Environmental Science and Pollution Research

, Volume 24, Issue 15, pp 13452–13465 | Cite as

Effect of earthworms on growth, photosynthetic efficiency and metal uptake in Brassica juncea L. plants grown in cadmium-polluted soils

  • Parminder Kaur
  • Shagun Bali
  • Anket Sharma
  • Adarsh Pal Vig
  • Renu BhardwajEmail author
Research Article


The present study has been carried out to examine the role of earthworms in phytoremediation of Cd and its effect on growth, pigment content, expression of genes coding key enzymes of pigments, photosynthetic efficiency and osmoprotectants in Brassica juncea L. plants grown under cadmium (Cd) metal stress. The effect of different Cd concentrations (0.50, 0.75, 1.0, 1.25 mM) was studied in 30 and 60-day-old plants grown in soils containing earthworms. It was observed that earthworm inoculation showed stimulatory effect on phytoremediation capacity and Cd uptake has increased by 49% (in 30-day-old plants) and 35% (in 60-day-old plants) in shoots and 13.3% (in 30-day-old plants) and 10% (in 60-day-old plants) in roots in 30 and 60-day-old plants in Cd (1.25 mM) treatments. Plant growth parameters such as root and shoot length, relative water content and tolerance index were found to increase in the presence of earthworms. Recovery in photosynthetic pigments (chlorophyll and carotenoid) and gas exchange parameters, i.e. net photosynthetic rate (P n ), stomatal conductance (G s ), intercellular CO2 concentration (C i ) and transpiration rate (E t ), was observed after earthworm’s supplementation. Modulation in expression of key enzymes for pigment synthesis, i.e. chlorophyllase, phytoene synthase, chalcone synthase and phenylalanine ammonia lyase, was also observed. The results of our study revealed that earthworms help to mitigate the toxic effects produced by Cd on plant growth and photosynthetic efficiency along with enhanced phytoremediation capacity when co-inoculated with Cd in soil.


Chlorophyllase Tolerance index Stomatal conductance Phytoremediation Osmoprotectants Gene expression 



Research fellowship to the first author was provided by University Grants Commission, under the Maulana Azad National Fellowship (MANF) scheme. The authors are also thankful to the University Grants Commission, New Delhi, for establishing sophisticated instrumentation facilities in the university campus under the Universities with Potential for Excellence (UPE) scheme.


  1. Aghababaei F, Raiesi F (2015) Mycorrhizal fungi and earthworms reduce antioxidant enzyme activities in maize and sunflower plants grown in Cd-polluted. Soil Biol Biochem 86:87–97CrossRefGoogle Scholar
  2. Aghababaei F, Raiesi F, Hosseinpur A (2014) The significant contribution of mycorrhizal fungi and earthworms to maize protection and phytoremediation in Cd-polluted soils. Pedobiologia 57:223–233CrossRefGoogle Scholar
  3. Ahmad P, Nabi G, Ashraf M (2011) Cadmium-induced oxidative damage in mustard [Brassica juncea (L.) Czern.& Coss.] plants can be alleviated by salicylic acid. S Afr J Bot 77:36–44CrossRefGoogle Scholar
  4. Ahmad P, Sarwat M, Bhat NA, Wani MR, Kazi AG, Tran LS (2015) Alleviation of cadmium toxicity in Brassica juncea L. (Czern. & Coss.) by calcium application involves various physiological and biochemical strategies. PLoS One 10(1):e0114571. doi: 10.1371/journal.pone.0114571 CrossRefGoogle Scholar
  5. Allen SE, Grimshaw HM, Rowland AP (1976) Chemical analysis. In: Chapman SB (ed) Methods in plant ecology. Blackwell Scientific Publications, Oxford, pp 335–335Google Scholar
