Contact Us

For Marketing, Sales and Subscriptions Inquiries
2637 E Atlantic Blvd #43110
Pompano Beach, FL 33062

Conference List

Interactive Effects of Zinc-Arbuscular Mycorrhizal (AM) Fungi on Cadmium Uptake, Rubisco, Osmolyte Synthesis and Yield in Cajanus cajan (L.) Millsp.

Harmanjit Kaur


Neera Garg

Harmanjit Kaur 1
Neera Garg 2

  1. Department of Botany, Akal University, Bathinda, India. 1

  2. Department of Botany, Panjab University, Chandigarh, India. 2

on Google Scholar
on PubMed

Pages: 17-42

DOI: 10.18488/journal.70.2021.81.17.42

Share :

Article History:

Received: 19 October, 2020
Revised: 09 November, 2020
Accepted: 30 November, 2020
Published: 14 December, 2020


Cadmium (Cd) and Zinc (Zn) are two closely associated chemical elements having varied biological roles. Cd is a non-essential noxious element whereas Zn is an indispensable micronutrient at low concentrations but toxic to plants at higher levels. At the root surface, Cd competes with Zn for the same transmembrane carriers and Zn reduces Cd uptake in plants. Arbuscular mycorrhizal (AM) fungi are considered potential biotechnological approach for increasing plant tolerance to Cd-polluted soils. Applications of Zn and AM fungal inoculations might augment metal tolerance by reducing Cd uptake through their interactive effects. Thus, experiments were carried out to investigate the interplay between Zn (500 and 1000 mg kg-1 dry soil) and AM fungus [Funneliformis mosseae (T.H. Nicolson & Gerd.) C. Walker & A. Schüßler] on growth, nutrient management, photosynthetic efficiency, osmotic equilibrium and productivity in two pigeonpea (Cajanus cajan (L.) Millsp.) genotypes (Tolerant- Sel 85N and Sensitive- P792) exposed to Cd stress (25 and 50 mg kg-1 dry soil). Results revealed that accumulation of Cd and Zn individually reduced plant dry matter, total chlorophyll contents, Rubisco activity and nutrient uptake resulting in loss of yield, with Cd proving to be more toxic. However, Zn and AM reduced Cd uptake and their combined treatments enhanced plant biomass, photosynthetic ability and harvest index (HI) significantly by providing osmotic balance (total soluble sugars, free amino acids, proline, glycine betaine). The effects were more discernible in Sel 85N than P792 which could be directly correlated with its better ability for mycorrhizal colonization under stress.
Contribution/ Originality
This study documents concomitant application of Zn and AM fungi as an economically feasible strategy in increasing the tolerance as well as yield potential of pigeonpea genotypes subjected to Cd stress by improving photosynthetic ability, nutrient status and osmoprotection.


Chlorophyll, Funneliformis mosseae, Heavy Metals, Nutrient, Productivity, Proline.


Abad, A. K. J., & Khara, H. (2010). Effects of arbuscular mycorrhizal fungus (Glomus veruciforme) on changes of some physiological parameters in cadmium treated wheat plants. Pakistan Journal of Biological Sciences, 10, 4279-4282.Available at: 10.3923/pjbs.2007.4279.4282.

Adamczyk-Szabela, D., Katarzyna, L., Zdzisława, R.-D., & Wolf, W. M. (2020). Combined cadmium-zinc interactions alter manganese, lead, copper uptake by Melissa officinalis. Scientific Reports (Nature Publisher Group), 10, 1675.Available at:

Aghajanzadeh, T. A., Prajapati, D. H., & Burow, M. (2020). Differential partitioning of thiols and glucosinolates between shoot and root in Chinese cabbage upon excess zinc exposure. Journal of Plant Physiology, 244, 153088.

Ali, H., Khan, E., & Ilahi, I. (2019). Environmental chemistry and ecotoxicology of hazardous heavy metals: Environmental persistence, toxicity, and bioaccumulation. Journal of Chemistry, 1-14.Available at:

Anjum, N. A., Singh, H. P., Khan, M. I. R., Masood, A., Per, T. S., Negi, A., . . . Pereira, E. (2015). Too much is bad—an appraisal of phytotoxicity of elevated plant-beneficial heavy metal ions. Environmental Science and Pollution Research, 22(5), 3361-3382.Available at:

Arnon, D. (1949). E949. Copper enzymes in chloroplasts. Polyphenoh oxidases in Beta vuignris. Plant Physiol, 24, 1-15.Available at:

Arumugam, R., Rajasekaran, S., & Nagarajan, S. (2010). Response of Arbuscular mycorrhizal fungi and Rhizobium inoculation on growth and chlorophyll content of Vigna unguiculata (L) Walp Var. Pusa 151. Journal of Applied Sciences and Environmental Management, 14(4), 113-115.Available at: 10.4314/jasem.v14i4.63282.

Asgharipour, M., Khatamipour, M., & Razavi-Omrani, M. (2011). Phytotoxicity of cadmium on seed germination, early growth, proline and carbohydrate content in two wheat varieties. Advances in Environmental Biology, 5(4), 559-565.

