The effect of glomalin on root stabilization of lead in clover plant inoculated with Rhizophagus irregularis fungus

Document Type : Complete scientific research article

Authors

Department of Soil Science, Faculty of Agriculture, University of Tabriz, Tabriz, Iran

Abstract

Background and objectives: Root stabilization of toxic metals by mycorrhizal plants is one of the protective mechanisms of symbiotic arbuscular mycorrhizal (AM) fungi in response to metal stress. Role of the glomalin as a specific glycoprotein of spore and hyphal cell wall of AM fungi can be remarkable in sequestration of toxic metals and reduction of stress effects on host plant. Considering this hypothesize, the study was conducted to investigate the role of glomalin produced by Rhizophagus irregularis fungus symbiosis of clover plant in root stabilization of Pb.
Materials and Methods: A pot culture experiment was performed as completely randomized block design by two factors including AM fungus (inoculated with R. irregularis and non-inoculated) and four levels of Pb+2 (0, 150, 300 and 450 µM) with five replications. For glomalin extraction, root samples were autoclaved at 121˚C with 50 mM sodium citrate buffer for 1 hr in three cycles. Glomalin concentration in the extracted samples were determined by ELISA method using monoclonal antibody 32B11. After precipitation of the glomalin and its digestion in concentrated nitric acid, Pb-sequestrated by the glomalin were measured. Shoot and root dry weights, root colonization percentage, shoot and root P and Pb contents, and plant uptake, extraction and translocation efficiency of Pb were assessed.
Results: Shoot and root dry weights of mycorrhizal (M) and non-mycorrhizal (NM) plants were decreased by increasing of Pb levels. At the levels of 150, 300 and 450 μm Pb, shoot and root dry weights were decreased by 11.2%, 12.9%, 18.3% and 7.5%, 18.1%, 36.7% compared to the control (0 μm Pb), respectively. Shoot and root dry weights of M plants were increased by 24.9% and 43.2% compared to the NM ones. P contents of shoot and root were affected by AM fungus, so that the shoot and root P contents of M plants were increased by 32.2% and 45.8 % compared to the NM ones. At different levels of Pb, shoot and root Pb contents in M plants significantly were higher than NM ones. Maximum contents of Pb of shoot and root were recorded at level of 450 µM Pb in M plants which were increased by 46.5% and 80.7% compared to the NM ones at the same level. At the levels of 150, 300 and 450 µM Pb, the uptake efficiency of Pb in M plants was increased by 8%, 14.5% and 80.7% compared to the NM ones at the same levels. Based on ANOVA results, Pb-extraction and translocation efficiency were affected by Pb treatments. Pb-extraction efficiency of plants was increased as Pb concentration increased, so that the content of Pb-extraction efficiency at 450 µM of Pb was increased by 69.3% and 27.8% compared to the 150 and 300 µM of Pb, respectively. Plant Pb-translocation efficiency from root to shoot was decreased as Pb concentration increased. The percentage of root colonization was increased as the Pb concentration increased up to 300 µM Pb and then was slightly decreased as the level of Pb rose from 300 to 450 µM, but there was no significant difference between the levels of 150, 300 and 450 µM Pb. Glomalin production in root and Pb sequestrated by glomalin was significantly increased as Pb concentration increased.
Conclusion: Root colonization of clover plant by R. irreqularis led to improved growth and phosphorus nutrition of M plants compared to the NM ones, under Pb stress condition. Pb uptake was greater in roots than in shoots, therefore the clover plants played a more effective role in root stabilisation of Pb.

