

    Article  PubMed  CAS  Google Scholar 

  • Bradford MM (1976) A rapid and sensitive method for the quantification of microgram quantities of protein utilizing the principle of protein dye-binding. Anal Biochem 72:248–254

    Article  PubMed  CAS  Google Scholar 

  • Chapman HD, Pratt PF (1961) Methods of analysis for soil plant and waters. Division of Agricultural Sciences, University of California, Berkley

    Google Scholar 

  • Chen S, Li J, Wang S, Huttermann A, Altman A (2001) Salt, nutrient uptake and transport and ABA of Populus euphratica; a hybrid in response to increasing soil NaCl. Trees Struct Funct 15:186–194

    Article  CAS  Google Scholar 

  • Colla G, Rouphael Y, Cardarelli M, Tullio M, Rivera CM, Rea E (2008) Alleviation of salt stress by arbuscular mycorrhizal in zucchini plants grown at low and high phosphorus concentration. Biol Fertil Soils 44:501–509

    Article  CAS  Google Scholar 

  • Dal Corso G, Farinati S, Maistri S, Furini A (2008) How plants cope with cadmium: Staking all on metabolism and gene expression. J Integr Plant Biol 50(10):1268–1280

    Article  CAS  Google Scholar 

  • Del Longo OT, Gonzalez CA, Pastori GM, Tripps VS (1993) Antioxidant defenses under hyperoxygenic and hyperosmotic conditions in leaves of two lines of maize with differential sensitivity to drought. Plant Cell Physiol 34:1023–1028

    CAS  Google Scholar 

  • FAO (2008) FAO land and plant nutrition management service. http://www.fao.org/ag/agl/ahll/spush. Accessed 13–15 May 2008

  • Feng J, Shi Q, Wang X, Wei M, Yang F, Xu H (2010) Silicon supplementation ameliorated the inhibition of photosynthesis and nitrate metabolism by cadmium (Cd) toxicity in Cucumis sativus L. Sci Hortic 123:521–530

    Article  CAS  Google Scholar 

  • Franzini VI, Azcon R, Mendes FL, Aroca R (2009) Interactions between Glomus species and Rhizobium affect the nutritional physiology of drought-stressed legume hosts. J Plant Physiol 167(8):614–619

    Article  PubMed  Google Scholar 

  • Gabrijel O, Davor R, Zed R, Marija R, Monika Z (2009) Cadmium accumulation by muskmelon under salt stress in contaminated organic soil. Sci Total Environ 407:2175–2182

    Article  PubMed  CAS  Google Scholar 

  • Garg N, Aggarwal N (2011) Effects of interactions between cadmium and lead on growth, nitrogen fixation, phytochelatin, and glutathione production in mycorrhizal Cajanus cajan (L.) Millsp. J Plant Growth Regul 30:286–300

    Article  CAS  Google Scholar 

  • Garg N, Chandel S (2010) Arbuscular mycorrhizal networks: process and functions. A review. Agron Sustain Dev 30(3):581–599

    Article  CAS  Google Scholar 

  • Garg N, Manchanda G (2009) Role of arbuscular mycorrhizae in the alleviation of ionic, osmotic and oxidative stresses induced by salinity in Cajanus cajan (L.) Millsp. (pigeonopea). J Agron Crop Sci 195(2):110–123

    Article  CAS  Google Scholar 

  • Giri B, Kapoor R, Mukerji KG (2007) Improved tolerance of Acacia nilotica to salt stress by arbuscular mycorrhiza, Glomus fasciculatum may be partly related to elevated K/Na ratios in root and shoot tissues. Microb Ecol 54:753–760

    Article  PubMed  CAS  Google Scholar 

  • Greive CM, Grattan SR (1983) Rapid assay for determination of water soluble quaternary–amino compounds. Plant Soil 70:303–307

    Article  Google Scholar 

  • Grewal HS (2010) Water uptake, water use efficiency, plant growth and ionic balance of wheat, barley, canola and chickpea plants on a sodic vertosol with variable subsoil NaCl salinity. Agric Water Manag 97:148–156