Ayako, N.-Y., Yabuta, Y., & Shigeoka, S. (2008). The contribution of carbohydrates including raffinose family oligosaccharides and sugar alcohols to protection of plant cells from oxidative damage. Plant Signaling & Behavior, 3(11), 1016-1018.Available at: 10.4161/psb.6738.

Bates, L. (1973). Waldren. F. apiddetennmation of free proline for water stress study Plnrrt Sorl, 33, 205-208.Available at:

Begum, N., Qin, C., Ahanger, M. A., Raza, S., Khan, M. I., Ahmed, N., . . . Zhang, L. (2019). Role of arbuscular mycorrhizal fungi in plant growth regulation: Implications in abiotic stress tolerance. Frontiers in Plant Science, 10, 1-15.Available at: 10.3389/fpls.2019.01068.

Biró, I., Nemeth, T., & Takács, T. (2009). Changes of parameters of infectivity and efficiency of different glomus mosseae arbuscular mycorrhizal fungi strains in cadmium-loaded soils. Communications in Soil Science and Plant Analysis, 40(1-6), 227-239.Available at:

Bradford, N. (1976). A rapid and sensitive method for the quantitation microgram quantities of a protein isolated from red cell membranes. Anal Biochem, 72, 248-254.Available at: 10.1006/abio.1976.9999.

Burleigh, S. H., & Bechmann, I. E. (2002). Plant nutrient transporter regulation in arbuscular mycorrhizas. Plant and Soil, 244(1-2), 247-251.

Carrenho, R., Alves, L. D. J., & Santos, I. D. S. (2018). Arbuscular mycorrhizal fungi, interactions with heavy metals and rehabilitation of abandoned mine lands. In: Prasad, M.N.V., Favas, P. de Campos., Maiti, S.K. (Eds), Bio-Geotechnologies for Mine Site Rehabilitation (pp. 261-279). USA: Elsevier.

Chapman, H. D., & Pratt, P. F. (1961). Methods of analysis for soils, plants and waters. Division of Agricultural Sciences (pp. 150-210). Berkley, USA: University of California.

Chen, S., Zhao, H., Zou, C., Li, Y., Chen, Y., Wang, Z., . . . Ahammed, G. J. (2017). Combined inoculation with multiple arbuscular mycorrhizal fungi improves growth, nutrient uptake and photosynthesis in cucumber seedlings. Frontiers in Microbiology, 8, 25–16.Available at: 10.3389/fmicb.2017.02516.

Cherif, I., Mediouni, C., Ben Ammar, W., & Jemal, F. (2011). Interactions of zinc and cadmium toxicity in their effects on growth and in antioxidative systems in tomato plants (Solanum lycopersicon). Journal of Environmental Sciences, 23(7), 837-844.Available at: 10.1016/s1001-0742(10)60415-9.

Clemens, S. (2001). Developing tools for phytoremediation: Towards a molecular understanding of plant metal tolerance and accumulation. International Journal of Occupational Medicine and Environmental Health, 14(3), 235-239.

Coccina, A., Cavagnaro, T. R., Pellegrino, E., Ercoli, L., McLaughlin, M. J., & Watts-Williams, S. J. (2019). The mycorrhizal pathway of zinc uptake contributes to zinc accumulation in barley and wheat grain. BMC Plant Biology, 19(1), 1-14.

Cui, G., Ai, S., Chen, K., & Wang, X. (2019). Arbuscular mycorrhiza augments cadmium tolerance in soybean by altering accumulation and partitioning of nutrient elements, and related gene expression. Ecotoxicology and Environmental Safety, 171, 231–239.Available at:

Doidy, J., Grace, E., Kühn, C., Simon-Plas, F., Casieri, L., & Wipf, D. (2012). Sugar transporters in plants and in their interactions with fungi. Trends in Plant Science, 17, 413-422.Available at:

Dražić, G., Mihailović, N., & Stojanović, Z. (2004). Cadmium toxicity: the effect on macro-and micro-nutrient contents in soybean seedlings. Biologia Plantarum, 48(4), 605-607.

El-Beltagi, H. S., Mohamed, A. A., & Rashed, M. M. (2010). Response of antioxidative enzymes to cadmium stress in leaves and roots of radish (Raphanus sativus L.). Notulae Scientia Biologicae, 2(4), 76-82.

El-Beltagi., H. S., & Mohamed, H. I. (2013). Alleviation of cadmium toxicity in Pisum sativum L. seedlings by calcium chloride. Notulae Botanicae Horti Agrobotanici, 41, 157–168.Available at:

Fair, P., Tew, J., & Cresswell, C. (1973). Enzyme activities associated with CO2 exchange in illuminated leaves of Hordeum vulgare L. effect of light period, leaf age and position on CO2 compensation point. Annals of Botany, 37(4), 831-844.