Keywords

References

1.Andrade, S.A.L., Abreu, C.A., de Abreu, M.F., and Silveira, A.P.D. 2004. Influence of lead addition on arbuscular mycorrhiza and Rhizobium symbioses under soybean plants. Applied Soil Ecology. 26: 2. 123-131.
2.Audet, P., and Charest, C. 2006. Effects of AM colonization on ‘wild tobacco’ grown in zinc contaminated soil. Mycorrhiza. 16: 4. 277-283.
3.Barber, S.A. 1984. Soil Nutrient Bioavailability. A Mechanistic Approach. John Wiley and Sons, New York, USA. 398p.
4.Chen, X., Wu, C., Tang, J., and Hu, S. 2005. Arbuscular mycorrhizae enhance metal lead uptake and growth of host plants under a sand culture experiment. Chemosphere. 60: 5. 665-671.
 5.Cottenie, A. 1980. Methods of Plant Analysis. In: Soil and Plant Testing. FAO Soils Bulletin, NO 38/2, Pp: 94-100.
6.de Andrade, S.A.L., da Silveira, A.P.D., Jorge, R.A., and de Abreu, M.F. 2008. Cadmium accumulation in sunflower plants influenced by arbuscular mycorrhiza. Inter. J. Phytoremed. 10: 1-13.
7.de Souza, L.A., de Andrade, S.A.L.,de Souza, S.C.R., and Schiavinato,M.A. 2012. Arbuscular mycorrhiza confers Pb tolerance in Calopogonium mucunoides. Acta Physiologiae Plantarum. 34: 2. 523-531.
8.Feddermann, N., Roger, F., Boller, T., and Elfstrand, M. 2010. Functional diversity in arbuscular mycorrhiza – the role of gene expression, phosphorous nutrition and symbiotic efficiency. Fungal Ecology. 3: 1-8.
9.Ferreira, A.S., Totola, M.R., Kasuya, M.C.M., Araujo, E.F., and Borges, A.C. 2005. Small heat shock proteins in the development of thermotolerance in Pisolithu ssp. J. Thermal Biol. 30: 8. 595-602.
10.Ferrol, N., Tamayo, E., and Vargas, P. 2016. The heavy metal paradox in arbuscular mycorrhizas: from mechanisms to biotechnological applications. J. Exp. Bot. 67: 22. 6253-6265.
11.Gadkar, V., and Rillig, M.C. 2006. The arbuscular mycorrhizal fungal protein glomalin is a putative homolog of heat shock protein 60. FEMS Microbiology Letters. 263: 93-101.
12.Garg, N., Singh, S., and Kashyap, L. 2017. Arbuscular mycorrhizal fungi and heavy metal tolerance in plants: An insight into physiological and molecular mechanisms. P 75-97, In: Varma, A., R. Prasad and N. Tuteja (eds.), Mycorrhiza-Nutrient Uptake, Biocontrol, Ecorestoration. Springer, Cham, Switzerland.
13.Gaur, A., and Adholeya, A. 2004. Prospects of arbuscular mycorrhizal fungi in phytoremediation of heavy metal contaminated soils. Current Science. 86: 528-534.
14.Giasson, P., Jaouich, A., Gagné, S., and Moutoglis, P. 2005. Phytoremediation of zinc and cadmium: A study of arbuscular mycorrhizal hyphae. Remediation. 15: 113-122.
15.Gil-Cardeza, M.L., Ferri, A., Cornejo, P., and Gomez, E. 2014. Distribution of chromium species in a Cr-polluted soil: presence of Cr(III) in glomalin related protein fraction. Science of the Total Environment. 493: 828-833.
16.Gohre, V., and Paszkowski, U. 2006. Contribution of the arbuscular mycorrhizal symbiosis to heavy metal phytoremediation. Planta. 223: 6. 1115-1122.
17.Gonzalez-Chavez, M.C., Carrillo-Gonzalez, R., Wright, S.F., and Nichols, K.A. 2004. The role of glomalin, a protein produced by arbuscular mycorrhizal fungi, in sequestering potentially toxic elements. Environmental Pollution. 130: 3. 317-323.
18.González-Guerrero, M., Melville, L.H., Ferrol, N., Lott, J.N.A., Azcón-Aguilar, C., and Peterson, R.L. 2008. Ultrastructural localization of heavy metals in the extraradical mycelium and spores of the arbuscular mycorrhizal fungus Glomus intraradices. Can. J. Microbiol. 54: 2. 103-10.
19.Gupta, D.K., Nicolosa, F.T., Schetinger, M.R.C., Rossato, L.V., Pereira, L.B., Castro, G.Y., Srivastava, S., and Tri- pathi, R.D. 2009. Antioxidant defense mechanism in hy- droponically grown Zea mays seedlings under moderate lead stress. J. Hazard. Mater. 172: 479-484.
20.Hall, J.L. 2002. Cellular mechanisms for heavy metal detoxification and toletance. J. Exp. Bot. 53: 366. 1-11.
21.Hammer, E.C., and Rillig, M.C. 2011. The Influence of different stresses on glomalin levels in an arbuscular mycorrhizal fungus- salinity increases glomalin content. PLoS One. 6: 12. 1-5.