  6. Amirjani M (2012) Effects of cadmium on wheat growth and some physiological factors. IJFSE 2(1):50–58Google Scholar
  7. Anderson JM (1988) Spatiotemporal effects of invertebrates on soils processes. Biol Fertil Soil 6:216–227CrossRefGoogle Scholar
  8. Arnon DI (1949) Copper enzymes in isolated chloroplasts, polyphenoxidase in Beta vulgaris. Plant Physiol 24:1–15CrossRefGoogle Scholar
  9. Assche FV, Clijsters H (1990) Effects of metals on enzyme activity in plants. Plant Cell Environ 13(3):195–206CrossRefGoogle Scholar
  10. Azevedo H, Pinto G, Fernandes J, Loureiro S, Santos C (2005) Cadmium effects on sunflower: growth and photosynthesis. J Plant Nutr 28:2211–2220CrossRefGoogle Scholar
  11. Baek SA, Han T, Ahn SK, Kang H, Cho MR, Lee SC, Im KH (2012) Effects of heavy metals on plant growths and pigment contents in Arabidopsis thaliana. Plant Pathol J 28(4):446–452CrossRefGoogle Scholar
  12. Bali S, Poonam KSK, Kaur H, Bhardwaj R (2016) Improvement in photosynthetic efficiency of Brassica juncea under copper stress by plant steroid hormone. J Chem Pharma Res 8(5):464–470Google Scholar
  13. Balint AF, Röder MS, Hell R, Galiba G, Börner A (2007) Mapping of QTLs affecting copper tolerance and the Cu, Fe, Mn and Zn contents in the shoots of wheat seedlings. Biol Plant 51(1):129–134CrossRefGoogle Scholar
  14. Basheer M, Agrawal OP (2013) Effect of vermicompost on the growth and productivity of tomato plant (Solanum lycopersicum) under field conditions. Int J Recent Sci Res 3(4):247–249Google Scholar
  15. Bastardie F, Ruy S, Cluzeau D (2005) Assessment of earthworm contribution to soil hydrology: a laboratory method to measure water diffusion through burrow walls. Biol Fertil Soils 41:124–128CrossRefGoogle Scholar
  16. Bates LS, Waldren RP, Teare ID (1973) Rapid determination of free proline for water stress studies. Plant Soil 39:205–207CrossRefGoogle Scholar
  17. Bauddh K, Singh RP (2012) Cadmium tolerance and its phytoremediation by two oil yielding plants Ricinus communis (L.) and Brassica juncea (L.) from the contaminated soil. Int J Phytorem 14(8):772–785CrossRefGoogle Scholar
  18. Bernard F, Brulle F, Dumez S, Lemiere S, Platel A, Nesslany F, Cuny D, Deram A, Vandenbulcke F (2015) Antioxidant responses of Annelids, Brassicaceae and Fabaceae to pollutants: a review. Ecotox Environ safe 114:273–303CrossRefGoogle Scholar
  19. Bernard F, Dumez S, Brulle F, Lemière S, Platel A, Nesslany F, Cuny D, Deram A, Vandenbulcke F (2016) Antioxidant defense gene analysis in Brassica oleracea and Trifolium repens exposed to Cd and/or Pb. Environ Sci Poll Res 23(4):3136–3151CrossRefGoogle Scholar
  20. Berova M, Pevicharova G, Stoeva N, Zlatev Z, Karanatsidis G (2013) Vermicompost affects growth, nitrogen content, leaf gas exchange and productivity of pepper plants. J Elem:565–576Google Scholar
  21. Blanchart E, Albrecht A, Brown G, Decaens T, Duboisset A, Lavelle P, Mariani L, Roose E (2004) Effects of tropical endogeic earthworms on soil erosion. Agric Ecosyst Environ 104:303–315CrossRefGoogle Scholar
  22. Blouin M, Lavelle P, Laffray D (2007) Drought stress in rice (Oryza sativa L.) is enhanced in the presence of the compacting earthworm Millsonia anomala. Environ Exp Bot 60(3):352–359CrossRefGoogle Scholar
  23. Brulle F, Bernard F, Vandenbulcke F, Cuny D, Dumez S (2014) Identification of suitable qPCR reference genes in leaves of Brassica oleracea under abiotic stresses. Ecotoxicology 23(3):459–471CrossRefGoogle Scholar
  24. di Cagno R, Guidi L, Stefani A, Soldatini GF (1999) Effects of cadmium on growth of Helianthus annuus seedlings: physiological aspects. New Phytol 144:65–71CrossRefGoogle Scholar
