Document Type : Research Paper

Authors

1 Department of Soil Science, Faculty of Agriculture, Ferdowsi University of Mashhad, Mashhad, Iran. E-mail: marziemowlavi@um.ac.ir

2 Department of Soil Science, Faculty of Agriculture, Ferdowsi University of Mashhad, Mashhad, Iran. E-mail: jalalsadeghi2@mail.um.ac.ir

3 Corresponding Author, Department of Soil Sciences, Faculty of Agriculture, Ferdowsi University of Mashhad, Mashhad, Iran. E-mail: alakzian@um.ac.ir

Abstract

Objective: In addition to improving root growth and increasing the absorption of nutrients by plants, mycorrhizae affect the availability and different forms of heavy metals in the soil. This study investigated the effect of two mycorrhizal species on the partitioning of cadmium element and also the absorption of this element by persian clover.
Methods: This experiment was carried out in a completely randomized design by factorial method with three replications with three levels of mycorrhiza (without mycorrhizae, funnelliformis mosseae and rhizophagus intraradices) and two levels of cadmium (0 and 10 mg.kg-1) in the research greenhouse of the Faculty of Agriculture of Ferdowsi University of Mashhad in 2018. After harvesting the plant, the dry weight of the shoot and root as well as the concentration of cadmium in these two parts of the plant were measured. Two parameters of mycorrhizal colonization and contribution of mycorrhizal participation in cadmium uptake by shoots and roots were measured. Finally, the effect of experimental treatments on the chemical forms of cadmium in the soil was measured.
Results: The results showed that cadmium caused an increase of 8.7% and a decrease of 31.5% in amount of colonization of funnelliformis mosseae and rhizophagus intraradices. Cadmium decreased the shoot dry weight by 28.7%. The behavior of two mycorrhizal species on the concentration of cadmium in the shoots and roots of persian clover was different. The presence of funnelliformis mosseae caused a significant (P<0.05) and 55.1% decrease in cadmium concentration of clover shoot and a 1.23-fold increase in concentration of this metal in plant roots. The measured decrease in the concentration of cadmium in the roots and shoots of clover in rhizo treatment was 14.5% and 14.3%, respectively, compared to the control. The carbonate form of cadmium had the highest amount of this metal in control soil (1.08 mg/kg) and contaminated soil (4.19 mg/kg). Mycorrhiza colonization of plant in control soil had no significant effect (P<0.05) on the concentration of different forms of cadmium.
Conclusion: Considering the increase of 70 (funnelliformis mosseae) and 63 (rhizophagus intraradices) percent of plant dry weight in contaminated soil in presence of mycorrhiza, as well as the low price of these fungi inoculum (80,000 Rials per kilogram at the time of purchase), the use of this microorganism can be a suitable solution in soils contaminated with heavy metals in greenhouse conditions.

Keywords

آقابابایی، فاطمه؛ رییسی، فایز و حسین‌پور، علیرضا (1394). اثر کرم خاکی و قارچ میکوریزا بر شکل‌های شیمیایی کادمیم در خاک‌های تحت کشت آفتابگردان. پژوهش‌های کاربردی زراعی (پژوهش و سازندگی). 108، 153-159.
آموزگار، مهدیه؛ عباسپور، علی؛ شاهسونی، شاهین؛ اصغری، حمیدرضا و پارسائیان، مهدیه (1394). تأثیر کاربرد کودهای فسفره و هم‌زیستی قارچ میکوریز با گیاه آفتابگردان بر قابلیت دسترسی سرب در یک خاک آلوده. نشریه علوم آب و خاک (علوم و فنون کشاورزی و منابع طبیعی). 19 (74)، 39-50.
امانی‌فر، ستاره؛ علی اصغرزاده، ناصر؛ نجفی، نصرت اله؛ اوستان، شاهین و بلندنظر، صاحبعلی (1391). اثر قارچ های میکوریز آربوسکولار بر گیاه پالایی سرب توسط سورگوم (.Sorghum bicolor L). دانش آب و خاک (دانش کشاورزی). 22 (1)، 155-170.
بهرامی‌نیا، محبوبه؛ زارعی، مهدی؛ رونقی، عبدالمجید و قاسمی، رضا (1394). کارایی قارچ‌های میکوریز آربوسکولار در گیاه‌پالایی یک خاک آهکی آلوده به روی به‌وسیله گیاه وتیور. مجله آب و خاک. 28 (6)، 1228-1237.
لطفی، فائزه؛ فتوت، امیر؛ خراسانی، رضا و بحرینی طوحان، مهدی (1396). اثر ماده آلی بر توزیع شکل‌های شیمیایی کادمیم در خاک در محیط ریشه ذرت. مجله آب و خاک. 31 (6)، 1611-1622.
 