Feigl, G., Molnár, Á., Szőllősi, R., Ördög, A., Törőcsik, K., Oláh, D., . . . Kolbert, Z. (2019). Zinc-induced root architectural changes of rhizotron-grown B. napus correlate with a differential nitro-oxidative response. Nitric Oxide, 90, 55-65.Available at: 10.1016/j.niox.2019.06.003.

Ferrol, N., Tamayo, E., & Vargas, P. (2016). The heavy metal paradox in arbuscular mycorrhizas: From mechanisms to biotechnological applications. Journal of Experimental Botany, 67(6253–6265).Available at: 10.1093/jxb/erw403.

Fodor, F., Gáspár, L., Morales, F., Gogorcena, Y., Lucena, J. J., Cseh, E., . . . Sárvári, É. (2005). Effects of two iron sources on iron and cadmium allocation in poplar (Populus alba) plants exposed to cadmium. Tree Physiology, 25(9), 1173-1180.Available at: 10.1093/treephys/25.9.1173.

Garcia, K., & Zimmermann, S. (2014). The disregarded mycorrhizal contribution to plant potassium nutrition. Frontiers in Plant Science, 5, 337.Available at: 10.3389/fpls.2014.00337.

Garg, N., & Kaur, H. (2013). Response of antioxidant enzymes, phytochelatins and glutathione production towards Cd and Zn stresses in Cajanus cajan (L.) Millsp. genotypes colonized by arbuscular mycorrhizal fungi. Journal of Agronomy and Crop Science, 199(2), 118-133.Available at:

Garg, N., & Singh, S. (2018). Arbuscular mycorrhiza Rhizophagus irregularis and silicon modulate growth, proline biosynthesis and yield in Cajanus cajan L. Millsp.(pigeonpea) genotypes under cadmium and zinc stress. Journal of Plant Growth Regulation, 37(1), 46-63.Available at:

Giovannetti, M., & Mosse, B. (1980). An evaluation of techniques for measuring vesicular arbuscular mycorrhizal infection in roots. New Phytol, 84, 489–500.Available at:

Gonçalves, J. F., Antes, F. G., Maldaner, J., Pereira, L. B., Tabaldi, L. A., Rauber, R., . . . de Moraes Flores, E. M. (2009). Cadmium and mineral nutrient accumulation in potato plantlets grown under cadmium stress in two different experimental culture conditions. Plant Physiology and Biochemistry, 47(9), 814-821.Available at: 10.1016/j.plaphy.2009.04.002.

Grieve, C., & Grattan, S. (1983). Rapid assay for determination of water soluble quaternary ammonium compounds. Plant and Soil, 70(2), 303-307.

Gupta, A. K., & Sinha, S. (2006). Chemical fractionation and heavy metal accumulation in the plant of Sesamum indicum (L.) var. T55 grown on soil amended with tannery sludge: Selection of single extractants. Chemosphere, 64(1), 161-173.Available at:

Hasanuzzaman, M., Banerjee, A., Bhuyan, M. B., Roychoudhury, A., Al Mahmud, J., & Fujita, M. (2019). Targeting glycinebetaine for abiotic stress tolerance in crop plants: physiological mechanism, molecular interaction and signaling. Phyton, 88(3), 185-221.Available at: 10.32604/phyton.2019.07559.

Hashem, A., Abd_Allah, E. F., Alqarawi, A. A., Aldubise, A., & Egamberdieva, D. (2015). Arbuscular mycorrhizal fungi enhances salinity tolerance of Panicum turgidum Forssk by altering photosynthetic and antioxidant pathways. Journal of Plant Interactions, 10(1), 230-242.Available at:

Helgason, T., & Fitter, A. H. (2009). Natural selection and the evolutionary ecology of the arbuscular mycorrhizal fungi (Phylum Glomeromycota). Journal of Experimental Botany, 60(9), 2465-2480.

Hidelbrant, U., Regvar, M., & Bothe, H. (2007). Asbuscular micorrhiza and heavy metals tolerance. Phytochemisty, 68, 138-146.Available at: 10.1016/j.phytochem.2006.09.023.

Hiscox, J., & Israelstam, G. (1979). Different methods of chlorophyll extraction. Canadian Journal of Chemistry, 57, 1332-1334.Available at:

Huang, Z., Zhao, L., Chen, D., Liang, M., Liu, Z., Shao, H., & Long, X. (2013). Salt stress encourages proline accumulation by regulating proline biosynthesis and degradation in Jerusalem artichoke plantlets. PLoS ONE, 8, e62085.Available at: 10.1371/journal.pone.0062085.

