اثر کادمیوم بر رشد و جذب برخی عناصر غذایی در گیاه یونجه همزیست با Rhizophagus intraradices

نوع مقاله : مقاله پژوهشی

نویسنده

استادیار گروه علوم خاک، دانشگاه علوم کشاورزی و منابع طبیعی گرگان

چکیده

هدف پژوهش، ارزیابی اثر سطوح کادمیوم بر رشد، جذب عناصر فسفر، آهن، روی، مس و منگنز در گیاه یونجه همزیست با قارچ Rhizophagus intraradices بود. آزمایش گلدانی به صورت فاکتوریل بر پایه طرح کاملاً تصادفی شامل دو سطح قارچ (تلقیح و عدم تلقیح با قارچR. intraradices ) و چهار سطح کادمیوم (0، 15، 30 و 45 میکرومولار کادمیوم) در سه تکرار انجام گردید. وزن خشک شاخسارها و ریشه گیاهان تلقیح‏شده با AM (M) و تلقیح‏نشده (NM) تحت تاثیر کادمیوم قرار گرفت. وزن خشک شاخسارها و ریشه در سطوح 15، 30 و 45 میکرومولار کادمیوم، به‏ترتیب کاهش 0، 2/8، 25 و 5/9، 2/16 و 8/39 درصدی نسبت به شاهد داشتند. وزن خشک شاخسارها و ریشه گیاهان M به‏ترتیب 7/48 و 8/42 درصد بیشتر از گیاهان NM بود. اثر قارچ بر جذب فسفر شاخسارها و ریشه معنی‏دار گردید. جذب فسفر شاخسارها و ریشه گیاهان M به‏ترتیب 1/54 و 6/49 درصد بیشتر از گیاهان NM بود. اثر کادمیوم بر درصد کلونیزاسیون ریشه و وابستگی مایکوریزی گیاه معنی‏دار گردید. در سطوح 15 و 30 میکرومولار کادمیوم، درصد کلونیزاسیون ریشه و وابستگی مایکوریزی به‏ترتیب افزایش 2/38، 7/35 و 100، 77 درصدی نسبت به تیمار شاهد داشتند. بیشترین کادمیوم جذب‏شده در شاخسارها و ریشه به‏ترتیب در تیمار مایکوریزی سطح 15و 45 میکرومولار کادمیوم بودند که افزایش 97/81 و 99/71 درصدی نسبت به تیمار غیرمایکوریزی در همان سطوح داشتند. با افزایش غلظت کادمیوم، از انتقال کادمیوم ریشه به شاخسارها کاسته شد. در تمام سطوح کادمیوم، مقدار آهن، روی، مس و منگنز غالباً در ریشه‏ها بیشتر از شاخسارها بود. به‏طورکلی، با افزایش غلظت کادمیوم، جذب آهن، روی، مس و منگنز در گیاه نسبت به شاهد کاهش یافت. در سطوح کادمیوم نسبت به شاهد، انتقال آهن، روی و منگنز از ریشه به شاخسارها کاهش و در مورد مس افزایش یافت.

کلیدواژه‌ها


عنوان مقاله [English]

The effect of Cadmium on growth and some nutrient uptake in alfalfa plant inoculated by Rhizophagus intraradices

نویسنده [English]

  • Elham Malekzadeh
Assistant Professor, Department of Soil Science, Gorgan university of Agricultural Science and Natural Resources
چکیده [English]