  25. Chaneva G, Parvanova P, Tzvetkova N, Uzunova N (2010) Photosynthetic response of maize plants against cadmium and paraquat impact. Water Air Soil Pollut 208:287–293CrossRefGoogle Scholar
  26. Cheng J, Wong MH (2002) Effects of earthworms on Zn fractionation in soils. Biol Fertil Soils 36(1):72–78CrossRefGoogle Scholar
  27. Chen X, Wang J, Shi Y, Zhao MQ, Chi GY (2011) Effects of cadmium on growth and photosynthetic activities in pakchoi and mustard. Bot Stud 52(1): 41-46Google Scholar
  28. Dandan W, Huixin L, Feng H, Xia W (2010) Role of earthworm-straw interactions on phytoremediation of Cu contaminated soil by ryegrass. Acta Ecol Sin 27(4):1292–1298CrossRefGoogle Scholar
  29. Dias MC, Monteiro C, Moutinho-Pereira J, Correia C, Gonçalves B, Santos C (2013) Cadmium toxicity affects photosynthesis and plant growth at different levels. Acta Physiol Plant 35(4):1281–1289CrossRefGoogle Scholar
  30. Edwards CA, Bohlen PJ (1996) Biology and ecology of earthworms, thrid edn. Chapman and Hall, UKGoogle Scholar
  31. Fang Z, Bouwkamp JC, Solomos T (1998) Chlorophyllase activities and chlorophyll degradation during leaf senescence in non-yellowing mutant and wild type of Phaseolus vulgaris L. J Exp Bot 49:503–510Google Scholar
  32. Gómez-Brandón M, Lazcano C, Lores M, Domínguez J (2010) Detritivorous earthworms modify microbial community structure and accelerate plant residue decomposition. App Soil Ecol 44(3):237–244CrossRefGoogle Scholar
  33. Grieve CM, Grattan SR (1983) Rapid assay for determination of water soluble quaternary ammonium compounds. Plant Soil 70:303–307CrossRefGoogle Scholar
  34. Hashem HA (2013) Cadmium toxicity induces lipid peroxidation and alters cytokinin content and antioxidant enzyme activities in soybean. Botany 92:1–7. doi: 10.1139/cjb-2013-0164 CrossRefGoogle Scholar
  35. Hassan Z, Aarts MG (2011) Opportunities and feasibilities for biotechnological improvement of Zn, Cd or Ni tolerance and accumulation in plants. Environ Exp Bot 72(1):53–63CrossRefGoogle Scholar
  36. Honnerova J, Rothova O, Hola D, Kocova M, Kohout L, Kvasnica M (2010) The exogenous application of brassinosteroids to Zea mays (L) stressed by long term chilling does not affect the activities of photosystem 1 or 2. J Plant Growth Regul 29:500–505. doi: 10.1007/s00344-010-9153-0 CrossRefGoogle Scholar
  37. Iqbal N, Masood A, Nazar R, Syeed S, Khan NA (2010) Photosynthesis, growth and antioxidant metabolism in mustard (Brassica juncea L.) cultivars differing in cadmium tolerance. Agr Sci China 9(4):519–527CrossRefGoogle Scholar
  38. Jihen EH, Fatima H, Nouha A, Baati T, Imed M, Abdelhamid K (2010) Cadmium retention increase: a probable key mechanism of the protective effect of zinc on cadmium induced toxicity in the kidney. Toxicol Lett 196:104–109. doi: 10.3109/15376510903572888 CrossRefGoogle Scholar
  39. Kachout S, Mansoura B, Bouraoui K (2015) Effects of metal toxicity on growth and pigment contents of annual halophyte (A. hortensis and A. rosea). Int J Environ Res 9:613–620Google Scholar
  40. Keilig K, Ludwig-Müller J (2009) Effect of flavonoids on heavy metal tolerance in Arabidopsis thaliana seedlings. Bot Studies 50(3):311–318Google Scholar
  41. Khan NA, Nazar R, Anjum NA (2009) Growth, photosynthesis and antioxidantmetabolisminmustard (Brassica juncea L.) cultivars differing in ATP-sulfurylase activity under salinity stress. Sci Hort 122:455–460CrossRefGoogle Scholar
  42. Kim MS, Kim C, Jo DH, Ryu YW (1999) Effect of fungal elicitor and heavy metals on the production of flavonol glycosides in the cell cultures of Ginko biloba. J Microbiol Biotechnol 9:661–667Google Scholar