Huang, X., Ho, S.-H., Zhu, S., Ma, F., Wu, J., Yang, J., & Wang, L. (2017). Adaptive response of arbuscular mycorrhizal symbiosis to accumulation of elements and translocation in Phragmites australis affected by cadmium stress. Journal of Environmental Management, 197, 448-455.Available at:

Irigoyen, J., Einerich, D., & Sánchez-Díaz, M. (1992). Water stress induced changes in concentrations of proline and total soluble sugars in nodulated alfalfa (Medicago sativd) plants. Physiologia Plantarum, 84(1), 55-60.Available at:

Islam, M. M., Hoque, M. A., Okuma, E., Jannat, R., Banu, M. N. A., Jahan, M. S., . . . Murata, Y. (2009). Proline and glycinebetaine confer cadmium tolerance on tobacco bright yellow-2 cells by increasing ascorbate-glutathione cycle enzyme activities. Bioscience, Biotechnology, and Biochemistry, 73, 2320-2323.Available at:

Ismael, M. A., Elyamine, A. M., Moussa, M. G., Cai, M., Zhao, X., & Hu, C. (2019). Cadmium in plants: uptake, toxicity, and its interactions with selenium fertilizers. Metallomics, 11(2), 255-277.Available at:

Jacobsen, I., Smith, S. E., & Smith, F. A. (2002). Function and diversity of arbuscular mycorrhizae in carbon and mineral nutrition,” In: M. G. A. van der heijden and I. R. Sanders (Eds.) Mycorrhizal ecology (pp. 75-92). New York: Springer-Verlag Berlin, Heidelberg.

Jain, R., Srivastava, S., S. Solomon, Shrivastava, A. K., & Chandra, A. (2010). Impact of excess zinc on growth parameters, cell division, nutrient accumulation, photosynthetic pigments and oxidative stress of sugarcane (Saccharum spp.). Acta Physiologiae Plantarum, 32, 979-986.Available at: 10.1007/s11738-010-0487.

Jaleel, C. A., Changxing, Z., Jayakumar, K., & Iqbal, M. (2009). Low concentration of cobalt increases growth, biochemical constituents, mineral status and yield in Zea mays. Journal of Scientific Research, 1(1), 128-137.Available at: 10.3329/jsr.v1i1.1226.

Jia-Dong, H., Tao, D., Hui-Hui, W., Zou, Y. N., Wu, Q. S., & Kamil, K. (2019). Mycorrhizas induce diverse responses of root TIP aquaporin gene expression to drought stress in trifoliate orange. Scientia Horticulturae, 243, 64–69.Available at:

Kanwal, S., Bano, A., & Malik, R. N. (2015). Effects of arbuscular mycorrhizal fungi on metals uptake, physiological and biochemical response of Medicago sativa L. with increasing Zn and Cd concentrations in soil. American Journal of Plant Sciences, 6(18), 2906-2923.Available at: 10.4236/ajps.2015.618287.

Karcz, W., & Kurtyka, R. (2007). Effect of cadmium on growth, proton extrusion and membrane potential in maize coleoptile segments. Biologia Plantarum, 51(4), 713-719.Available at:

Kaur, H., & Garg, N. (2017). Zinc-arbuscular mycorrhizal interactions: effect on nutrient pool, enzymatic antioxidants, and osmolyte synthesis in pigeonpea nodules subjected to Cd stress. Communications in Soil Science and Plant Analysis, 48(14), 1684-1700.Available at:

Khan, K., Moses, S., & Kumar, A. (2017). Physical properties of pigeon pea grains at different moisture content. International Journal of Pure and Applied Bioscience, 5(2), 556-562.Available at: .

Kolahi, M., Kazemi, E. M., Yazdi, M., & Goldson-Barnaby, A. (2020). Oxidative stress induced by cadmium in lettuce (Lactuca sativa Linn.): Oxidative stress indicators and prediction of their genes. Plant Physiology and Biochemistry, 146, 71-89.Available at:

Koleva, L., Semerdjieva, I., Nikolova, A., & Vassilev, A. (2010). Comparative morphological and histological study on zinc-and cadmium-treated durum wheat plants with similar growth inhibition. General and Applied Plant Physiology, 36(1/2), 8-11.

Krishnamoorthy, R., Kim, C.-G., Subramanian, P., Kim, K.-Y., Selvakumar, G., & Sa, T.-M. (2015). Arbuscular mycorrhizal fungi community structure, abundance and species richness changes in soil by different levels of heavy metal and metalloid concentration. PLoS One, 10(6), e0128784.Available at:

Kumar, P., Lucini, L., Rouphael, Y., Cardarelli, M., Kalunke, R. M., & Colla, G. (2015). Insight into the role of grafting and arbuscular mycorrhiza on cadmium stress tolerance in tomato. Frontiers in Plant Science, 6, 1-16.Available at: 10.3389/fpls.2015.00477.

Laspina, N., & Groppa, M. (2005). Nitric oxide protects sunflower leaves against Cd-induced oxidative stress. Plant Sci, 169, 323-330.Available at:

Lee, Y. P., & Takahashi, T. (1966). An improved colorimetric determination of amino acids with the use of ninhydrin. Analytical Biochemistry, 14(1), 71-77.Available at:

Lee, K. R., & Roh, K. S. (2003). Influence of cadmium on rubisco activation inCanavalia ensiformis L. leaves. Biotechnology and Bioprocess Engineering, 8(2), 94-100.Available at:

Leport, L., Turner, N. C., Davies, S., & Siddique, K. (2006). Variation in pod production and abortion among chickpea cultivars under terminal drought. European Journal of Agronomy, 24(3), 236-246.Available at:

Li, T., Hu, J. L., Hao, Z. P., Li, H., Wang, Y. S., & Chen, B. D. (2013). First cloning and characterization of two functional aquaporin genes from an arbuscular mycorrhizal fungus Glomus intraradices. New Phytol, 197, 617–630.Available at: 10.1111/nph.12011.

