Arbuscular mycorrhizal fungal inoculation protects Miscanthus×giganteus against trace element toxicity in a highly metal-contaminated site

Science of the Total Environment

Volumn 527-528, Issue , 2015, Pages 91-99

  Firmin, Stéphane ^a,b   Labidi, Sonia ^a,c   Fontaine, Joël ^a   Laruelle, Frédéric ^a   Tisserant, Benoit ^a   Nsanganwimana, Florian ^d   Pourrut, Bertrand ^d   Dalpé, Yolande ^e   Grandmougin, Anne ^a   Douay, Francis ^d   Shirali, Pirouz ^a   Verdin, Anthony ^a   Lounès Hadj Sahraoui, Anissa ^a  

^a UNIVERSITÉ DU LITTORAL CÔTE D OPALE   (France)

^b INSTITUT POLYTECHNIQUE LASALLE BEAUVAIS   (France)

^c INSTITUT NATIONAL AGRONOMIQUE DE TUNISIE   (Tunisia)

^d Mines Douai   (France)

^e AGRICULTURE AND AGRI FOOD CANADA   (Canada)

Author keywords

Arbuscular mycorrhizal inoculation; Miscanthus giganteus; Oxidative stress biomarkers; Phytomanagement; Polluted soils; Trace elements

Indexed keywords

BIOMARKERS; BIOREMEDIATION; CONTAMINATION; FATTY ACIDS; FUNGI; OXIDATIVE STRESS; OXYGEN; PLANTS (BOTANY); SOIL POLLUTION CONTROL; SOILS; TOXICITY; TRACE ELEMENTS;

ARBUSCULAR MYCORRHIZAL; MISCANTHUS; OXIDATIVE STRESS BIOMARKERS; PHYTOMANAGEMENT; POLLUTED SOILS;

SOIL POLLUTION;

FATTY ACID; GLUTATHIONE; GLUTATHIONE DISULFIDE; MALONALDEHYDE; PEROXIDASE; SUPEROXIDE DISMUTASE; TRACE ELEMENT; METAL; SOIL POLLUTANT;

ARBUSCULAR MYCORRHIZA; BIOMARKER; FATTY ACID; FUNGUS; GRASS; INOCULATION; PHYTOREMEDIATION; SOIL POLLUTION; TOXICITY; TRACE ELEMENT;

ARTICLE; BIOACCUMULATION; CONTROLLED STUDY; ENZYME ACTIVITY; GRASS; LIPID COMPOSITION; LIPID PEROXIDATION; MISCANTHUS GIGANTEUS; MYCORRHIZAL INOCULATION; NONHUMAN; OXIDATIVE STRESS; PHYTOREMEDIATION; PLANT LEAF; PLANT ROOT; PRIORITY JOURNAL; SOIL POLLUTION; AGRICULTURAL INOCULATION; BIOREMEDIATION; DRUG EFFECTS; MYCORRHIZA; PHYSIOLOGY; POACEAE; SOIL POLLUTANT; TOXICITY;

FUNGI; MISCANTHUS; MISCANTHUS X GIGANTEUS;

AGRICULTURAL INOCULANTS; BIODEGRADATION, ENVIRONMENTAL; METALS; MYCORRHIZAE; POACEAE; SOIL POLLUTANTS; TRACE ELEMENTS;

EID: 84929466599     PISSN: 00489697     EISSN: 18791026     Source Type: Journal    
DOI: 10.1016/j.scitotenv.2015.04.116     Document Type: Article

References (83)