  43. Krantev A, Yordanova R, Janda T, Szalai G, Popova L (2008) Treatment with salicylic acid decreases the effect of cadmium on photosynthesis in maize plants. J Plant Physiol 165:920–931CrossRefGoogle Scholar
  44. Krishnapriya K, Padmadevi SN (2011) Effect of vermicompost on the growth and biochemical contents of Oryza sativa var. ponni. Asian J Environ Sci 6(2):168–170Google Scholar
  45. Küpper H, Küpper F, Spiller M (1996) Environmental relevance of heavy metal-substituted chlorophylls using the example of water plants. J Exp Bot 47(2):259–266CrossRefGoogle Scholar
  46. Lawrence JF (1990) Determination of total xanthophyll and marigold oleoresin. JAOAC Int 2:970–975Google Scholar
  47. Lee KE (1985) Earthworms: their ecology and relationships with soils and land use. Academic Press, Sydney, pp 224–411Google Scholar
  48. Lee YP, Takahashi T (1966) An improved colorimetric determination of amino acids with the use of ninhydrin. Anal Biochem 14(1):71–77CrossRefGoogle Scholar
  49. Li H, Li X, Dou Z, Zhang J, Wang C (2012) Earthworm (Aporrectodea trapezoides)– mycorrhiza (Glomus intraradices) interaction and nitrogen and phosphorus uptake by maize. Biol Fertil Soil 48:75–85CrossRefGoogle Scholar
  50. Liu C, Guo J, Cui Y, Lü T, Zhang X, Shi G (2011) Effects of cadmium and salicylic acid on growth, spectral reflectance and photosynthesis of castor bean seedlings. Plant Soil 344(1–2):131–141CrossRefGoogle Scholar
  51. Liu L, Sun H, Chen J, Zhang Y, Li D, Li C (2014) Effects of cadmium (Cd) on seedling growth traits and photosynthesis parameters in cotton (Gossypium hirsutum L.) Plant Omics J 7(4):284–290CrossRefGoogle Scholar
  52. Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2−11CT method. Methods 25:402–408CrossRefGoogle Scholar
  53. Ma Y, Dickinson NM, Wong MH (2002) Toxicity of Pb/Zn mine tailings to the earthworm Pheretima and the effects of burrowing on metal availability. Biol Fertil Soils 36:79–86CrossRefGoogle Scholar
  54. Macinelli AL (1984) Photoregulation of anthocyanin synthesis. VIII. Effects of light pretreatments. Plant Physiol 75:447–453CrossRefGoogle Scholar
  55. Maclachlan C, Zalik S (1963) Plastid structure, chlorophyll concentration and free amino acid composition of a chlorophyll mutant of barley. C J Bot 41:1053–1062CrossRefGoogle Scholar
  56. Milleret R, Le Bayon RC, Gobat JM (2009) Root, mycorrhizal and earthworm interactions: their effects on soil structuring processes, plant and soil nutrient concentration and plant biomass. Plant Soil 316:1–12CrossRefGoogle Scholar
  57. Mobin M, Khan NA (2007) Photosynthetic activity, pigment composition and antioxidative response of two mustard (Brassica juncea) cultivars differing in photosynthetic capacity subjected to cadmium stress. J Plant Physiol 164:601–610CrossRefGoogle Scholar
  58. Mohamed AA, Castagna A, Ranieri A, Sanità di Toppi L (2012) Cadmium tolerance in Brassica juncea roots and shoots is affected by antioxidant status and phytochelatin biosynthesis. Plant Physiol Biochem 57:15–22CrossRefGoogle Scholar
  59. Moody SA, Briones MJI, Piearce TG, Dighton J (1995) Selective consumption of decomposing wheat straw by earthworms. Soil Biol Biochem 27:1209–1213CrossRefGoogle Scholar
  60. Moosavi SA, Gharineh MH, Afshari RT, Ebrahimi A (2012) Effects of some heavy metals on seed germination characteristics of canola (Barassica napus), wheat (Triticum aestivum) and safflower (Carthamus tinctorious) to evaluate phytoremediation potential of these crops. J Agr Sci 4(9):11Google Scholar