Lindner, R. (1944). Rapid analytical methods for some of the more common inorganic constituents of plant tissues. Plant Physiology, 19(1), 76-89.Available at:

Liu, Z., He, X., Chen, W., Yuan, F., Yan, K., & Tao, D. (2009). Accumulation and tolerance characteristics of cadmium in a potential hyperaccumulator- Lonicera japonica Thunb. Journal of Hazardous Materials, 169, 170-175.Available at:

Liu, C. (2011). Effects of cadmium and salicylic acid on growth, spectral reflectance and photosynthesis of castor bean seedlings. Plant Soil, 344(1), 131-141.

Liu, Z., Chen, W., & He, X. (2011). Cadmium-induced changes in growth and antioxidative mechanisms of a medicine plant (Lonicera japonica Thunb.). Journal of Medicinal Plants Research, 5(8), 1411-1417.Available at:

Maggio, A., Miyazaki, S., Veronese, P., Fujita, T., Ibeas, J. I., Damsz, B., . . . Bressan, R. A. (2002). Does proline accumulation play an active role in stress-induced growth reduction? The Plant Journal, 31(6), 699-712.Available at: 10.1046/j.1365-313x.2002.01389.x.

Meena, M., Divyanshu, K., Kumar, S., Swapnil, P., Zehra, A., Shukla, V., . . . Upadhyay, R. (2019). Regulation of L-proline biosynthesis, signal transduction, transport, accumulation and its vital role in plants during variable environmental conditions. Heliyon, 5(12), e02952.Available at: 10.1016/j.heliyon.2019.e02952.

Mehlich, A. (1953). Determination of P, Ca, Mg, K, Na and NH4 (pp. 16). North Carolina Soil Test Division, Department of Agriculture, Raleigh, North Carolina, Mimeo 1953.

Miyasaka, S. C., Habte, M., Friday, J. B., & Johnson, E. V. (2003). Manual on arbuscular mycorrhizal fungus production and inoculation techniques (pp. 4). Honolulu (HI): University of Hawaii. (Soil and Crop Management; SCM-5).

Muneer, S., Qadri, T. N., & Siddiqi, T. (2011). Cytogenetic and biochemical investigations to study the response of Vigna radiata to cadmium stress. African Journal of Plant Science, 5(3), 183-192.Available at:

Mysliwa-Kurdziel, B., Prasad, M. N. V., & Strzalka, K. (2004). Photosynthesis in metal stressed plants,” In: M. N. V. Prasad (Ed) Heavy metal stress in plants: From biomolecules to ecosystems (2nd ed., pp. 146-181). Heidelberg, Narosa, New Delhi: Springer-Verla.

Nayuki, K., Chen, B., Ohtomo, R., & Kuga, Y. (2014). Cellular imaging of cadmium in resin sections of arbuscular mycorrhizas using synchrotron micro X-ray fluorescence. Microbes and Environments, 29(60), 60-66.

Nelson, D. W., & Sommers, L. E. (1980). Total nitrogen analysis of soil and plant tissues. Journal of the Association of Official Analytical Chemists, 63(4), 770-778.Available at:

Olsen, S. R., & Sommers, L. E. (1982). Phosphorus,” In: A. L. Page, (Ed) Methods of soil analysis, Agron. No. 9, Part 2: Chemical and microbiological properties (2nd ed.). Madison, WI, USA: American Society of Agronomy.

Pathak, G. C., Gupta, B., & Pandey, N. (2012). Improving reproductive efficiency of chickpea by foliar application of zinc. Brazilian Journal of Plant Physiology, 24(3), 173-180.Available at:

Perveen, R., Faizan, S., Tiyagi, S. A., & Kausar, S. (2011). Performance of Cd stress condition on growth and productivity parameters of Trigonella foenum-graecum Linn. World Journal of Agricultural Sciences, 7(5), 607-612.

Phillips, J. M., & Hayman, D. S. (1970). Improved procedures for clearing and staining parasitic and vesicular–arbuscular mycorrhizal fungi for rapid assessment of infection. Transactions of the British Mycological Society, 55, 158-161.Available at:

Qiu, Q., Wang, Y., Yang, Z., & Yuan, J. (2011). Effects of phosphorus supplied in soil on subcellular distribution and chemical forms of cadmium in two Chinese flowering cabbage (Brassica parachinensis L.) cultivars differing in cadmium accumulation. Food and Chemical Toxicology, 49(9), 2260-2267.Available at: 10.1016/j.fct.2011.06.024.

Rask, K. A., Johansen, J. L., Kjøller, R., & Ekelund, F. (2019). Differences in arbuscular mycorrhizal colonisation influence cadmium uptake in plants. Environmental and Experimental Botany, 162, 223-229.Available at: 10.1016/j.envexpbot.2019.02.022.