References
Aghababaei F., Raiesi F., & Hosseinpur, A. R. (2014a). The combined effects of earthworms and arbuscular mycorrhizal fungi on microbial biomass and enzyme activities in a calcareous soil spiked with cadmium. Applied Soil Ecology, 75, 33-42. https://doi.org/10.1016/j.apsoil.2013.10.006.
Aghababaei F., Raiesi F., & Hosseinpur, A. R. (2014b). The influence of earthworm and mycorrhizal co-inoculation on Cd speciation in a contaminated soil. Soil Biology and Biochemistry, 78, 21-29. https://doi.org/10.1016/j.soilbio.2014.06.010.
Aghababai F., Raeisi, F., & Hosseinpour, A. R (2014). Effect of soil worm and mycorrhiza on chemical forms of cadmium in sunflower soils. Journal of Agriculture (Research and Construction), 108, 159-153. (In Persian).
Amanifar, S., Ali Asgharzad, N., Najafi, N. A., Ostan, S. H., & Bolandnazar, P. (2010). The effect of arbuscular mycorrhizal fungi on lead purification by Sorghum (Sorghum bicolor L.). Journal of Soil and Water Knowledge, 22(1), 155-170. (In Persian).
Amoozgar, M., Abbaspour, A., Shahsoni, SH., Asghari, H. R., & Parsaiyan, M. (2015). The effect of phosphorus fertilizer application and coexistence of mycorrhizal fungus with sunflower on lead availability in a contaminated soil. Journal of Water and Soil (Agricultural Science and Technology and Natural Resources), 19(74), 39-50. (In Persian).
Bahraminia, M., Zarei, M., Ronaghi, A., & Ghasemi, R. (2014). Efficacy of arbuscular mycorrhizal fungi in phytoremediation of a zinc-contaminated calcareous soil by vetiver. Journal of Water and Soil (Agricultural Sciences and Industries), 28(6), 1228-1237. (In Persian).
Chen L., Hu X., Yang W., Xu Z., Zhang D., & Gao, S. (2015). The effects of arbuscular mycorrhizal fungi on sex-specific responses to Pb pollution in Populus cathayana. Ecotoxicology and environmental safety, 113, 460-468.https://doi.org/10.1016/j.ecoenv.2014.12.033.
Dehghanian, H., Halajnia, A., Lakzian, A., & Astaraei, A. R. (2018). The effect of earthworm and arbuscular mycorrhizal fungi on availability and chemical distribution of Zn, Fe and Mn in a calcareous soil. Applied Soil Ecology, 130, 98-103. https://doi.org/10.1016/j.apsoil.2018.06.002.
Diaz Franco, A., Alvarado Carrillo, M., Ortiz Chairez, F., & Grageda Cabrera, O. (2013). Plant nutrition and fruit quality of pepper associated with arbuscular mycorrhizal in greenhouse.  Revista Mexicana de Ciencias Agrícolas, 4, 315-321. https://doi.org/10.1017/S0021859615000714.
Gao, S., Luo, T. C., Zhang, B. R., Zhang, H. F., Han, Y., Zhao, Z. D., & Hu, Y. K. (1998). Chemical composition of the continental crust as revealed by studies in East China. Geochimica etCosmochimica Acta, 62, 1959-1975.https://doi.org/10.1016/S0016-7037(98)00121-5.
Gil, C., Ramos-Miras, J., Roca-Perez, L., & Boluda, R. (2010). Determination and assessment of mercury content in calcareous soils. Chemosphere, 78, 409-415. https://doi.org/10.1016/j.chemosphere.2009.11.001
Giovannetti, M., Sbrana, C., & Logi, C. (1994). Early processes involved in host recognition by Arbuscular mycorrhizal fungi. New Phytologist, 127, 703-709. https://doi.org/10.1111/j.1469-8137.1994.tb02973.x.
Huang, Y., Tao, S., & Chen, Y. (2005). The role of arbuscular mycorrhiza on change of heavy metal speciation in rhizosphere of maize in wastewater irrigated agriculture soil. Journal of Environmental Science, 17, 276-280.
Huang, Y., Ting, L. I., Huang, Z. J., & Ying-Heng, F. E. I. (2008). Ectomycorrhizal fungus-induced changes of Cu and Cd speciation in the rhizosphere of Chinese pine seedlings. Pedosphere, 18, 758-765. https://doi.org/10.1016/S1002-0160(08)60071-5.
Huo, J., Dong, A., Niu, X., Dong, A., Lee, S. Ma, C., & Wang, L. (2018). Effects of cadmium on oxidative stress activities in plasma of freshwater turtle Chinemys reevesii. Environmental Science and Pollution Research, 25, 8027-8034.https://doi.org/10.1007/s11356-017-1139-z.
