Plant tolerance to mercury in a contaminated soil is enhanced by the combined effects of humic matter addition and inoculation with arbuscular mycorrhizal fungi

Environmental Science and Pollution Research

Volumn 23, Issue 11, 2016, Pages 11312-11322

  Cozzolino, V ^a   De Martino, A ^a   Nebbioso, A ^a   Di Meo, V ^a   Salluzzo, A ^b   Piccolo, A ^a  

^a UNIVERSITY OF NAPLES FEDERICO II   (Italy)

^b ENEA   (Italy)

Author keywords

Humic acid; Lettuce; Mercury; Metal toxicity; Natural organic matter; Phytostabilization; Plant uptake; Soil contamination

Indexed keywords

ARBUSCULAR MYCORRHIZA; BIOLOGICAL UPTAKE; FUNGUS; HUMIC ACID; INOCULATION; LEAFY VEGETABLE; MERCURY (ELEMENT); PHYTOREMEDIATION; PHYTOTOXICITY; PIGMENT; POLLUTION TOLERANCE; SOIL ORGANIC MATTER; SOIL POLLUTION;

FUNGI; LACTUCA; LACTUCA SATIVA; RHIZOPHAGUS;

HUMIC SUBSTANCE; MERCURY; SOIL; SOIL POLLUTANT;

ANALYSIS; BIOMASS; CHEMISTRY; GLOMEROMYCOTA; GROWTH, DEVELOPMENT AND AGING; HUMIC SUBSTANCE; LETTUCE; METABOLISM; MICROBIOLOGY; MYCORRHIZA; PLANT ROOT; SOIL; SOIL POLLUTANT; TOXICITY;

BIOMASS; GLOMEROMYCOTA; HUMIC SUBSTANCES; LETTUCE; MERCURY; MYCORRHIZAE; PLANT ROOTS; SOIL; SOIL MICROBIOLOGY; SOIL POLLUTANTS;

EID: 84959373530     PISSN: 09441344     EISSN: 16147499     Source Type: Journal    
DOI: 10.1007/s11356-016-6337-6     Document Type: Article

References (78)