Rivera-Becerril, F., van Tuinen, D., Martin-Laurent, F., Metwally, A., Dietz, K.-J., Gianinazzi, S., & Gianinazzi-Pearson, V. (2005). Molecular changes in Pisum sativum L. roots during arbuscular mycorrhiza buffering of cadmium stress. Mycorrhiza, 16(1), 51-60.Available at: 10.1007/s00572-005-0016-7.

Schubler, A., & Walker, C. (2010). The Glomeromycota: A species list with new families and genera,” Edinburgh & Kew, UK, The Royal Botanic Garden; Munich, Germany: Botanische Staatssammlung Munich and Oregon. USA: Oregon State University.

Senbayram, M., Gransee, A., & Wahle, V. (2015). Role of magnesium fertilisers in agriculture: Plant–soil continuum. Crop & Pasture Science, 66, 1219-1229.Available at:

Sharma, S. S., & Dietz, K. J. (2006). The significance of amino acids and amino acid-derived molecules in plant responses and adaptation to heavy metal stress. Journal of Experimental Botany, 57, 711-726.Available at:

Shekoofeh, E., Sepideh, H., & Roya, R. (2012). Role of mycorrhizal fungi and salicylic acid in salinity tolerance of Ocimum basilicum resistance to salinity. African Journal of Biotechnology, 11, 2223–2235.Available at: 10.5897/AJB11.1672.

Sheng, M., Tang, M., Chan, H., Yang, B., Zhang, F., & Huang, Y. (2008). Influence of arbuscular mycorrhizae on photosynthesis and water status of maize plants under salt stress. Mycorrhiza, 18, 287–296.Available at:

Shukla, U., Murthy, R., & Kakkar, P. (2008). Combined effect of ultraviolet-B radiation and cadmium contamination on nutrient uptake and photosynthetic pigments in Brassica campestris L. seedlings. Environmental Toxicology: An International Journal, 23(6), 712-719.Available at: 10.1002/tox.20378.

Srivastava, R., Khan, R., Manzoor, N., & Mahmooduzzafar. (2011). Responses of cadmium exposures on growth, physio-biochemical characteristics and the antioxidative defence system of soybean. Journal Phytol, 3(10), 20-25.

Tandon, P. K., & Srivastava, M. (2004). Effect of cadmium and nickel on metabolism during early stages of growth in gram (Cicer arietinum L.) seeds. Indian Journal of Agricultural Biochemistry, 17(1), 31-34.

Thompson, A. R., & Vierstra, R. D. (2005). Autophagic recycling: Lessons from yeast help define the process in plants. Current Opinion in Plant Biology, 8(2), 165-173.

Van der Heijden, E. W., & Kuyper, T. W. (2001). Does origin of mycorrhizal fungus or mycorrhizal plant influence effectiveness of the mycorrhizal symbiosis? Plant and Soil, 230(2), 161-174.Available at:

Vassilev, A., Perez-Sanz, A., Cuypers, A., & Vangronsveld, J. (2007). Tolerance of two hydroponically grown Salix genotypes to excess zinc. Journal of Plant Nutrition, 30(9), 1471-1482.Available at:

Vijayaragavan, M., Prabhahar, C., Sureshkumar, J., Natarajan, A., Vijayarengan, P., & Sharavanan, S. (2011). Toxic effect of cadmium on seed germination, growth and biochemical contents of cowpea (Vigna unguiculata L.) plants. International multidisciplinary research journal, 1(5), 1-6.

Walkley, A. (1947). A critical examination of a rapid method for determining organic carbon in soils—effect of variations in digestion conditions and of inorganic soil constituents. Soil Science, 63(4), 251-264.

Wang, H., Zhao, S., Liu, R., Zhou, W., & Jin, J. (2009). Changes of photosynthetic activities of maize (Zea mays L.) seedlings in response to cadmium stress. Photosynthetica, 47(2), 277-283.Available at:

Whetherley, P. (1950). Studies in the water relations of cotton plants. I. The field measurement of water deficit in leaves. New Phytol., 49, 81-87.Available at:

Wu, N., Li, Z., Wu, F., & Tang, M. (2016). Comparative photochemistry activity and antioxidant responses in male and female Populus cathayana cuttings inoculated with arbuscular mycorrhizal fungi under salt. Scientific Reports, 6, 37663.Available at:

Wu, C., Dun, Y., Zhang, Z., Li, M., & Wu, G. (2020). Foliar application of selenium and zinc to alleviate wheat (Triticum aestivum L.) cadmium toxicity and uptake from cadmium-contaminated soil. Ecotoxicology and Environmental Safety, 190, 110091.Available at: 10.1016/j.ecoenv.2019.110091.

Xu, J., Sun, J., Du, L., & Liu, X. (2012). Comparative transcriptome analysis of cadmium responses in Solanum nigrum and Solanum torvum. New Phytologist, 196(1), 110-124.