22.Hildebrandt, U., Regvar, M., and Bothe, H. 2007. Arbuscular mycorrhiza and heavy metal tolerance. Phytochemistry. 68: 1. 139-146.
23.Hutchinson, J.J., Young, S.D., Black, C.R., and West, H.M. 2004. Determining uptake of radio-labile soil cadmium by arbuscular mycorrhizal hyphae using isotopic dilution in a compartmented-pot system. New Phytologist. 164: 3. 477-484.
 24.Jankong, P., and Visoottiviseth, P. 2008. Effects of arbuscular mycorrhizal inoculation on plants growing on arsenic contaminated soil. Chemosphere. 72: 7. 1092-1097.
25.Janouskova, M., Pavlikova, D., Macek, T., and Vosatka, M. 2005. Arbuscular mycorrhiza decreases cadmium phytoextraction by transgenic tobacco with inserted metallothionein. Plant and Soil. 272: 29-40.
26.Jansa, J., Finlay, R., Wallander, H., Smith, F.A., and Smith, S.E., 2011. Role of mycorrhizal symbioses in phosphorus cycling. In: Phosphorus in action. Soil Biology. Springer, Berlin, Heidelbe, Pp: 137-168.
27.Kabata-Pendias, A. 2011. Trace Elements in Soils and Plants, 4td ed. CRC Press/Taylor and Francis, Boca Raton, USA. 548p.
28.Kormanik, P.P., and McGraw, A.C. 1982. Quantification of vesicular-arbuscular mycorrhizae in plant roots.
P 37-45, In: N.C. Schenck, (ed.), Methods and Principles of Mycorrhizal Research, American Phytopathological Society, Saint Paul, MN.
29.Liang, C., Li, T., Xiao, Y., Liu, M.L., Zhang, H.B. and Zhao, Z.W. 2009. Effects of inoculation with arbuscular mycorrhizal fungi on maize grown in multi-metal contaminated soils. Inter. J. Phytoremed. 11: 8. 692-703.
30.Lingua, G., Franchin, C., Todeschini, V., Castiglione, S., Biondi, S., Burlando, B., Parravicini, V., Torrigiani, P., and Berta, G. 2008. Arbuscular mycorrhizal fungi differentially affect the response to high zinc concentrations of two registered poplar clones. Environmental Pollution. 153: 137-147.
31.Lombi, E., Wenzel, W.W., Gobran, G.R., and Adriano, D.C. 2001. Dependency of metals on indigenous and induced rhizosphere processes: A review. P 3-24, In: G.R. Gobran, , W.W. Wenzel and E. Lombi (eds.), Trace Elements in the Rhizopshere. CRC Press, Boca Raton, Florida.
32.Lopez, M.L., Peralta-Videa, J.R., Castillo-Michel, H., Martinez-Martinez, A., Duarte-Gardea, M., and Gardea-Torresdey,
J.L. 2007. Lead toxicity in alfalfa plants exposed to phytohormones and ethylene diamine tetra acetic acid monitored by peroxidase, catalase and amylase activities. Environmental Toxicology and Chemistry. 26: 12. 2717-2723.
33.Millner, P.D., and Kitt, D.G. 1992. The Beltsville method for soilless production of vesicular arbuscular mycorrhizal fungi. Mycorrhiza. 2: 9-15.
34.Nayuki, K., Chen, B., Ohtomo, R., and Kuga, Y. 2014. Cellular imaging of cadmium in resin sections of arbuscular mycorrhizas using synchrotron micro X-ray fluorescence. Microbes and Environments. 29: 60-66.35.Nichols, K.A., and Wright, S.F. 2005. Comparison of glomalin and humic acid in eight native United State soils. Soil Science. 170: 12. 985-997.
36.Pawlowska, T.E., and Charvat, I. 2004. Heavy-metal stress and developmental patterns of arbuscular mycorrhizal fungi. Applied and Environmental Microbiology. 70: 11. 6643-6649.
37.Peer, W., Baxter, I., Richards, E., Freeman, J., and Murphy, A. 2005. Phytoremediation and hyperaccumulator plants. 14: P 299-340, In: M. Tamas and E. Martinoia (eds.), Topics in Current Genetics, Molecular Biology of Metal Homeostasis and Detoxification. Springer, Berlin.
38.Pellegrino, E., and Bedini, S. 2014. Enhancing ecosystem services in sustainable agriculture: biofertilization and biofortification of chickpea (Cicer arietinum L.) by arbuscular mycorrhizal fungi. Soil Biology and Biochemistry. 68: 429-439.
39.Pourmoradi, S., and Jafari, A.A. 2011. Evaluation of forage yield and quality traits in seven varieties of white clover grown in rangelands of Mazandaran province, Iran. Iran. J. Range Des. Res. 17: 4. 615-623. (In Persian) 40.Purin, S., and Rillig, M.C. 2008. Immuno-cytolocalization of glomalin in the mycelium of the arbuscular mycorrhizal fungus Glomus intraradices. Soil Biology and Biochemistry. 40: 4. 1000-1003.