1. Adriano DC (2001) Trace elements in terrestrial environments. Springer, New York, pp 1–27
2. Andrade SA, Gratao PL, Azevedo RA, Silveira AP, Schiavinato MA, Mazzafera P (2010) Biochemical and physiological changes in jack bean under mycorrhizal symbiosis growing in soil with increasing Cu concentrations. Environ Exp Bot 68:198–207
3. Beauford W, Barber J, Barringer AR (1977) Uptake and distribution of mercury within higher plants. Physiol Plant 39:261–265
4. Bothe H, Regvar M, Turnau K (2010) Arbuscular mycorrhiza, heavy metal and salt tolerance. In: Sherameti I, Varma A (eds) Soil heavy metals. Springer, Heidelberg, pp 87–111
5. Canellas LP, Olivares FL (2014) Physiological responses to humic substances as plant growth promoter. Chemical and Biological Technologies in Agriculture 1:3
6. Cavallini A, Natali L, Durante M, Maserti B (1999) Mercury uptake, distribution and DNA affinity in durum wheat (Triticum durum Desf.) plants. Sci Total Environ 243:119–127
7. Chakraborty P, Vudamala K, Coulibaly M, Ramteke D, Chennuri K, Lean D (2015) Reduction of mercury (II) by humic substances—influence of pH, salinity of aquatic system. Environ Sci Pollut Res 22:10529–10538
8. Chen J, Shiyab S, Han FX, Monts DL, Waggoner CA, Yang Z, Su Y (2009) Bioaccumulation and physiological effects of mercury in Pteris vittata and Nephrolepis exaltata. Ecotoxicology 18:110–121
9. Cho UH, Park JO (2000) Mercury-induced oxidative stress in tomato seedlings. Plant Sci 156:1–9
10. Cornejo P, Pérez-Tienda J, Meier S, Valderas A, Borie F, Azcón-Aguilar C, Ferrol N (2013) Copper compartmentalization in spores as a survival strategy of arbuscular mycorrhizal fungi in Cu-polluted environments. Soil Biol Biochem 57:925–928
11. Cozzolino A, Piccolo A (2002) Polymerization of dissolved humic substances catalyzed by peroxidase. Effects of pH and humic composition. Org Geochem 33:281–294
12. Cozzolino V, Pigna M, Di Meo V, Caporale AG, Violante A (2010) Effects of arbuscular mycorrhizal inoculation and phosphorus supply on the growth of Lactuca sativa L. and arsenic and phosphorus availability in an arsenic polluted soil under non-sterile conditions. Appl Soil Ecol 45:262–268
13. Cozzolino V, Di Meo V, Piccolo A (2013) Impact of arbuscular mycorrhizal fungi applications on maize production and soil phosphorus availability. J Geochem Explor 129:40–44
14. 198Hg in four crop species. Environ Toxicol Chem 33:334–340
15. Ekamawanti HA, Setiadi Y, Sopandie D, Santosa DA (2014) Mercury stress resistances in Nauclea orientalis seedlings inoculated with arbuscular mycorrhizal fungi. Agriculture, Forestry and Fisheries 3:113–120
16. Ferreira PAA, Ceretta CA, Soriani HH, Tiecher TL, Soares CRFS, Rossato LV et al (2015) Rhizophagus clarus and phosphate alter the physiological responses of Crotalaria juncea cultivated in soil with a high Cu level. Appl Soil Ecol 91:37–47
17. Fodor F (2002) Physiological responses of vascular plants to heavy metals. In: Physiology and biochemistry of metal toxicity and tolerance in plants. Springer, Netherlands, pp 149–177
18. Garau G, Castaldi P, Santona L, Deiana P, Melis P (2007) Influence of red mud, zeolite and lime on heavy metal immobilization, culturable heterotrophic microbial populations and enzyme activities in a contaminated soil. Geoderma 142:47–57
19. Gaur A, Adholeya A (2004) Prospects of arbuscular mycorrhizal fungi in phytoremediation of heavy metal contaminated soils. Current Sci India 86:528–534
20. Gil-Cardeza ML, Ferri A, Cornejo P, Gomez E (2014) Distribution of chromium species in a Cr-polluted soil: presence of Cr (III) in glomalin related protein fraction. Sci Total Environ 493:828–833
21. Giovannetti M, Mosse B (1980) An evaluation of techniques to measure VA infection in roots. New Phytol 84:167–174
22. Gnamuš A, Byrne AR, Horvat M (2000) Mercury in the soil–plant–deer–predator food chain of a temperate forest in Slovenia. Environ Sci Technol 34:3337–3345
23. Godbold DL, Huettermann A (1988) Inhibition of photosynthesis and transpiration in relation to mercury-induced root damage in spruce seedlings [methyl-mercury]. Physiol Plant
24. Göhre V, Paszkowski U (2006) Contribution of the arbuscular mycorrhizal symbiosis to heavy metal phytoremediation. Planta 223:1115–1122
25. Gonzalez-Chavez C, D'haen J, Vangronsveld J, Dodd JC (2002) Copper sorption and accumulation by the extraradical mycelium of different Glomus spp. (arbuscular mycorrhizal fungi) isolated from the same polluted soil. Plant Soil 240:287–297