    Article  Google Scholar 

  • Hajiboland R, Aliasgharzadeh N, Laiegh SF, Poschenrieder C (2010) Colonization with arbuscular mycorrhizal fungi improves salinity tolerance of tomato (Solanum lycopersicum L.) plants. Plant Soil 331:313–327

    Article  CAS  Google Scholar 

  • Hajlaoui H, Ayeb NE, Garrec JP, Denden M (2010) Differential effects of salt stress on osmotic adjustment and solutes allocation on the basis of root and leaf tissue senescence of two silage maize (Zea mays L.) varieties. Indust Crops Prod 31:122–130

    Article  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Hillocks RJ, Minja E, Nahdy MS, Subrahmanyam P (2000) Diseases and pests of pigeonpea in eastern Africa. Int J Pest Manag 46:7–18

    Article  Google Scholar 

  • Hiscox TD, Israelstam GF (1979) A method for extraction of chlorophyll from leaf tissue without maceration. Can J Bot 57:1331–1334

    Article  Google Scholar 

  • Irigoyen JJ, Emerich DW, Sanchez-Diaz M (1992) Water stress induced changes in concentrations of proline and total soluble sugars in nodulated alfalfa (Medicago sativa) plants. Physiol Plant 84:55–60

    Article  CAS  Google Scholar 

  • Katerji N, Mastrorilli M, van Hoorn JW, Lahmer FZ, Hamdy A, Owies T (2009) Durum wheat and barley productivity in saline-drought environments. Eur J Agron 31:1–19

    Article  Google Scholar 

  • Kaya C, Ashraf M, Sonmez O, Aydemir S, Tuna AL, Cullu MA (2009) The influence of arbuscular mycorrhizal colonization on key growth parameters and fruit yield of pepper plants at high salinity. Sci Hortic 121:1–6

    Article  CAS  Google Scholar 

  • Khade SW, Adholeya A (2007) Feasible bioremediation through arbuscular mycorrhizal fungi imparting heavy metal tolerance: a retrospective. Biorem J 11(1):33–43

    Article  CAS  Google Scholar 

  • Khan MN, Siddiqui MH, Mohammad F, Naeem M, Khan MA (2010) Calcium chloride and gibberellic acid protect linseed (Linum usitatissimum L.) from NaCl stress by inducing antioxidative defence system and osmoprotectant accumulation. Acta Physiol Plant 32:121–132

    Article  Google Scholar 

  • Khudsar T, Mahmooduzzafar Iqbal M (2001) Cadmium-induced changes in leaf epidermis, photosynthetic rate and pigment concentrations in Cajanus cajan. Boil Plant 44(1):59–64

    Article  CAS  Google Scholar 

  • Kolb D, Muller M, Zelling G, Zechmann (2010) Cadmium induced changes in subcellular glutathione contents within glandular trichomes of Cucurbita pepo L. Protoplasma 243:87–94

    Article  PubMed  CAS  Google Scholar 

  • Lee YP, Takashi T (1966) An improved colorimetric determination of amino acids with the use of ninhydrin. Anal Biochem 14:71–77

    Article  CAS  Google Scholar 

  • Lin R, Wang X, Luo Y, Du W, Guo H, Yin D (2007) Effects of soil cadmium on growth, oxidative stress and antioxidant system in wheat seedlings (Triticum aestivum L.). Chemosphere 69:89–98

    Article  PubMed  CAS  Google Scholar 

  • Lopez-Chuken UJ, Young SD, Sanchez-Gonzalez MN (2009) The use of chlorocomplexation to enhance Cd uptake by Zea mays and Brassica juncea: evaluating a ‘free ion activity model’ and implications for phytoremediation. Int J Phytorem 12(7):680–696

    Article  Google Scholar 

  • Lopez-Chuken UJ, Young SD, Guzman-Mar JL (2010) Evaluating a ‘biotic ligand model’ applied to chloride-enhanced Cd uptake by Brassica juncea from nutrient solution at constant Cd2+ activity. Environ Technol 31(3):307–318

    Article  PubMed  CAS  Google Scholar 

  • Manchanda G, Garg N (2011) Alleviation of salt-induced ionic, osmotic and oxidative stresses in Cajanus cajan nodules by AM inoculation. Plant Biosyst 145(1):88–97