1. Akmal M., Jianming X. Microbial biomass and bacterial community changes by Pb contamination in acidic soil. J. Agric. Biol. Sci. 2009, 1:30-37.
2. Alford E.R., Pilon-Smits E.A.H., Paschke M.W. Metallophytes-a view from the rhizosphere. Plant Soil 2010, 337:33-50.
3. Alia, Prasad K.V.S.K., Pardha Saradhi P. Effect of zinc on free radical and proline in Brassica juncea and Cajanuscajan. Phytochemistry 1995, 39:45-47.
4. An G.H., Miyakawa S., Kawahara A., Osaki M., Ezawa T. Community structure of arbuscular mycorrhizal fungi associated with pioneer grass species Miscanthus sinensis in acid sulfate soils: habitat segregation along pH gradients. Soil Sci. Plant Nutr. 2008, 54:517-528.
5. Andrade S.A.L., Silveira A.P.D., Mazzafera P. Arbuscular mycorrhiza alters metal uptake and the physiological response of Coffea Arabica seedlings to increasing Zn and Cu concentrations in soil. Sci. Total Environ. 2010, 408:5381-5391.
6. Apel K., Hirt H. Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Annu. Rev. Plant Biol. 2004, 55:373-399.
7. Benabdellah K., Azcón-Aguilar C., Valderas A., Speziga D., Fitzpatrick T.B., Ferrol N. GintPDX1 encodes a protein involved in vitamin B6 biosynthesis that is up-regulated by oxidative stress in the arbuscular mycorrhizal fungus Glomus intraradices. New Phytol. 2009, 184:682-693.
8. Bidar G., Verdin A., Garçon G., Pruvot C., Laruelle F., Grandmougin-Ferjani A., Shirali P. Changes in fatty acid composition and content of two plants (Lolium perenne and Trifolium repens) grown during 6 and 18months in a metal (Pb, Cd, Zn) contaminated field. Water Air Soil Pollut. 2008, 192:281-291.
9. Blaudez D., Botton B., Chalot M. Cadmium uptake and subcellular compartmentation in the ectomycorrhizal fungus Paxillus involutus. Microbiology 2000, 46:1109-1117.
10. Bor M., Özdemir F., Türkan I. The effect of salt stress on lipid peroxidation and antioxidants in leaves of sugar beet Beta vulgaris L and wild beet Beta maritima L. Plant Sci. 2003, 164:77-84.
11. Burleigh S.H., Bechmann I.E. Plant nutrient transporter regulation in arbuscular mycorrhizas. Plant Soil 2002, 244:247-251.
12. Campbell J.E., Lobell D.B., Genova R.C., Field C.B. The global potential of bioenergy on abandoned agriculture lands. Environ. Sci. Technol. 2008, 42:5791-5794.
13. Chaudhry T.M., Khan A.G. Role of symbiotic organisms in sustainable plant growth on heavy metal contaminated industrial sites. Biotechnology of Microbes and Sustainable Utilization 2002, 270-279. Scientific Publishers, Jodhpur. R.C. Rajak (Ed.).
14. Christian D.G., Riche A.B., Yates N.E. Growth, yield and mineral content of Miscanthus×giganteus grown as a biofuel for 14 successive harvests. Ind. Crop. Prod. 2008, 28:320-327.
15. Cicatelli A., Lingua G., Todeschini V., Biondi S., Torrigiani P., Castiglione S. Arbuscular mycorrhizal fungi restore normal growth in a white poplar clone grown on heavy metal-contaminated soil, and this is associated with upregulation of foliar metallothionein and polyamine biosynthetic gene expression. Ann. Bot. 2010, 106:791-802.
16. Clemens S. Toxic metal accumulation, responses to exposure and mechanisms of tolerance in plants. Biochimie 2006, 88:1707-1719.
17. Cobbett C., Goldsbrough P. Phytochelatins and metallothioneins: roles in heavy metal detoxification and homeostasis. Annu. Rev. Plant Biol. 2002, 53:159-182.
18. Cornejo P., Perez-Tienda J., Meier S., Valderas A., Borie F., Azcon-Aguilar C., Ferrol N. Copper compartmentalization in spores as a survival strategy of arbuscular mycorrhizal fungi in Cu-polluted environments. Soil Biol. Biochem. 2013, 57:925-928.
19. Dalpé Y., Hamel C. Arbuscular mycorrhizae. Manual of Soil Sampling and Methods of Analysis. Fla 2007, 355-377. Canadian Society of Soil Science, Lewis Publishers of CRC Press, Boca Raton. 3rd ed. M.R. Carter, E.G. Gregorich (Eds.).
20. De Andrade S.A.L., da Silveira A.P.D., Jorge R.A., de Abreu M.F. Cadmium accumulation in sunflower plants influenced by arbuscular mycorrhiza. Int. J. Phytoremediation 2008, 10:1-13.