41.Rabie, G.H. 2005. Contribution of AM fungus to red kidney and wheat plants tolerance grown in heavy metal-polluted soil. Afric. J. Biotechnol. 4: 4. 332-345.
42.Rillig, M.C., and Steinberg, P.D. 2002. Glomalin production by an arbuscular mycorrhizal fungus, a mechanism of habitat modification? Soil Biology and Biochemistry. 34: 9. 1371-1374.
43.Rosier, C.L., Hoye, A.T., and Rillig, M.C. 2006. Glomalin-related soil protein: Assessment of current detection and qualification tools. Soil Biology and Biochemistry. 38: 8. 2205-2211.
44.Seregin, I.V., and Ivanov, V.B. 2001. Physiological aspects of cadmium and lead toxic effects on higher plants. Russ. J. Plant Physiol. 48: 4. 523-544.
45.Sheikh-Assadi, M., Khandan-Mirkohi, A., Alemardan, A., and Moreno-Jiménez, E. 2015. Mycorrhizal Limonium sinuatum (L.) mill. Enhances accumulation of lead and cadmium. Inter. J. Phytoremed. 17: 6. 556-562.
46.Smith, S.E., and Read, D.J. 1997. Mycorrhizal symbiosis, 2nd ed. Academic Press, San Diego, California. 605p.
47.Soleimani, M., Akbar, S., and Hajabbasi, M.A. 2011. Enhancing Phytoremediation Efficiency in Response to Environmetal Pollution Stress. P 1-14, In: H.K.N., Vasanthaiah, and D.M. Kambiranda (eds.), Plants and Environment, In Tech-Open Access Publisher.
48.Subramanian, K.S., Balakrishnan, N., and Senthil, N. 2013. Mycorrhizal symbiosis to increase the grain micronutrient content in maize. Austr. J. Crop Sci. 7: 7. 900-910.
49.Sudova, R., and Vosatka, M. 2007. Differences in the effects of three arbuscular mycorrhizal fungal strains on P and Pb accumulation by maize plants. Plant and Soil. 296: 77-83.
50.Vaidya, G.S., Rillig, M.C., and Wallander, H. 2011. The role of glomalin in soil erosion. Scientific World. 9: 9. 82-85.
51.Vogel-Mikuš, K., Drobne, D., and Regvar, M. 2005. Zn, Cd and Pb accumulation and arbuscular mycorrhizal colonization of pennycress Thlaspi praecox Wulf. (Brassicaceae) from the vicinity of a lead mine and smelter in Slovenia. Environmental Pollution.133: 2. 233-242.
52.Waling, I., Vark, W.V., Houba, V.J.G., and Vanderlee, J.J. 1989. Soil and plant analysis, a series of syllabi: Part 7-
Plant Analysis Procedures. Wageningen Agricultural University, Netherlands.
53.Wang, F., Li, X., and Yin, R. 2005. Heavy metal uptake by arbuscular mycorrhizas of Elsholtzia splendens
and the potential for phytoremediation of contaminated soil. Plant and Soil. 269: 225-232.
54.Wang, F.Y., Lin, X.G., and Yin,R. 2007. Inoculation with arbuscular mycorrhizal fungus Acaulospora mellea decrease Cu phytoextraction by maize from Cu-contaminated soil. Pedobiologia. 51:2. 99-109.
55.Wang, Z.H., Yuan, K., and Yang, L. 2013. Response of maize leaf proteins induced/modulated by AM mycorrhizal inoculation and (or) arsenic stress. China Agriculture Science. 46: 18. 3758-3767.
56.Wright, S.F., Franke-Snyder, M., Morton, J.B., and Upadhyaya, A.1996. Time-course study and partial characterization of a protein on hyphae of arbuscular mycorrhizal fungi during active colonization of roots. Plant and Soil. 181: 2. 193-203.
57.Wright, S.F., and Upadhyaya, A. 1996. Extraction of an abundant and unusual protein from soil and comparison
with hyphal protein from arbuscular mycorrhizal fungi. Soil Science.161: 575-586.
58.Wu, C., Chen, X., and Tang, J.2005. Lead accumulation in weed communities with various species. Communications in Soil Science and Plant Analysis. 36: 13-14. 1891-1902.
59.Wu, S., Zhang, X., Chen, B., Wu, Z.,Li, T., Hu, Y., Sun, Y., and Wang,Y. 2016. Chromium immobilization by extraradical mycelium of arbuscular mycorrhiza contributes to plant chromium tolerance. Environmental and Experimental Botany. 122: 10-18.
60.Zhu, J., Zhang, C., and Lynch, J.P. 2010. The utility of phenotypic plasticity for root hair length for phosphorus acquisition. Functional Plant Biology. 37: 313-322.
Journal of Soil Management and Sustainable Production
Volume 9, Issue 3
December 2020
Pages 69-90

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