    Article  Google Scholar 

  • Manousaki E, Kalogerakis N (2009) Phytoextraction of Pb and Cd by the Mediterranean saltbush (Atriplex halimus L.): metal uptake in relation to salinity. Environ Sci Pollut Res 16:844–854

    Article  CAS  Google Scholar 

  • Miransari M (2010) Contribution of arbuscular mycorrhizal symbiosis to plant growth under different types of soil stress. Plant Biol (Stuttg) 12(4):563–569

    CAS  Google Scholar 

  • Monteiro MS, Santos C, Soares AMVM, Mann RM (2009) Assessment of biomarkers of cadmium stress in lettuce. Ecotoxicol Environ Saf 72:811–818

    Article  PubMed  CAS  Google Scholar 

  • Muhling KH, Lauchli A (2003) Interaction of NaCl and Cd stress on compartmentation pattern of cations, antioxidant enzymes and proteins in leaves of two wheat genotypes differing in salt tolerance. Plant Soil 253(1):219–231

    Article  Google Scholar 

  • Munns R (2005) Genes and salt tolerance: bringing them together. Plant Cell 25:239–250

    Google Scholar 

  • Munns R, Tester M (2008) Mechanisms of salinity tolerance. Annu Rev Plant Biol 59:651–681

    Article  PubMed  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Odeny DA (2007) The potential of pigeonpea (Cajanus cajan (L.) Millsp.) in Africa. Nat Res Forum 31:297–305

    Article  Google Scholar 

  • Ouzounidou GE, Eleftheriou P, Karataglis S (1992) Ecophysiological and ultrastructural effects of copper in Thlaspi ochroleucum (cruciferae). Can J Bot 70:947–957

    Article  CAS  Google Scholar 

  • Palma F, Lluch C, Iribane C, Garcia-Garrido JM, Garcia Tejera NA (2009) Combined effect of salicylic acid and salinity on some antioxidant activities, oxidative stress and metabolite accumulation in Phaseolus vulgaris. Plant Growth Regul 58:307–316

    Article  CAS  Google Scholar 

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

    Article  Google Scholar 

  • Porras-Soriano A, Soriano-Martin MS, Porras-Piedra A, Azcon R (2009) Arbuscular mycorrhizal fungi increased growth, nutrient uptake and tolerance to salinity in olive trees under nursery conditions. J Plant Physiol 166:1350–1359

    Article  PubMed  CAS  Google Scholar 

  • Raziuddin F, Hassan G, Akmal M, Shah SS, Mohammad F et al (2011) Effects of cadmium and salinity on growth and photosynthesis parameters of Brassica species. Pakistan J Bot 43(1):333–340

    CAS  Google Scholar 

  • Richards LA (1954) Diagnosis and improvement of saline and alkali soils. U. S. Department of Agriculture Handbook 60

  • Rivera-Becerril F (2003) Physiological and molecular responses to cadmium in mycorrhizal and non mycorrhizal pea. Ph.D thesis, Universite de Bourgogne, Dijon

  • Rivera-Becerril F, Calantzis C, Turnau K, Caussanel JP, Belimov AA, Gianinazzi S et al (2002) Cadmium accumulation and buffering of cadmium-induced stress by arbuscular mycorrhiza in three Pisum sativum L. genotypes. J Exp Bot 53:1177–1185

    Article  PubMed  CAS  Google Scholar 

  • Roy BK, Prasad R, Gunjan (2010) Heavy metal accumulation and changes in metabolic parameters in Cajanus cajan grown in mine soil. J Environ Biol 31(5):567–573

    PubMed  CAS  Google Scholar 

  • Sairam RK, Kumutha D, Ezhilmathi K, Chinnusamy V, Meena RC (2009) Waterlogging induced oxidative stress and antioxidant enzyme activities in pigeon pea. Biol Plant 53(3):493–504

    Article  CAS  Google Scholar 

  • Schonfeld MA, Johnson RC, Carver BF, Mornhinweg DW (1988) Water relations in winter wheat as drought resistance indicator. Crop Sci 28:526–531