  61. Muradoglu F, Gundogdu M, Ercisli S, Encu T, Balta F, Jaafar HZE, Zia-Ul-Haq M, Muradoglu F (2015) Cadmium toxicity affects chlorophyll a and b content, antioxidant enzyme activities and mineral nutrient accumulation in strawberry. Biol Res 48:11CrossRefGoogle Scholar
  62. Muscolo A, Felici M, Concheri G, Nardi S (1993) Effect of earthworm humic substances on esterase and peroxidase activity during growth of leaf explants of Nicotiana plumbaginifolia. BiolFertil Soils 15(2):127–131CrossRefGoogle Scholar
  63. Muscolo A, Bovalo F, Gionfriddo F, Nardi S (1999) Earthworm humic matter produces auxin-like effects on Daucus carota cell growth and nitrate metabolism. Soil Biol Biochem 31(9):1303–1301CrossRefGoogle Scholar
  64. Pagliano C, Raviolo M, DallaVecchia F, Gabbrielli R, Gonnelli C, Rascio N, Barbato R (2006) Evidence for PSII donor-side damage photoinhibition induced by cadmium treatment of rice (Oryza sativa). J Photochem Photobiol 84:70–78CrossRefGoogle Scholar
  65. Panković D, Plesničar M, Arsenijević-Maksimović I, Petrović N, Sakač Z, Kastori R (2000) Effects of nitrogen nutrition on photosynthesis in Cd-treated sunflower plants. Ann Bot 86:841–847CrossRefGoogle Scholar
  66. Parandian F, Samavat S (2012) Effects of fulvic and humic acid on anthocyanin, soluble sugar,∝−amylase enzyme and some micronurient elements in Lilium. Int Res J Appl Basic Sci 3:924–929Google Scholar
  67. Patil NM (2010) Biofertilizer effect on growth, protein and carbohydrate content in Stevia rebaudiana var bertoni. Recent Res Sci Technol 2(10):42–44Google Scholar
  68. Qadir M, Ghafoor A, Murtaza G (2000) Amelioration strategies for saline soils: a review. Land Degrad Develop 11(6):501–521CrossRefGoogle Scholar
  69. Qian H, Li J, Sun L, Chen W, Sheng GD, Liu W, Fu Z (2009) Combined effect of copper and cadmium on Chlorella vulgaris growth and photosynthesis related gene transcription. Aquat Toxicol 94:56–61CrossRefGoogle Scholar
  70. Rascio N, Navari-Izzo F (2011) Heavy metal hyperaccumulating plants: how and why do they do it? And what makes them so interesting? Plant Sci 180:169–181CrossRefGoogle Scholar
  71. Rida AM (1996) Concentrations et croissance de lombriciens et de plantes dans des sols contamines ou non par Cd, Cu, Fe, Pb et Zn: interactions sol-Lombricien. Soil Biol Biochem 28(8):1029–1035CrossRefGoogle Scholar
  72. Saberi M, Nezhad FM, Etemadi N (2015) Interactive effects of vermicompost and salicylic acid on chlorophyll and carotenoid contents of Petunia Hybrid under drought stress. J Earth Environ Health Sci 1:52–57CrossRefGoogle Scholar
  73. Santos C, Monteiro M, Dias MC (2010) Cadmium toxicity in crops: a review. Environ Sci Eng Tech. Nova Publishers, NovinkaGoogle Scholar
  74. Scott TA, Melvin EH (2010) Determination of dextrann with anthrone. Analytical Chem 6:2–12Google Scholar
  75. Sethi R, Khan TI, Shrimal P (2015) Effects of vermicompost on physioloigical and biochemical parameters of Arachis hypogaea l. Var. M-13. GJBB 4(2):195–198Google Scholar
  76. Shah K, Dubey RS (1997) Effect of cadmium on proline accumulation and ribonuclease activity in rice seedlings: role of proline as a possible enzyme protectant. Biol Plantarum 40(1):121–130CrossRefGoogle Scholar
  77. Sharma P, Dubey RS (2006) Cadmium uptake and its toxicity in higher plants. In: Khan NA, Samiullah , (eds.) Cadmium toxicity and tolerance in plants. Narosa Publishers, New Delhi, India, pp 63–86 Google Scholar
  78. Sharma S, Pradhan K, Satya S, Vasudevan P (2005) Potentiality of earthworms for waste management and in other uses–A review. J Ame Sci 1(1):4-16Google Scholar