Jankong, P., & Visoottiviseth, P. (2008). Effects of arbuscular mycorrhizal inoculation on plants growing on arsenic contaminated soil. Chemosphere, 72, 1092-1097. https://doi.org/10.1016/j.chemosphere.2008.03.040.
Jiang, Q. Y., Zhuo, F., Long, S. H., Zhao, H. D., Yang, D. J., Ye, Z. H., Li, S. S., & Jing, Y. X. (2016). Can arbuscular mycorrhizal fungi reduce Cd uptake and alleviate Cd toxicity of Lonicera japonica grown in Cd-added soils? Scientific reports, 6, 1-9.
Jones, J. B. (2001). Laboratory Guide for Conduction Soil Tests and Plant Analysis. Boca Raton: CRC press. https://doi.org/10.1201/9781420025293.
Kartal, S., Aydın, Z., & Tokalıoglu, S. (2006). Fractionation of metals in street sediment samples by using the BCR sequential extraction procedure and multivariate statistical elucidation of the data. Journal of Hazardous Materials, 132, 80-89. https://doi.org/10.1016/j.jhazmat.2005.11.091.
Kaschuk, G., Kuyper, T. W., Leffelaar, P. A., Hungria, M., & Giller, K. E. (2009). Are the rates of photosynthesis stimulated by the carbon sink strength of rhizobial and arbuscular mycorrhizal symbioses? Soil Biology and Biochemistry, 41, 1233-1244. https://doi.org/10.1016/j.soilbio.2009.03.005.
Li, X., & Christie, P. (2001). Changes in soil solution Zn and pH and uptake of Zn by arbuscular mycorrhizal red clover in Zn-contaminated soil. Chemosphere, 42(2), 201-207. https://doi.org/10.1016/s0045-6535(00)00126-0.
Li, X., & Thornton, I. (2001). Chemical partitioning of trace and major elements in soils contaminated by mining and smelting activities. Applied Geochemistry, 16, 1693-1706. https://doi.org/10.1016/S0883-2927(01)00065-8.
Liu, L., Li, J., Yue, F., Yan, X., Wang, F., Bloszies, S., & Wang, Y. (2018). Effects of arbuscular mycorrhizal inoculation and biochar amendment on maize growth, cadmium uptake and soil cadmium speciation in Cd-contaminated soil. Chemosphere, 194, 495-503. https://doi.org/10.1016/j.chemosphere.2017.12.025.
Lotfi, F., Fotovat, A., Khorasani R., & Bahraini Tuhan, M. (2017). Effect of organic matter on the distribution of chemical forms of cadmium in soil in maize root environment. Journal of Water and Soil (Agricultural Sciences and Industries). 31(6), 1622-1611. (In Persian).
Luo N., Li, X., Chen, A. Y., Zhang, L. J., Zhao, H. M., Xiang, L., Cai, Q. Y., Mo, C. H., Wong, M. H., & Li, H. (2017). Does arbuscular mycorrhizal fungus affect cadmium uptake and chemical forms in rice at different growth stages? Science of the Total Environment, 599-600, 1564-1572. https://doi.org/10.1016/j.scitotenv.2016.07.124.
Muthukrishnan, G., Gopalasubramaniam, S. K., & Perumal, P. (2018). Prospects of arbuscular mycorrhizal fungi for heavy metal-polluted soil management. Microorganisms for Green Revolution. 2, 91-113. https://doi.org/10.1007/978-981-10-7146-1_5.
Nyamangara, J. (1998). Use of sequential extraction to evaluate zinc and copper in a soil amended with sewage sludge and inorganic metal salts. Agriculture, Ecosystems and Environment, 69, 135-141. https://doi.org/10.1016/S0167-8809(98)00101-7.
Olsen S. R., & Sommers L. E. (1982). Phosphorus, In Methods of Soil Analysis, part 2, Chemical and Microbiological Properties. edited by Page A. L. Madison: American Society of Agronomy, Soil Science Society of America.
Orlowska, E., Przyby1owicz, W., Orlowski, D., Turnau, K., & Mesjasz-Przyby1owicz, J. (2011). The effect of mycorrhiza on the growth and elemental composition of Ni-hyperaccumulating plant Berkheya coddii Roessler. Environmental Pollution, 159, 3730-3738. https://doi.org/10.1016/j.envpol.2011.07.008.
Pawlowska, T. E., & Charvat, I. (2004). Heavy-metal stress and developmental patterns of arbuscular mycorrhizal fungi. Applied and Environmental Microbiology, 70, 6643-6649. https://doi.org/10.1128/AEM.70.11.6643-6649.