The main objective of the current research was to evaluate the effect of Cd concentrations on the growth, uptake of P, Fe, Zn, Cu and Mn of alfalfa plant mycorrhized by Rhizophagus intraradices. A pot culture experiment was performed as completely randomized design by two factors, including AM fungus (inoculated with R. intraradices and non-inoculated) and four levels of Cd (0, 15, 30 and 45 µM Cd+2) with three replications. Shoot and root dry weights of mycorrhizal (M) and non-mycorrhizal (NM) plants were affected by increasing of Cd levels. At the levels of 15, 30 and 45 µM Cd+2 shoot and root dry weights were decreased by 0%, 8.2%, 25% and 9.5%, 16.2%, 39.8% compared to the control (0 µM Cd+2), respectively. Shoot and root dry weights of M plants were increased by 48.7% and 42.8% 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 54.1% and 49.6% compared to the NM ones. Root colonization and mycorrhizal dependency were affected by Cd treatments. At the levels of 15 and 30 µM Cd+2, root colonization and mycorrhizal dependency were increased by 38.2%, 35.7% and 100%, 77% compared to the control, respectively. Maximum Cd contents of shoot and root were recorded at the levels of 15 and 45 µM Cd+2 in M plants which were increased by 81.97% and 71.99% respectively, compared to the NM ones at the same levels. Cd-translocation from root to shoot was decreased as the Cd concentration increased. At the all levels of Cd, the concentrations of Fe, Zn, Cu and Mn were often higher in roots than in shoots. Generally, with increasing Cd concentration, plant uptake of Fe, Zn, Cu and Mn were decreased compared to the control. At the Cd levels, metal translocation from root to shoot were decreased for Fe, Zn and Mn and increased for Cu compared to the control, respectively.

کلیدواژه‌ها [English]