Yang, L. P., Zhu, J., Wang, P., Zeng, J., Tan, R., Yang, Y. Z., & Liu, Z. M. (2018). Effect of Cd on growth, physiological response, Cd subcellular distribution and chemical forms of Koelreuteria paniculata. Ecotoxicology and Environmental Safety, 160, 10-18.Available at: 10.1016/j.ecoenv.2018.05.026.

Yousuf, P. Y., Ahmad, H. A., Ganie, A. H., Aref, I. M., & Iqbal, M. (2015). Potassium and calcium application ameliorates growth and oxidative homeostasis in salt stressed Indian mustard (Brassica juncea) Plants. Pakistan Journal of Botany, 47(5), 1629–1639.

Zaefarian, F., Rezvani, M., Rejali, F., Ardakani, M. R., & Noormohammadi, G. (2011). Effect of heavy metals and arbuscular mycorrhizal fungal on growth and nutrients (N, P, K, Zn, Cu and Fe) accumulation of alfalfa (Medicago sativa L.). American-Eurasian Journal of Agricultural & Environmental Sciences, 11(3), 346-352.

Zare, A., Khoshgoftarmanesh, A., Malakouti, M., Bahrami, H., & Chaney, R. (2018). Root uptake and shoot accumulation of cadmium by lettuce at various Cd: Zn ratios in nutrient solution. Ecotoxicology and Environmental Safety, 148, 441-446.Available at: 10.1016/j.ecoenv.2017.10.045.

Zhang, S., Zhou, J., Wang, G., Wang, X., & Liao, H. (2015). The role of mycorrhizal symbiosis in aluminum and phosphorus interactions in relation to aluminum tolerance in soybean. Applied Microbiology and Biotechnology, 99, 10225–10235.Available at: 10.1007/s00253-015-6913-6.

Zhou, J., Cheng, K., Huang, G., Chen, G., Zhou, S., Huang, Y., . . . Fan, H. (2020). Effects of exogenous 3-indoleacetic acid and cadmium stress on the physiological and biochemical characteristics of Cinnamomum camphora. Ecotoxicology and Environmental Safety, 191, 109998.Available at:

Zhu, G., Xiao, H., Guo, Q., Zhang, Z., Zhao, J., & Yang, D. (2018). Effects of cadmium stress on growth and amino acid metabolism in two Compositae plants. Ecotoxicology and Environmental Safety, 158, 300-308.Available at: 10.1016/j.ecoenv.2018.04.045.

Zouari, M., Ahmed, C. B., Zorrig, W., Elloumi, N., Rabhi, M., Delmail, D., . . . Abdallah, F. B. (2016). Exogenous proline mediates alleviation of cadmium stress by promoting photosynthetic activity, water status and antioxidative enzymes activities of young date palm (Phoenix dactylifera L.). Ecotoxicology and Environmental Safety, 128, 100-108.Available at: 10.1016/j.ecoenv.2016.02.015.


Google Scholor ideas Microsoft Academic Search bing Google Scholor


This study received financial support from University Grants Commission (UGC), New Delhi, India [grant number 42-945/2013(SR)].

Competing Interests:

The authors declare that they have no competing interests.


Both authors contributed equally to the study conception and experimental design.