Philips, J. M., & Hayman, D. S. (1970). Improved procedures for cleaning roots and staining parasitic and vesicular arbuscular mycorrhizal fungi for rapid assessment of infection. Transactions of the British Mycological Society, 55, 158-161. https://doi.org/10.1016/S0007-1536(70)80110-3.
Rodrıguez, L., Ruiz, E., Alonso-Azcarate J., & Rincon, J. (2009). Heavy metal distribution and chemical speciation in tailings and soils around a Pb–Zn mine in Spain. Journal of Environmental Management, 90, 1106-1116. https://doi.org/10.1016/j.jenvman.2008.04.007.
Sekara, A., Poniedzialek, M., Ciura, J., & Jedrszczyk, E. (2005). Cadmium and lead accumulation and distribution in the organs of nine crops: implications for phytoremediation. Polish Journal of Environmental Studies, 14, 509-516.
Shahabivand, S., Maivan, H. Z., Goltapeh, E. M., Sharifi, M., & Aliloo, A. A. (2012). The effects of root endophyte and arbuscular mycorrhizal fungi on growth and cadmium accumulation in wheat under cadmium toxicity. PlantPhysiology and Biochemistry, 60, 53-58. https://doi.org/10.1016/j.plaphy.2012.07.018.
Sheetal, K. R., Singh, S. D., Anand, A., & Prasad, S. (2016). Heavy metal accumulation and effects on growth, biomass and physiological processes in mustard. Indian Journal of Plant Physiology, 21, 219-223. https://doi.org/10.1007/s40502-016-0221-8.
Subramanian, K. S., Tenshia, V., Jayalakshmi, K., & Ramachandran, V. (2009). Biochemical changes and zinc fractions in arbuscular mycorrhizal fungus (Glomus intraradices) inoculated and uninoculated soils under differential zinc fertilization. Applied Soil Ecology, 43, 32-39. https://doi.org/10.1016/j.apsoil.2009.05.009.
Tessier, A., Campbell, P. G., & Bisson, M. (1979). Sequential extraction procedure for the speciation of particulate trace metals. Analytical Chemistry, 51, 844–851. https://doi.org/10.1021/ac50043a017.
Ul-Kalam, S., Naushin, F., Bagyaraj, D. J., & Khan, F. A. (2019). Role of AM fungi in the uptake and accumulation of Cd and Ni by Luffa aegyptiaca. Water, Air, and Soil Pollution, 13, 230-266. https://doi.org/10.1007/s11270-019-4295-6.
Walkley A., & Black, I. A. (1934). An examination of the Degtjareff method for determining soil organic matter, and a proposed modification of the chromic acid titration method. Soil Science, 37(1), 29-38.
Wang, F. Y., Lin, X. G., & Yin, R. (2007). Role of microbial inoculation and chitosan in phytoextraction of Cu, Zn, Pb and Cd by Elsholtzia splendens a field case. Environmental Pollution, 147, 248-255. https://doi.org/10.1016/j.envpol.2006.08.005.
Wang, J., Zhang, C., & Jin, Z. (2009). The distribution and phytoavailability of heavy metal fractions in rhizosphere soils of Paulowniu fortunei (seem) Hems near a Pb/Zn smelter in Guangdong, PR China. Geoderma, 148(3), 229-306. https://doi.org/10.1016/j.geoderma.2008.10.015.
Yang, Y., He, C., Huang, L., Ban, Y., & Tang, M. (2017). The effects of arbuscular mycorrhizal fungi on glomalin-related soil protein distribution, aggregate stability and their relationships with soil properties at different soil depths in lead-zinc contaminated area. PloS one, 12(8), 1-19. https://doi.org/10.1371/journal.pone.0182264.
Zhan, F., Li, B., Jiang, M., Yue, X., He, Y., Xia, Y., & Wang, Y. (2018). Arbuscular mycorrhizal fungi enhance antioxidant defense in the leaves and the retention of heavy metals in the roots of maize. Environmental Science and Pollution Research, 25, 24338-24347. https://doi.org/10.1007/s11356-018-2487-z.
Zhang, H. H., Tang, M., Chen, H., Zheng, C., & Niu, Z. (2010). Effect of inoculation with AM fungi on lead uptake, translocation and stress alleviation of Zea mays L. seedlings planting in soil with increasing lead concentrations. European Journal of Soil Biology, 46, 306-311. https://doi.org/10.1016/j.ejsobi.2010.05.006.