  • Soil pollution
  • Micronutrients
  • Heavy metals
  • Arbuscular mycorrhizal fungi
  • Forage crop
Abbaspour A., Kalbasi M., Haj Rasouliha Sh., and Golchin Ahmad. 2006. Investigation of contamination in some agricultural soils of Iran with cadmium and lead. 9th Iranian Soil Science Congress, Soil Conservation and Watershed Management, Research Center, Tehran, Iran. (In persian)
Ali N.A., Pilar Bernal M., and Ater M. 2004. Tolerance and bioaccumulation of cadmium by Phragmites australis grown in the presence of elevated concentrations of cadmium, copper, and zinc. Aquatic Botany, 80:163-176.
Amir H., Lagrange A., Hassaïne N., and Cavaloc Y. 2013. Arbuscular mycorrhizal fungi from New Caledonian ultramafic soils improve tolerance to nickel of endemic plant species. Mycorrhiza, 23: 585-595.
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.
Aravind P., Prasad M.N.V., Malec P., Waloszek A., and Strzaka K. 2009. Zinc protects Ceratophyllum demersum L. (free-floatingh ydrophyte) against reactive oxygen species induced by cadmium. Journal of Trace Elements in Medicine and Biology, 23: 50–60.
Audet P., and Charest C. 2006. Effects of AM colonization on ‘wild tobacco’ grown in zinc contaminated soil. Mycorrhiza, 16 (4): 277-283.
Balen B., Tkalec M., Šikić S., Tolić S., Cvjetko P., Pavlica M., and Vidakovic-Cifrek Z. 2011. Biochemical responses of Lemna minor experimentally exposed to cadmium and zinc. Ecotoxicology, 20: 815–826.
Baszynski T., Wajda L., Krol M., Wolinska D., Krupa Z., and Tukendorf A. 1980. Photosynthetic activities of cadmium-treated tomato plants. Physiologia Plantarum, 48: 365–370.
Bissonnette L., St-Arnaud M., and Labrecque M. 2010. Phytoextraction of heavy metals by two Salicaceae clones in symbiosis with arbuscular mycorrhizal fungi during the second year of a field trial. Plant and Soil, 332: 55–67.
Cakmak I.H., and Marschner H. 1986. Mechanism of phosphorus induced zinc deficiency in cotton. I. Zinc deficiency-enhanced uptake rate of phosphorus. Physiologia Plantarum, 68: 483–490.
Cataldo D.A., Garland T.R., and Wildung R.E. 1998. Cadmium uptake kinetics in intact soybean plants. Plant Physiology, 73:844–848.
Chen B.D., Zhu Y.G., and Smith F.A. 2006. Effects of arbuscularmycorrhizal inoculation on uranium and arsenic accumulation by Chinese brake fern (Pteris vittata L.) from a uranium mining-impacted soil. Chemosphere, 62: 1464–1473.
Citterio S., Prato N., Fumagalli P., Aina R., Massa N., Santagostino A., Sgorbati S., and Berta G. 2005. The arbuscular mycorrhizal fungus Glomus mosseae induces growth and metal accumulation changes in Cannabis sativa L. Chemosphere, 59:21–29.
Clemens S. 2006. Toxic metal accumulation, responses to ex­posure and mechanisms of tolerance in plants. Biochimie, 88: 1707–1719.
Cottenie, A. 1980. Methods of Plant Analysis. In: Soil and Plant Testing. NO. 38/2. FAO Soils Bulletin, pp. 94-100.
Cozzolino V., Perelomov L., Caporale A.G., and Pigna M. 2010. Mobility and bioavailability of heavy metals and metalloids in soil environments. Journal of Soil Science and Plant Nutrition, 10: 268–292.
De Maria S., Puschenreiter M., and Rivelli A.R. 2013. Cadmium accumulation and physiological response of sunflower plants to Cd during the vegetative growing cycle. Plant, Soil and Environment, 59: 254–261.
Dinakar N., Nagajyothi P.C., Suresh S., Udaykiran Y., and Damodharam T. 2008. Phytotoxicity of cadmium on protein, proline and antioxidant enzyme activities in growing Arachis hypogaea L. seedling. Journal of Environmental Science, 20: 199-206.
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.
Ferrol N., Tamayo E., and Vargas P. 2016. The heavy metal paradox in arbuscular mycorrhizas: from mechanisms to biotechnological applications. Journal of Experimental Botany, 67 (22): 6253-6265.
Food and Agricultural Organization (FAO). 1999. Summary and conclusions. In: 53rd Meeting, Rome, 1-10 June, Rome, pp.123-130.
Gerdemann J.W., and Nicolson T.H. 1963. Spores of mycorrhizal endogen species extracted from soil by wet-sieving and decanting. Transactions of the British Mycological Society, 46: 235-244.