21. De Vos C.H., Vonk M.J., Vooijs R., Schat H. Glutathione depletion due to copper-induced phytochelatin synthesis causes oxidative stress in Silene cucubalus. Plant Physiol. 1992, 98:853-858.
22. Debiane D., Garçon G., Verdin A., Fontaine J., Durand R., Grandmougin-Ferjani A., Shirali P., Lounes-Hadj Sahraoui A. In vitro evaluation of the genotoxic and oxidative stress potentials of antrhracene on mycorrhizal chicory roots. Environ. Exp. Bot. 2008, 64:120-127.
23. Debiane D., Garçon G., Verdin A., Fontaine J., Durand R., Grandmougin-Ferjani A., Shirali P., Lounes-Hadj Sahraoui A. Mycorrhization alleviates benzo[a]pyrene-induced oxidative stress in an in vitro chicory root model. Phytochemistry 2009, 70:1421-1427.
24. Debiane D., Calonne M., Fontaine J., Laruelle F., Grandmougin-Ferjani A., Lounès-Hadj Sahraoui A. Benzo[a]pyrene induced lipid changes in the monoxenic arbuscular mycorrhizal chicory roots. J. Hazard. Mater. 2012, 209:18-26.
25. Del Val C., Barea J.M., Azcon-Aguilar C. Diversity of arbuscular mycorrhizal fungus populations in heavy-metal-contaminated soils. Appl. Environ. Microbiol. 1999, 65:718-723.
26. Dixit V., Pandey V., Shyam R. Differential antioxidative responses to cadmium in roots and leaves of pea (Pisum sativum L. cv. Azad). J. Exp. Bot. 2001, 52:1101-1109.
27. Ezaki B., Nagao E., Yamamoto Y., Nakashima S., Enomoto T. Wild plants, Andropogon virginicus L and Miscanthus sinensis Anders, are tolerant to multiple stresses including aluminum, heavy metals and oxidative stresses. Plant Cell Rep. 2008, 27:951-961.
28. Fazeli F., Ghorbanli M., Niknam V. Effect of drought on biomass, protein content, lipid peroxidation and antioxidant enzymes in two sesame cultivars. Biol. Plant. 2007, 51:98-103.
29. Garg N., Kaur H. Impact of cadmium-zinc interactions on metal uptake, translocation and yield in pigeonpea genotypes colonized by arbuscular mycorrhizal fungi. J. Plant Nutr. 2013, 36:67-90.
30. Gerdemann J.W., Nicolson T.H. Spores of mycorrhizal Endogone species extracted from soil by wet sieving and decanting. Trans. Br. Mycol. Soc. 1963, 46:235-244.
31. Gildon A., Tinker P.B. Interactions of vesicular arbuscular mycorrhizal infection and heavy metals in plants. New Phytol. 1983, 95:247-261.
32. Göhre V., Paszkowski U. Contribution of the arbuscular mycorrhizal symbiosis to heavy metal phytoremediation. Planta 2006, 223:1115-1122.
33. Grandmougin-Ferjani A., Dalpé Y., Hartmann M.A., Laruelle F., Couturier D., Sancholle M. Taxonomic aspect of the sterol and D11-hexadecenoic acid (C16:1D11) distribution in arbuscular mycorrhizal spores. Physiology, Biochemistry and Molecular Biology of Plant Lipids 1996, 195-197. Kluwer, Dordrecht. J.P. Williams, M.U. Kahn, N.W. Lem (Eds.).
34. Ha S.B., Smith A.P., Howden R., Dietrich W.M., Bugg S., O'Connell M.J., Goldsbroughb P.B., Cobbetta C.S., Cobbett C.S. Phytochelatin synthase genes from Arabidopsis and the yeast Schizosaccharomyces pombe. Plant Cell Online 1999, 11:1153-1163.
35. Harms H., Schlosser D., Wick L.Y. Untapped potential: exploiting fungi in bioremediation of hazardous chemicals. Nat. Rev. Microbiol. 2011, 9:177-192.
36. Hartley W., Dickinsona N.M., Ribyb P., Leppa N.W. Arsenic mobility in brownfield soils amended with green waste compost or biochar and planted with Miscanthus. Environ. Pollut. 2009, 157:2654-2662.
37. Hildebrandt U., Regvar M., Bothe H. Arbuscular mycorrhiza and heavy metal tolerance. Phytochemistry 2007, 68:139-146.
38. Kaldorf M., Kuhn A.J., Schroeder W.H., Hildebrandt U., Bothe H. Selective element deposits in maize colonized by a heavy metal tolerance conferring arbuscular mycorrhizal fungus. J. Plant Physiol. 1999, 154:718-728.
39. Koske R.E., Gemma J.N. A modified procedure for staining roots to detect V-A mycorrhizas. Mycol. Res. 1989, 92:486-488.
40. Lenton K.J., Therriault H., Wagner J.R. Analysis of glutathione and glutathione disulfide in whole cells and mitochondria by postcolumn derivatization high-performance liquid chromatography with ortho-phthalaldehyde. Anal. Biochem. 1999, 274:125-130.
