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

Journal of Plant Growth Regulation

Volumn 31, Issue 3, 2012, Pages 292-308

  Garg, Neera ^a   Chandel, Shikha ^a  

^a PANJAB UNIVERSITY   (India)

Author keywords

Arbuscular mycorrhiza; Cadmium; Phytochelatins; Proline; Sodium chloride

Indexed keywords

ARBUSCULAR; CAJANUS CAJAN; FUNGI; GLOMUS MOSSEAE;

EID: 84864531917     PISSN: 07217595     EISSN: 14358107     Source Type: Journal    
DOI: 10.1007/s00344-011-9239-3     Document Type: Article

References (79)

1. Anderson ME (1985) Determination of glutathione and glutathione disulfides in biological samples. Methods Enzymol 113: 548-570.
2. Andrade SAL, Silveira APD (2008) Mycorrhiza influence on maize development under Cd stress and P supply. Braz J Plant Physiol 20(1): 39-50.
3. 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.
4. AOAC (1990) Official method of analysis of the association of official analytical chemists, 15th edn, vol 1. Association of Analytical Chemists, Arlington.
5. Arnon DI (1949) Copper enzymes in isolated chloroplasts. Polyphenyloxidase in Beta vulgaris. Plant Physiol 24: 1-15.
6. 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.
7. 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.
8. 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.
9. Bates LS, Waldran RP, Teare ID (1973) Rapid determination of free proline for water studies. Plant Soil 39: 205-208.
10. 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.
11. 2-fixing cyanobacterium Anabaenadoliolum. J Plant Physiol 162: 1220-1225.
12. 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.
13. Chapman HD, Pratt PF (1961) Methods of analysis for soil plant and waters. Division of Agricultural Sciences, University of California, Berkley.
14. 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.
15. 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.
16. 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.
17. 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.
18. FAO (2008) FAO land and plant nutrition management service. http://www. fao. org/ag/agl/ahll/spush. Accessed 13-15 May 2008.
19. 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.
20. 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.
21. 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.
22. 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.
23. Garg N, Chandel S (2010) Arbuscular mycorrhizal networks: process and functions. A review. Agron Sustain Dev 30(3): 581-599.
24. 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.
25. 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.
26. Greive CM, Grattan SR (1983) Rapid assay for determination of water soluble quaternary-amino compounds. Plant Soil 70: 303-307.
27. 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.
28. 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.
29. 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.
30. Heath RL, Packer I (1968) Photoperoxidation in isolated chloroplast I, Kinetics and stoichiometry of fatty acid peroxidation. Arch Biochem Biophys 125: 189-198.
31. Hillocks RJ, Minja E, Nahdy MS, Subrahmanyam P (2000) Diseases and pests of pigeonpea in eastern Africa. Int J Pest Manag 46: 7-18.
32. Hiscox TD, Israelstam GF (1979) A method for extraction of chlorophyll from leaf tissue without maceration. Can J Bot 57: 1331-1334.
33. 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.
34. 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.
35. 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.
36. Khade SW, Adholeya A (2007) Feasible bioremediation through arbuscular mycorrhizal fungi imparting heavy metal tolerance: a retrospective. Biorem J 11(1): 33-43.
37. 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.
38. 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.
39. 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.
40. Lee YP, Takashi T (1966) An improved colorimetric determination of amino acids with the use of ninhydrin. Anal Biochem 14: 71-77.
41. 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.
42. 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.
43. 2+ activity. Environ Technol 31(3): 307-318.
44. 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.
45. 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.
46. Miransari M (2010) Contribution of arbuscular mycorrhizal symbiosis to plant growth under different types of soil stress. Plant Biol (Stuttg) 12(4): 563-569.
47. Monteiro MS, Santos C, Soares AMVM, Mann RM (2009) Assessment of biomarkers of cadmium stress in lettuce. Ecotoxicol Environ Saf 72: 811-818.
48. 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.
49. Munns R (2005) Genes and salt tolerance: bringing them together. Plant Cell 25: 239-250.
50. Munns R, Tester M (2008) Mechanisms of salinity tolerance. Annu Rev Plant Biol 59: 651-681.
51. Nelson DW, Sommers LE (1973) Determination of total nitrogen in plant material. Agron J 65: 109-112.
52. Odeny DA (2007) The potential of pigeonpea (Cajanus cajan (L.) Millsp.) in Africa. Nat Res Forum 31: 297-305.
53. Ouzounidou GE, Eleftheriou P, Karataglis S (1992) Ecophysiological and ultrastructural effects of copper in Thlaspi ochroleucum (cruciferae). Can J Bot 70: 947-957.
54. 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.
55. 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.
56. 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.
57. 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.
58. Richards LA (1954) Diagnosis and improvement of saline and alkali soils. U. S. Department of Agriculture Handbook 60.
59. Rivera-Becerril F (2003) Physiological and molecular responses to cadmium in mycorrhizal and non mycorrhizal pea. Ph. D thesis, Universite de Bourgogne, Dijon.
60. 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.
61. 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.
62. 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.
63. Schonfeld MA, Johnson RC, Carver BF, Mornhinweg DW (1988) Water relations in winter wheat as drought resistance indicator. Crop Sci 28: 526-531.
64. 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.
65. 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.
66. 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.
67. 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.
68. 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.
69. 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.
70. 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.
71. 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.
72. 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.
73. 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.
74. 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.
75. 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.
76. 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.
77. 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.
78. 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.
79. Zwiazek JJ, Blake TJ (1991) Early detection of membrane injury in black spruce (Piceamariana). Can J For Res 21: 401-404.