26. Gonzalez-Chavez MC, Carrillo-Gonzalez R, Wright SF, Nichols KA (2004) The role of glomalin, a protein produced by arbuscular mycorrhizal fungi, in sequestering potentially toxic elements. Environ Pollut 130:317–323
27. Greger M, Wang Y, Neuschütz C (2005) Absence of Hg transpiration by shoot after Hg uptake by roots of six terrestrial plant species. Environ Pollut 134:201–208
28. Halim M, Conte P, Piccolo A (2003) Potential availability of heavy metals to phytoextraction from contaminated soils induced by exogenous humic substances. Chemosphere 52:265–275
29. Haneef I, Faizan S, Perveen R, Kausar S (2013) Role of arbuscular mycorrhizal fungi on growth and photosynthetic pigments in Coriandrum sativum L. grown under cadmium stress. World J Agric Sci 9(3):245–250
30. Hartley-Whitaker J, Ainsworth G, Vooijs R, Ten Bookum W, Schat H, Meharg AA (2001) Phytochelatins are involved in differential arsenate tolerance in Holcus lanatus. Plant Physiol 126:299–306
31. Israr M, Sahi S, Datta R, Sarkar D (2006) Bioaccumulation and physiological effects of mercury in Sesbania drummondii. Chemosphere 65:591–598
32. Joner EJ, Briones R, Leyval C (2000) Metal-binding capacity of arbuscular mycorrhizal mycelium. Plant Soil 226:227–234
33. Kaldorf M, Kuhn AJ, Schröder WH, Hildebrandt U, Bothe H (1999) Selective element deposits in maize colonized by a heavy metal tolerance conferring arbuscular mycorrhizal fungus. J Plant Physiol 154:718–728
34. Khan AG, Kuek C, Chaudhry TM, Khoo CS, Hayes WJ (2000) Role of plants, mycorrhizae and phytochelators in heavy metal contaminated land remediation. Chemosphere 41:197–207
35. Krupp EM, Mestrot A, Wielgus J, Meharg AA, Feldmann J (2009) The molecular form of mercury in biota: identification of novel mercury peptide complexes in plants. Chem Commun 28:4257–4259
36. Lenti K, Fodor F, Böddi B (2002) Mercury inhibits the activity of the NADPH: protochlorophyllide oxidoreductase (POR). Photosynthetica 40:145–151
37. Lichtenthaler HK (1987) Chlorophyll fluorescence signatures of leaves during the autumnal chlorophyll breakdown. J Plant Physiol 131:101–110
38. Ma C (1998) Mercury harm on cell membrane of rape leaf and cell endogenous protection effect. Yingyong Shengtai Xuebao 9:23–326
39. Maggio A, Joly RJ (1995) Effects of mercuric chloride on the hydraulic conductivity of tomato root systems (evidence for a channel-mediated water pathway). Plant Physiol 109:331–335
40. Mauclair C, Layshock J, Carpi A (2008) Quantifying the effect of humic matter on the emission of mercury from artificial soil surfaces. Appl Geochem 23:594–601
41. McBride MB (2003) Toxic metals in sewage sludge-amended soils: has promotion of beneficial use discounted the risks? Adv Environ Res 8:5–19
42. Meng DK, Chen J, Yang ZM (2011) Enhancement of tolerance of Indian mustard (Brassica juncea) to mercury by carbon monoxide. J Hazard Mater 186:1823–1829
43. Millán R, Gamarra R, Schmid T, Sierra MJ, Quejido AJ, Sánchez DM et al (2006) Mercury content in vegetation and soils of the Almadén mining area (Spain). Sci Total Environ 368:79–87
44. Miretzky P, Bisinoti MC, Jardim WF (2005) Sorption of mercury (II) in Amazon soils from column studies. Chemosphere 60:1583–1589
45. Moreno FN, Anderson CWN, Stewart RB, Robinson BH, Ghomshei M, Meech JA (2005) Induced plant uptake and transport of mercury in the presence of sulphur-containing ligands and humic acid. New Phytol 166:445–454
46. Moreno-Jiménez E, Peñalosa JM, Esteban E, Carpena-Ruiz RO (2007) Mercury accumulation and resistance to mercury stress in Rumex induratus and Marrubium vulgare grown in perlite. J Plant Nutr Soil Sci 170:485–494
47. Murphy J, Riley JP (1962) A modified single solution method for the determination of phosphate in natural waters. Anal Chim Acta 27:31–36
48. Nebbioso A, Piccolo A (2012) Advances in humeomic: enhanced structural identification of humic molecules after size fractionation of a soil humic acid. Anal Chim Acta 720:77–90
49. Nebbioso A, Mazzei P, Savy D (2014) Reduced complexity of multidimensional and diffusion NMR spectra of soil humic fractions as simplified by Humeomics. Chemical and Biological Technologies in Agriculture 1:24
50. Newsham KK, Fitter AH, Watkinson AR (1995) Multi-functionality and biodiversity in arbuscular mycorrhizas. Trends Ecol Evol 10:407–441