41. Leung H.M., Ye Z.H., Wong M.H. Survival strategies of plants associated with arbuscular mycorrhizal fungi on toxic mine tailings. Chemosphere 2007, 66:905-915.
42. Mc Gonigle T.P., Miller M.H., Evans D.G., Fairchild G.L., Swan J.A. A new method which gives an objective measure of colonization of roots by vesicular-arbuscular mycorrhizal fungi. New Phytol. 1990, 115:495-501.
43. Miranda D., Fischer G., Ulrichs C. The influence of arbuscular mycorrhizal colonization on the growth parameters of Cape gooseberry (Physalis peruviana L.) plants grown in a saline soil. Journal of Soil Sci. Plant Nutr. 2011, 11:18-30.
44. Morrison W.R., Smith L.M. Preparation of fatty acid methyl esters and dimethylacetals from lipids with boron fluoride-methanol. J. Lipid Res. 1964, 5:600-608.
45. Niyogi K.K. Photoprotection revisited: genetic and molecular. Annu. Rev. Plant Biol. 1999, 50:333-359.
46. Noyd R.K., Pfleger F.L., Norland M.R., Sadowsky M.J. Native prairie grasses and microbial community responses to reclamation of taconite iron ore tailing. Can. J. Bot. 1995, 73:1645-1654.
47. Nsanganwimana F., Pourrut B., Mench M., Douay F. Suitability of Miscanthus species for managing inorganic and organic contaminated land and restoring ecosystem services. A review. J. Environ. Manag. 2014, 143:123-134.
48. Oliveira R.S., Vosátka M., Dodd J.C., Castro P.M.L. Studies on the diversity of arbuscular mycorrhizal fungi and the efficacy of two native isolates in a highly alkaline anthropogenic sediment. Mycorrhiza 2005, 16:23-31.
49. Olsson P.A. Signature fatty acids provide tools for determination of the distribution and interactions of mycorrhizal fungi in soil. FEMS Microbiol. Ecol. 1999, 29:303-310.
50. Ouariti O., Boussama N., Zarrouk M., Cherif A., Habib Ghorbal M. Cadmium-and copper-induced changes in tomato membrane lipids. Phytochemistry 1997, 45:1343-1350.
51. Ouziad F., Hildebrandt U., Schmelzer E., Bothe H. Differential gene expressions in arbuscular mycorrhizal-colonized tomato grown under heavy metal stress. J. Plant Physiol. 2005, 162:634-649.
52. Pál M., Leskó K., Janda T., Páldi E., Szalai G. Cadmium-induced changes in the membrane lipid composition of maize plants. Cereal Res. Commun. 2007, 354:1631-1642.
53. Pavel P.B., Puschenreiter M., Wenzel W.W., Diacu E., Barbu C.H. Aided phytostabilization using Miscanthus sinensis×giganteus on heavy metal-contaminated soils. Sci. Total Environ. 2014, 479:125-131.
54. Phillips J.M., Hayman D.S. Improved procedures for clearing roots and staining parasitic and vesicular-arbuscular mycorrhizal fungi for rapid assessment of infection. Trans. Br. Mycol. Soc. 1970, 55:158-161.
55. Pulford I.D., Watson C. Phytoremediation of heavy metal-contaminated land by trees-a review. Environ. Int. 2003, 29:529-540.
56. Robinson B., Schulin R., Nowack B., Roulier S., Menon M., Clothier B., Green S., Mills T. Phytoremediation for the management of metal flux in contaminated sites. For. Snow Landsc. Res. 2006, 80:221-234.
57. Ryszka P., Turnau K. Arbuscular mycorrhiza of introduced and native grasses colonizing zinc wastes: implications for restoration practices. Plant Soil 2007, 298:219-229.
58. Scebba F., Arduini I., Ercoli L., Sebastiani L. Cadmium effects on growth and antioxidant enzymes activities in Miscanthus sinensis. Biol. Plant. 2006, 50:688-692.
59. Schützendübel A., Polle A. Plant responses to abiotic stresses: heavy metal-induced oxidative stress and protection by mycorrhization. J. Exp. Bot. 2002, 57:711-726.
60. Sharma S.S., Dietz K.J. The significance of amino acids and amino acid-derived molecules in plant responses and adaptation to heavy metal stress. J. Exp. Bot. 2006, 57:711-726.
61. Sharmin S.A., Alam I., Kim K.H., Kim Y.G., Kim P.J., Bahk J.D., Lee B.H. Chromium-induced physiological and proteomic alterations in roots of Miscanthus sinensis. Plant Sci. 2012, 187:113-126.
62. Sinha S., Saxena R., Singh S. Chromium induced lipid peroxidation in the plants of Pistia stratiotes L: role of antioxidants and antioxidant enzymes. Chemosphere 2005, 58:595-604.