Related Article

( 1 ) Interactive Effects of Arbuscular Mycorrhizal Fungi and Rhizobium on Growth and Nutrient Content of Arachis hypogaea
( 2 ) Interactive Effects of Zinc-Arbuscular Mycorrhizal (AM) Fungi on Cadmium Uptake, Rubisco, Osmolyte Synthesis and Yield in Cajanus cajan (L.) Millsp.
( 3 ) Effects of Cotton Gin Trash Level on the Performance of Desert Lambs in New Halfa Area, Kassala State, Sudan
( 4 ) Effects of Age at Fattening On Butana Camel Males Carcass Characteristics in the Sudan
( 5 ) Germination Effects of Purposive Bruchid Screening of African Ebony (Dalbergia Melanoxylon) Seeds In the Arid and Semi-Arid Region of South Eastern Kenya
( 6 ) Effects of Ebola (EVD) Outbreak on Bush Meat Marketing and Consumption in Ibarapa Central Local Government Area of Oyo State, Nigeria
( 7 ) Effects of Degasified Extender on Quality Parameters of Cryopreserved Bull Spermatozoa
( 8 ) Effects of Dried Rumen Contents Level in Rations on the Performance of Shugor Desert Sheep in Halfa Elgadeda, Kassala State, Sudan
( 9 ) Physiological Effects of Some Artificial and Natural Food Coloring on Young Male Albino Rats
( 10 ) Protective Effects of Sweet Orange Peel (Citrus Sinensis L.) The Induction of Micronuclei Induced by Cyclophosphamide in Human Peripheral Lymphocytes
( 11 ) Analysis of Climate Change Effects among Rice Farmers in Benue State, Nigeria
( 12 ) The Effects of Magnetic Field on Germination of Seeds and Growth of Seedlings of Stone Pine
( 13 ) Effects of Segregated Early Weaning at 7 Days on Dams Body Condition, Parturition Interval and Offspring Birth Weight and Litter Size in the Agouti (Dasyprocta Leporina) for Intensive Production
( 14 ) Rural Farmers’ Coping Strategies to Effects of Climate Change on Watermelon Production in Igboora, Oyo State, Nigeria
( 15 ) Effects of Different Storage Conditions on Rooting and Shooting Performance of Grapevine (Vitis Vinifera L.) Cuttings in Hydroponic Culture System
( 16 ) Effects of Community Financing Institutions on Cassava Farmers Income in Oyo State, Nigeria
( 17 ) Effects of Inclusion of Processed Grapefruit Pulp on Wheat Flour Biscuit
( 18 ) Effects of Melon Seed or Soybean Meal Supplementation on the Physicochemical and Sensory Properties of Incompletely Peeled Cassava Garri
( 20 ) Storage Effects on Microbiological and Some Antioxidant Potentials of Partially Substituted Bread Produced from Wheat Flour and Fresh Coconut Meat
( 21 ) Assessment of the Processing Effects of Fresh Solanum Anguivi Berries on Biochemical Contents and Functional Properties of Powder
( 22 ) Preservative Effects of Ginger (Zingiber officinale), Tumeric (Curcuma longa) Extract and Citric Acid and Pasteurization on the Nutritional Quality and Shelf Life of Tiger-Nut Non-Dairy Milk
( 25 ) Improvement of Maize Productivity (Zea Mays L.) by Mycorrhizal Inoculation on Ferruginous Soil in Center of Benin
( 29 ) Effect of Fungi and Manure on Cadmium Content and Biomass of Maize Grown In Cadmium Contaminated Tailing from Bangka Indonesia
( 30 ) Effect of Contamination by Fungi and Yeast on the Physiochemical Characteristics of Gum Arabic Stored in Semi-Desert Climate of Khartoum City, Sudan
( 31 ) The Effect of Varieties and Fungicide Spray Frequencies on Septoria Leaf Blotch (Mycosphaerella graminicola) Epidemics on Bread Wheat in Western Amhara, Ethiopia
( 32 ) The Fungicide and Variety Integration Effect on Late Blight (Phytophthora infestans) Disease of Potato (Solanum tuberosum L.) in Western Amhara Region, Ethiopia
( 40 ) Synthesis of Biodiesel from Tropical Almond (Terminalia Catappa) Seed Oil
( 42 ) Effect of Different Sources of Fertilizers on the Yield and Yield Components of Wheat Variety Kohat-2000 Under Rainfed Conditions of Kohat During 2012
( 43 ) GGE and Ammi Biplot Analysis for Field PEA Yield Stability in Snnpr State, Ethiopia
( 44 ) Effect of Different Types of Surfectants on Zinc Efficiency in Spinach Yield
( 45 ) Evaluation of Field Pea (Pisum Sativum L) Genotypes Performance for Yield and Yield Components at Five Growing Environments of Southern Ethiopia
( 46 ) Characterization and Association among Yield and Yield Related Traits in Sunflower (Helianthus Annus L) Genotypes
( 47 ) Association between Yield Components of Sorghum (Sorghum Bicolor L. (Moench) Under Different Watering Intervals
( 48 ) Effect of Sowing Date on Maize Seed Yield and Quality: A Review
( 49 ) Comparative Growth Analysis and Yield Performance of Glycine Max under Jatropha Curcas Based Agrisilviculture System of Agroforestry in the Northern Part of Bangladesh
( 50 ) Correlation between Milk Yield, Somatic Cell Count and Milk Quality in Dairy Farming
( 51 ) Stover Yield and Chemical Composition in Some Sorghum Varieties in Gadarif State, Sudan
( 52 ) Genotype X Environment Interaction and Stability Analysis for Yield and Yield Related Traits of Desi-Type Chickpea (Cicer Arietinum L.) In Ethiopia
( 53 ) Effect of Intra Spacing on Yield and Yield Components of Carrot (Daucus Carrota L.Sub Sp. Sativus)
( 54 ) Genotypic Difference in Growth and Yield Related Traits of Onion (Allium Cepa L.) Varieties at Southern Tigray
( 55 ) Study on Agronomic Evaluation of Tomato (Lycopersicon Esculentum, Mill.) Varieties for Phonological, Growth and Yield Characters
( 56 ) Effect of Integrated Application of Poultry Manure and Chemical NP Fertilizers on Growth, Yield and Yield Components of Highland Maize Variety on Vertisol at Ambo University on Station, Ethiopia
( 57 ) Evaluation of Different Tillage Practices on Growth and Yield of Fluted Pumpkin Telfairia Occidentalis in Uyo, Southeastern Nigeria
( 58 ) Heterosis for Nitrogen Fixation and Seed Yield and Yield Components in Chickpea (Cicer arietinum L.)
( 59 ) Molecular Characterization of Parental Lines of Rice Aiming to Address High Yield and Nutritional Quality Under Drought and Cold Stress Condition
( 60 ) Harvesting Date Influences Cassava (Manihot Esculenta Crantz) Yield and Quality of Based-Products