Ghaderian S.M., and Jamali Hajiani N. 2010. The evaluation of tolerance and accumulation of cadmium in Matthiola chenopodiifolia. Iranian Journal of Botanical Biology, 6(8): 87-98.
Gharineh M.H., Haydari M., and Nadian H. 2012. Interactive effects of salinity and mycorrhizal colonization on some heavy metals uptake by saffron plant (Crocus sativus L.). International Conference on Agriculture, Chemical and Environmental Sciences (ICACES’2012) Oct. 6–7, Dubai (UAE).
Gohre V., and Paszkowski U. 2006. Contribution of the arbuscular mycorrhizal symbiosis to heavy metal phytoremediation. Planta, 223: 1115–1122.
Gomes M.P., Marques T.C.L.L.S.M., Soares A.M. 2013. Cadmium effects on mineral nutrition of the Cd-hyperaccumulator Pfaffia glomerata. Biologia, 68 (2): 223-230.
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 extra radical mycelium and spores of the arbuscular mycorrhizal fungus Glomus intraradices. Canadian Journal of Microbiology, 54 (2): 103–10.
Gopal R., and Rizvi A.H. 2008. Excess lead alters growth, metabolism and translocation of certain nutrients in radish. Chemosphere, 70 (9): 1539-1544.
Grath M.C., Postma S.L. and Mc Cormeck R.J. 2000. Analysis of Irish sewage slug suitability of sludge for us in agriculture Irish. Agricultural and food Research, 39 (1): 73-78.
Hall J.L., and Williams L.E. 2004. Transition metal transporters in plants. Journal of Experimental Botany, 54: 2601–2613.
Hossain K. G., Islam N., Ghavami F., Durant C., Durant C., and Johnson M. 2017. Effect of increased amounts of Fe, Zn, and Cd uptake, translocation, and accumulation of human health related micronutrients in wheat. Asian Journal of Agriculture and Food Sciences, 5(1): 19-29.
Hossain M.A., Piyatida P., da Silva J.A.T., and Fujita M. 2012. Molecular mechanism of heavy metal toxicity and tolerance in plants: Central role of glutathione in detoxification of reactive oxygen species and methylglyoxal and in heavy metal chelation. Journal of Botany, 2:1-37.
Howard H. 2002. Human health and heavy metals exposure. In: McCally M. (Ed.), Life Support: The Environment and Human Health. MIT Press, pp. 1-13
Humphries J., Stangoulis J., and Graham R. 2007. Manganese. In: Barker A. and Pilbeam D. (Eds.), Handbook of Plant Nutrition. Taylor and Francis, USA, pp. 351–366.
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.
Jianfeng H., Xiangui L., Rui Y., and Yufang S. 2009. Effects of arbuscular mycorrhizal fungi inoculation on arsenic accumulation by tobacco (Nicotiana tabacum L.). Journal of Environmental Sciences, 21:1214–1220.
Jiang Q.Y., Zhuo F., Long S.H., Zhao H.D., Yang D.J., Ye Z.H., Li S.S., and Jing Y.X. 2016. Can arbuscular mycorrhizal fungi reduce Cd uptake and alleviate Cd of Lonicera japonica grown in Cd-added soils? Scientific Reports, 6: 21805; doi: 10.1038/srep21805.
Joner E.J., and Leyval C. 1997. Uptake of 109Cd by roots and hyphae of a Glomus mosseae/Trifolium subterraneum mycorrhiza from soil amended with high and low concentrations of cadmium. New Phytologist, 135(2): 353-360.
Kapoor R., and Bhatnagar A.K. 2007. Attenuation of cadmium toxicity in mycorrhizal celery (Apium graveolens L.). World Journal of Microbiology and Biotechnology, 23: 1083–1089.
Karimi A., Khodaverdiloo H., Sepehri M., and Rasouli Sadaghiani M.H. 2011. Arbuscular mycorrhizal fungi and heavy metal contaminated soils. African Journal of Microbiology Research, 5: 1571-1576.
Kormanik P.P., and McGraw A.C. 1982. Quantification of vesicular-arbuscular mycorrhizae in plant roots. In: Schenck N.C. (Ed.), Methods and Principles of Mycorrhizal Research. American Phytopathological Society, Saint Paul, MN. pp. 37-45.
Krämer U., Talke I.A., and Hanikenne M. 2007. Transition metal transport. FEBS Letters, 581: 2263–2272.
Lenoir, I., Fontaine, J., and Sahraoui, A.L.H. 2016. Arbuscular mycorrhizal fungal responses to abiotic stresses: a review. Phytochemistry, 123: 4–15.
Liu D.H., Wang M., Zon J.H., and Jiang W.S. 2006. Uptake and accumulation of cadmium and some nutrient ions by root and shoots of maize (Zea mays L.). Pakistan Journal of Botany, 38: 701 – 709.
Marquez A.P.G.C., Oliveira R.S., Samardjieva K.A., Pissarra J., Rangel A.O.S.S., and Castro P.M.L. 2008. EDDS and EDTA-enhanced zinc accumulation by Solanum nigrum inoculated with arbuscular mycorrhizal fungi grown in contaminated soil. Chemosphere, 70: 1002-1014.