    Article  Google Scholar 

  • Shafi M, Bakht J, Hassan MJ, Raiziuddin M, Zhang G (2009) Effect of cadmium and salinity stresses on growth and antioxidant enzyme activities of wheat (Triticum aestivum L.). Bull Environ Contam Toxicol 82:772–776

    Article  PubMed  CAS  Google Scholar 

  • Shafi M, Zhang G, Bakht J, Khan MA, Islam UE, Khan MD et al (2010) Effect of cadmium and salinity stresses on root morphology of wheat. Pakistan J Bot 42(4):2747–2754

    CAS  Google Scholar 

  • Shao G, Chen M, Wang W, Zhang G (2008) The effect of salinity pretreatment on Cd accumulation and Cd-induced stress in BADH-transgenic and nontransgenic rice seedling. J Plant Growth Regul 27:205–210

    Article  CAS  Google Scholar 

  • Sheng M, Tang M, Chen H, Yang B, Zhang F, Huang Y (2008) Influence of arbuscular mycorrhizae on photosynthesis and water status of maize plant under salt stress. Mycorrhiza 18:287–296

    Article  PubMed  CAS  Google Scholar 

  • Siddiqui MH, Mohammad F, Khan MN (2009) Morphological and physio-biochemical characterization of Brassica juncea L. Czern. & Coss. genotypes under salt stress. J Plant Interact 4(1):67–80

    Article  CAS  Google Scholar 

  • Sobrino-Plata S, Ortego-Villasante C, Flore-Caceres M, Escobar C, Campo FFD, Hernandez LE (2009) Differential alterations of antioxidant defenses as bioindicators of mercury and cadmium toxicity in alfalfa. Chemosphere 77:946–954

    Article  PubMed  CAS  Google Scholar 

  • Storey R (1995) Salt tolerance, ion relations and the effects of root medium on the response of Citrus to salinity. Aust J Plant Physiol 22:101–114

    Article  CAS  Google Scholar 

  • Vazquez S, Goldsbrough P, Carpena RO (2009) Comparative analysis of the contribution of phytochelatins to cadmium and arsenic tolerance in soybean and white lupin. Plant Physiol Biochem 47:63–67

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Weggler-Beaton K, McLaughlin MJ, Graham RD (2000) Salinity increases cadmium uptake by wheat and Swiss chard from soil amended with biosolids. Aust J Soil Res 38:37–45

    Article  CAS  Google Scholar 

  • Wu QS, Zou YN, He XH (2010) Contributions of arbuscular mycorrhizal fungi to growth, photosynthesis, root morphology and ionic balance of citrus seedlings under salt stress. Acta Physiol Plant 32:297–304

    Article  Google Scholar 

  • Xu J, Yin H, Liu X, Li X (2010) Salt affects plant Cd-stress responses by modulating growth and Cd accumulation. Planta 231:449–459

    Article  PubMed  CAS  Google Scholar 

  • Zeng X, Ma LQ, Qiu R, Tang Y (2009) Responses of non-protein thiols to Cd exposure in Cd hyperaccumulator Arabis paniculata French. Environ Exp Bot 66:242–248

    Article  Google Scholar 

  • Zhang XH, Lin AJ, Chen BD, Wang YS, Smith SE, Smith FA (2006) Effects of Glomus mosseae on the toxicity of heavy metals to Vicia faba. J Environ Sci 18(4):721–726

    CAS  Google Scholar 

  • Zhou YQ, Huang SZ, Yu SL, Gu JG, Zhao JZ, Han YL et al (2010) The physiological responses and sub-cellular localization of lead and cadmium in Iris pseudacorus L. Ecotoxicology 19:69–76

    Article  PubMed  CAS  Google Scholar 

  • Zwiazek JJ, Blake TJ (1991) Early detection of membrane injury in black spruce (Picea mariana). Can J For Res 21:401–404

    Article  Google Scholar 

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Acknowledgment

The authors are deeply grateful to University Grants Commission (UGC), New Delhi, India, for providing the financial support required for undertaking this research.

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  1. Department of Botany, Panjab University, Chandigarh, 160014, India

    Neera Garg & Shikha Chandel

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Garg, N., Chandel, S. 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 (2012). https://doi.org/10.1007/s00344-011-9239-3

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