51. Niu Z, Zhang X, Wang S, Zeng M, Wang Z, Zhang Y, Ci Z (2014) Field controlled experiments on the physiological responses of maize (Zea mays L.) leaves to low-level air and soil mercury exposures. Environ Sci Pollut Res 21:1541–1547
52. Padmavathiamma PK, Li LY (2010) Phytoavailability and fractionation of lead and manganese in a contaminated soil after application of three amendments. Bioresour Technol 101:5667–5676
53. 2+ on growth and metabolism of cabbage. Plant Sci 163:753–758
54. Parniske M (2008) Arbuscular mycorrhiza: the mother of plant root endosymbioses. Nat Rev Microbiol 6:763–775
55. Patra M, Sharma A (2000) Mercury toxicity in plants. Bot Rev 66:379–422
56. Patra M, Bhowmik N, Bandopadhyay B, Sharma A (2004) Comparison of mercury systems and the development of genetic tolerance. Environ Exp Bot Rev 52:199–223
57. Pedron F, Petruzzelli G, Barbafieri M, Tassi E (2013) Remediation of a mercury-contaminated industrial soil using bioavailable contaminant stripping. Pedosphere 23:104–110
58. Piccolo A (2002) The supramolecular structure of humic substances: a novel understanding of humus chemistry and implications in soil science. Adv Agron 75:57–134
59. Quiñones MA, Ruiz-Díez B, Fajardo S, López-Berdonces MA, Higueras PL, Fernández-Pascual M (2013) Lupinus albus plants acquire mercury tolerance when inoculated with an Hg-resistant Bradyrhizobium strain. Plant Physiol Biochem 73:168–175
60. 2+-dependent protein kinase (CDPK) at early stages of lateral plant root development. Chemical and Biological Technologies in Agriculture 2:3
61. Ravichandran M (2004) Interactions between mercury and dissolved organic matter—a review. Chemosphere 55:319–331
62. Rivera-Becerril F, Calantzis C, Turnau K, Caussanel JP, 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
63. Sanità di Toppi L, Gabbrielli R (1999) Response to cadmium in higher plants. Environ Exp Bot 41:105–130
64. Schat H, Mercè L, Bernhard R (2000) Metal-specific patterns of tolerance, uptake and transport of heavy metals in hyperaccumulating and nonhyperaccumulating metallophytes. In: Terry N, Banuelos G (eds) Phytoremediation of contaminated soil and water. CRC Press, Boca Raton, pp 171–188
65. Schuster E (1991) The behavior of mercury in the soil with special emphasis on complexation and adsorption processes—a review of the literature. Water Air Soil Pollut 56:667–680
66. Šeršeň F, Král'ová K, Bumbalova A (1998) Action of mercury on the photosynthetic apparatus of spinach chloroplasts. Photosynthetica 35:551–559
67. Shiyab S, Chen J, Han FX, Monts DL, Matta FB, Gu MY (2009) Phytotoxicity of mercury in Indian mustard (Brassica juncea L.). Ecotoxicol Environ Saf 72:619–625
68. Sierra MJ, Millán R, Esteban E (2009) Mercury uptake and distribution in Lavandula stoechas plants grown in soil from Almadén mining district (Spain). Food Chem Toxicol 47:2761–2767
69. Smith SE, Read DJ (2008). Mycorrhizal Symbiosis. (3th ed). Academic Press
70. Tahir MM, Khurshid M, Khan MZ, Abbasi MK, Kazmi MH (2011) Lignite-derived humic acid effect on growth of wheat plants in different soils. Pedosphere 21:124–131
71. Tipping E, Lofts S, Hooper H, Frey B, Spurgeon D, Svendsen C (2010) Critical limits for Hg (II) in soils, derived from chronic toxicity data. Environ Pollut 158:2465–2471
72. Van Steveninck RFM, Babare A, Fernando DR, Van Steveninck ME (1994) The binding of zinc, but not cadmium, by phytic acid in roots of crop plants. Plant Soil 167:157–164
73. Wang Y, Greger M (2004) Clonal differences in mercury tolerance, accumulation, and distribution in willow. J Environ Qual 33:1779–1785
74. Wang DY, Qing CL, Guo TY, Guo YJ (1997) Effects of humic acid on transport and transformation of mercury in soil-plant systems. Water Air Soil Pollut 95:35–43
75. Warwick P, Inam E, Evans N (2005) Arsenic’s interaction with humic acid. Environ Chem 2:119–124
76. Wu SL, Chen BD, Sun YQ, Ren BH, Zhang X, Wang YS (2014) Chromium resistance of dandelion (Taraxacum platypecidum Diels.) and bermudagrass (Cynodon dactylon [Linn.] Pers.) is enhanced by arbuscular mycorrhiza in Cr (VI)‐contaminated soils. Environ Toxicol Chem 33:2105–2113
77. Yu Y, Zhang S, Huang H (2010) Behavior of mercury in a soil–plant system as affected by inoculation with the arbuscular mycorrhizal fungus Glomus mosseae. Mycorrhiza 20:407–414
78. 2+) on humic acids and fulvic acids extracted from typical soils in China. Colloids Surf A 335:194–201