Marschner P. 2012. Mineral Nutrition of Higher Plants. 3.Ed. Londres, Elsevier, 649p.
Millner P.D., and Kitt D.G. 1992. The Beltsville method for soilless production of vesicular arbuscular mycorrhizal fungi. Mycorrhiza, 2: 9-15.
Mozafar A., Ruh R., Kilingel P., Gamper H., Egli S., and Frossard E. 2002. Effect of heavy metal contaminated shooting range soils on mycorrhizal colonization of roots and metal uptake by leek. Environmental Monitoring and Assessment, 79: 177-191.
Nan Z., Li J., Zhang J., and Cheng Z. 2002. Cadmium and Zinc interactions and their transfer in soil-crop system under actual field conditions. Science of the Total Environment, 285:187–195.
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.
Olsson P.A., Thingstrup I., Jakobsen I., and Bååth E. 1999. Estimation of the biomass of arbuscular mycorrhizal fungi in a linseed field. Soil Biology Biochemistry, 31: 1879-1887.
Park S., and Ahn Y.J. 2016. Multiwalled carbon nanotubes and silver nanoparticles differentially affect seed germination, chlorophyll content and hydrogen peroxide accumulation in carrot (Daucus carota L.). Biocatalysis and Agricultural Biotechnology, 8: 257-262.
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.
Puga A.P., Abreu C.A., Melo L.C.A., and Beesley L. 2015. Biochar application to a contaminated soil reduces the availability and plant uptake of zinc, lead and cadmium. Journal of Environmental Management, 15: 86-93.
Punamiya P., Datta R., Sarkar D., Barber S., Patel M., and Da P. 2010. Symbiotic role of Glomus mosseae in phytoextraction of lead in vetiver grass (Chrysopogon zizanioides L.). Journal of Hazardous Materials, 177:465-474.
Rask K.A., Johansen J.L., Kjoller R., and Ekelund F. 2019. Differences in arbuscular mycorrhizal colonization influence cadmium uptake in plants. Environmental and Experimental Botany, 162: 223-229.
Ribera-Fonsecc A., Rumpel C., Mora M.D., Nikolic M., and Cartes P. 2013. Early induction of Fe-SOD gene expression is involved in tolerance to Mn toxicity in perennial ryegrass. Plant Physiology and Biochemistry, 73:77-82, 2013.
Romheld V., and Nikolic M. 2007. Iron. In: Barker A.V. and Pilbeam D.J. (Eds.), Handbook of Plant Nutrition-Chapter 11. CRC Press: Taylor and Francis Group, Boca Raton, pp. 329–350.
Saad E.H., Mohamed H., and Marc S.A. 2013. Effect of arbuscular mycorrhizal fungi on trace metal uptake by sunflower plants grown on cadmium contaminated soil. New Biotechnology, 30: 780-787.
Sahmurova A., Celik M., Allahverdiyev, S. 2010. Determination of the accumulator plants in Kucukcekmece Lake (Istanbul). African Journal of Biotechnology, 6(4): 6545-6551.
Salt D.E., and Rauser W.E. 1995. Mg-ATP-dependent transport of phytochelatins across the tonoplast of oat roots. Plant Physiology, 107: 1293–1301.
Sandalio L.M., Dalurzo H.C., Gomez, M. M., Romero-Puertas, C., and Del Rio, L.A. 2001. Cadmium-induced changes in the growth and oxidation metabolism of pea plants. Journal of Experimental Botany, 52(364): 2115-2126.
Sarwar N., Malhi S.S., Zia M.H., Naeem A., Bibi S., and Farid G. 2010. Role of mineral nutrition in minimizing cadmium accumulation by plants. Journal of the Science of Food and Agriculture, 90: 925–37.
Shahabivand S., Maivan H.Z., Goltapeh E.M., Sharifi M., and Aliloo A.A. 2012. The effects of root endophyte and arbuscular mycorrhizal fungi on growth and cadmium accumulation in wheat under cadmium toxicity. Plant Physiology and Biochemistry, 60: 53–58.
Shao G., Chen M., Wang W., Mou R., and Zhang G. 2007. Iron nutrition affects cadmium accumulation and toxicity in rice plants. Plant Growth Regulation, 53: 33–42.
Sharma S.S., and 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.
Sharma N.C., Gardea-Torresdey J.L., Parsons J., and Sahi S.V. 2004. Chemical speciation and cellular deposition of lead in Sesbania drummondii. Environmental Toxicology Chemistry, 23: 134.
Sinha P., Dube B., Srivastava P., and Chatterjee C. 2006. Alteration in uptake and translocation of essential nutrients in cabbage by excess lead. Chemosphere, 65(4): 651-656.