63. Smith S., Read D. Mycorrhizal Symbiosis 2008, Academic Press, New York. 3rd edition.
64. Soleimani M., Akbar S., Hajabbasi M.A. Enhancing phytoremediation efficiency in response to environmental pollution stress. Plants Environ. 2011, 81:1-14.
65. Sterckeman T., Douay F., Fourrier H., Proix N. Référentiel Pédo-Géochimique du Nord-Pas de Calais Technical report 2002, Conseil Régional Nord-Pas de Calais - Ministère de l'Aménagement du Territoire et de l'Environnement, (128pp.).
66. Técher D., Laval-Gillya P., Henry S., Bennasroune S., Formanek P., Martinez-Chois C., D'Innocenzo M., François Muanda F., Amadou Dicko A., Klement Rejšek K., Jairo Falla J. Contribution of Miscanthus x giganteus root exudates to the biostimulation of PAH degradation: an in vitro study. Environ. Pollut. 2011, 159:1721-1729.
67. Thompson J., Bannigan J. Cadmium: toxic effects on the reproductive system and the embryo. Reprod. Toxicol. 2008, 25:304-315.
68. Thompson J.E., Froese C.D., Madey E., Smith M.D., Hong Y.W. Lipid metabolism during plant senescence. Prog. Lipid Res. 1998, 37:119-141.
69. Ussiri D.A., Lal R. Long-term tillage effects on soil carbon storage and carbon dioxide emissions in continuous corn cropping system from an alfisol in Ohio. Soil Tillage Res. 2009, 104:39-47.
70. Vangronsveld J., Herzig R., Weyens N., Boulet J., Adriaensen K., Ruttens A., Thewys T., Vassilev A., Meers E., Nehnevajova E., van der Lelie D., Mench M. Phytoremediation of contaminated soils and groundwater: lessons from the field. Environ. Sci. Pollut. Res. 2009, 16:765-794.
71. Vassilev A., Schwitzguébel J.P., Thewys T., van der Lelie D., Vangronsveld J. The use of plants for remediation of metal-contaminated soils. Sci. World J. 2004, 4:9-34.
72. Vázquez S., Esteban E., Carpena R.O. Evolution of arsenate toxicity in nodulated White Lupine in a long-term culture. J. Agric. Food Chem. 2008, 56:8580-8587.
73. Verdin A., Lounès-Hadj Sahraoui A., Fontaine J., Grandmougin-Ferjani A., Durand R. Effects of anthracene on development of an arbuscular mycorrhizal fungus and contribution of the symbiotic association to pollutant dissipation. Mycorrhiza 2006, 16:397-405.
74. Verkleij J.A.C., Schat H. Mechanisms of metal tolerance in higher plants. Heavy Metal Tolerance in Plants: Evolutionary Aspects 1990, 179-193. CRC Press, Boca Raton.
75. Vosátka M., Dodd J.C. Ecological considerations for successful application of arbuscular mycorrhizal fungi inoculum. Mycorrhizal Technology in Agriculture 2002, 235-247. Birkhäuser Basel. S. Gianinazzi, H. Schüepp, J. Miguel Barea, K. Haselwandter (Eds.).
76. Wanat N., Austruy A., Joussein E., Soubrand M., Hitmi A., Gauthier-Moussard C., Pichon M. Potentials of Miscanthus giganteus grown on highly contaminated technosols. J. Geochem. Explor. 2013, 126:78-84.
77. Waterlot C., Douay F. The problem of arsenic interference in the analysis of Cd to evaluate its extractability in soils contaminated by arsenic. Talanta 2009, 80:716-722.
78. Waterlot C., Bidar G., Douay F., Daurangeon F. Analysis of trace elements in solution, assessment of a background compensation technique on the As interference in the Cd analysis. Spectra Anal. 2008, 261:48-52.
79. Weissenhorn I., Leyval C., Berthelin J. Cd-tolerant arbuscular mycorrhizal (AM) fungi from heavy-metal polluted soils. Plant Soil 1993, 157:247-256.
80. Weissenhorn I., Glashoff A., Leyval C., Berthelin J. Differential tolerance to Cd and Zn of arbuscular mycorrhizal (AM) fungal spores isolated from heavy metal-polluted and unpolluted soils. Plant Soil 1994, 167:189-196.
81. http://www.zor.zut.edu.pl/Glomeromycota/.
82. Yamauchi Y., Furutera A., Seki K., Toyoda Y., Tanaka K., Sugimoto Y. Malondialdehyde generated from peroxidized linolenic acid causes protein modification in heat-stressed plants. Plant Physiol. Biochem. 2008, 46:786-793.
83. Zhuang P., McBride M.B., Xia H.P., Li N.Y., Lia Z.A. Health risk from heavy metals via consumption of food crops in the vicinity of Dabaoshan mine, South China. Sci. Total Environ. 2009, 407:1551-1561.