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.
Tabrizi L., Mohammadi S., Delshad M., and Motesharezadeh B. 2015. Effect of arbuscular mycorrhizal fungi on yield and phytoremediation performance of pot marigold (Calendula officinalis L.) under heavy metals stress. International Journal of Phytoremediation, 17(12): 1244-1252.
Tkalec M., Stefanic P.P., Cvjetko P., Sikic S., Pavlica M., Balen B. 2014. The effects of cadmium-zin interactions on biochemical responses in tobacco seedling and adult plants. PLoS ONE, 9(1): e87582. doi: 10.1371/journal.pone.0087582
Tawaraya k. 2003. Arbuscular mycorrhizal dependency of different plant species and cultivars. Soil Science and Plant Nutrition, 49 (5): 655-668.
Vallee B.L., and Falchuk H. 1993. The biochemical basis of zinc physiology. Physiological Reviews. 73: 79–117.
Wagner G. 1993. Accumulation of cadmium in crop plants and its consequences to human health. Advances in Agronomy, 51:173-211.
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, Netherland, 263p.
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.
Wang X., Zhang ZW., Tu SH., Feng WQ., Xu F., Zhu F., Zhang DW., Du JB., Yuan S., and Lin HH. 2013. Comparative study of four rice cultivars with different levels of cadmium tolerance. Biologia, 68 (1): 74-81.
Wang C., Zhang S.H., Wang P.F., Hou J., Zhang W.J., Li W., and Lin Z.P. 2009. The effect of excess Zn on mineral nutrition and antioxidative response in rapeseed seedlings. Chemosphere, 75: 1468–1476.
Webb M.J., and Loneragan J.F. 1990. Zinc translocation to wheat roots and its implications for phosphorus/zinc interaction in wheat plants. Journal of Plant Nutrition, 13: 1499–1512.
Whitfield L., Richards A.J., and Rimmer D.L. 2004. Relationships between soil heavy metal concentration and mycorrhizal colonization in Thymus polytrichus in northern England. Mycorrhiza Journal,14(1): 55-62.
Wu F.Y., Hu J.L., Wu S.C., and Wong M.H. 2015. Grain yield and arsenic uptake of upland rice inoculated with arbuscular mycorrhizal fungi in As-spiked soils. Environmental Science and Pollution Research, 22: 8919–8926.
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.
Yang M.G., Lin X.Y., and Yang X.E. 1998. Impact of Cd on growth and nutrient accumulation of different plant species. China Journal of Applied Ecology, 19:89–94.
Yao Q., Yang R., Long L., and Zhu, H 2013: Phosphate application enhances the resistance of arbuscular mycorrhizae in clover plants to cadmium via polyphosphate accumulation in fungal hyphae. Environmental and Experimental Botany, 108: 63–70.
Zhang X., Chen B., and Ohtomo R. 2015. Mycorrhizal effects on growth, P uptake and Cd tolerance of the host plant vary among different AM fungal species. Soil Science and Plant Nutrition, 61 (2): 359-368.
Zhang G.P., Fukami M., and Sekimoto H. 2002. Influence of cadmium on mineral concentration and yield components in wheat genotypes differing in Cd tolerance at seedling stage. Field Corp Research, 40(79): 1-7.
Zhang X., Gao B., and Xia H. 2014b. Effect of cadmium on growth, photosynthesis, mineral nutrition and metal accumulation of bana grass and vetiver grass. Ecotoxicology and Environmental Safety, 106:102-108.
Zhang X.H., Lin A.J., Chen B.D., Wang Y.S., Smith S.E., and Smith F.A. 2006. Effects of Glomus mosseae on the toxicity of heavy metals to Vicia faba. Journal of Environmental Sciences, 18: 721–726.
Zhang H.H., Tang M., and Zheng C. 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.
Zhang X., Zhang X., Gao B., Li Z., Xia H., Li H., and Li J. 2014a. Effect of cadmium on growth, photosynthesis, mineral nutrition and metal accumulation of an energy crop, king grass (Pennisetum americanum x P. purpureum). Biomass and Bioenergy, 67:179-187.
Zhiqiang X., Qixing Z., and Weitao L., 2009. Joint effects of cadmium and lead on seedlings of four Chinese cabbage cultivars in northeastern China. Environmental Sciences, 21: 1598-1606.
Zhi-Xin N., Li-na S., Tie-heng S., Yu-shuangL., and Hong W. 2007. Evaluation of phytoextracting cadmium and lead by sunflower, ricinus, alfalfa and mustard in hydroponic culture. Environmental Sciences, 19: 961-967.
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.