  79. Sharma A, Thakur S, Kumar V, Kanwar MK, Kesavan AK, Thukral AK, Bhardwaj R, Alam P, Ahmad P (2016) Pre-sowing seed treatment with 24-epibrassinolide ameliorates pesticide stress in Brassica juncea L. through the modulation of stress markers. Front Plant Sci 7:1569. doi: 10.3389/fpls.2016.01569 Google Scholar
  80. Shi G, Liu C, Cai Q, Liu Q, Hou C (2010) Cadmium accumulation and tolerance of two safflower cultivars in relation to photosynthesis and antioxidantive enzymes. Bull Environ Contam Toxicol 85:256–263CrossRefGoogle Scholar
  81. Singh RP, Agrawal M (2007) Effects of sewage sludge amendment on heavy metal accumulation and consequent responses of Beta vulgaris plants. Chemosphere 67:2229–2240CrossRefGoogle Scholar
  82. Srivastava M, Ma LQ, Singh N, Singh S (2005) Antioxidant responses of hyper-accumulator and sensitive fern species to arsenic. J Exp Bot 56(415):1335–1342CrossRefGoogle Scholar
  83. Tanaka M, Takamura T, Watanabe H, Endo M, Yanagi T, Okamoto K (1998) In vitro growth of cymbidium plantlets cultured under superbright red and blue light-emitting diodes (LEDs). J Hort Sci and Biotechnol 73(1):39–44CrossRefGoogle Scholar
  84. Tejada M, Gonzalez JL (2006) Crushed cotton gin compost on soil biological properties and rice yield. Eur J Agro 25(1):22–29CrossRefGoogle Scholar
  85. Tejada M, Gonzalez JL, García-Martínez AM, Parrado J (2008) Effects of different green manures on soil biological properties and maize yield. Bioresour Technol 99(6):1758–1767CrossRefGoogle Scholar
  86. Thapar R, Srivastava AK, Bhargava P, Mishra Y, Rai LC (2008) Impact of different abiotic stress on growth, photosynthetic electron transport chain, nutrient uptake and enzyme activities of Cu-acclimated Anabaena doliolum. J Plant Physiol 165:306–316CrossRefGoogle Scholar
  87. Vig K, Megharaj M, Sethunathan N, Naidu R (2003) Bioavailability and toxicity of cadmium to microorganisms and their activities in soil: a review. Adv Environ Res 8:121–135CrossRefGoogle Scholar
  88. Wang D, Li H, Wei Z, Wang X, Hu F (2006) Effect of earthworms on the phytoremediation of zinc-polluted soil by ryegrass and Indian mustard. Biol Fertil Soils 43(1):120–123CrossRefGoogle Scholar
  89. Winding A, Ronn R, Hendriksen NB (1997) Bacteria and protozoa in soil microhabitats as affected by earthworms. Biol Fertil Soil 24:133–140CrossRefGoogle Scholar
  90. Wurst S, Dugassa-Gobena D, Langel R, Bonkowski M, Scheu S (2004) Combined effects of earthworms and vesicular arbuscular mycorrhizas on plant and aphid performance. New Phytol 163:169–176CrossRefGoogle Scholar
  91. Xi ZM, Zhang ZW, Huo SS, Luan LY, Gao X, Ma LN, Fang YL (2013) Regulating the secondary metabolism in grape berry using exogenous 24-epibrassinolide for enhanced phenolics content and antioxidant capacity. Food Chem 141:3056–3065. doi: 10.1016/j.foodchem.2013.05.137 CrossRefGoogle Scholar
  92. Xu H, Weng X, Mao W, Yang Y (2005) Effects of cadmium stress on photosynthesis, chlorophyll fluorescence characteristics and excitation energy distribution in leaves of rice. Chin J Rice Sci 19:338–342Google Scholar
  93. Yadav SK (2010) Heavy metals toxicity in plants: an overview on the role of glutathione and phytochelatins in heavy metal stress tolerance of plants. S Afr J Bot 76:167–179CrossRefGoogle Scholar
  94. Yadav A, Garg VK (2015) Influence of vermi-fortification on chickpea (Cicer arietinum L.) growth and photosynthetic pigments. Int J Recycl Org Waste Agricult 4:299–305CrossRefGoogle Scholar
  95. Yadavi A, Pireh P, Balouchi H (2014) Effect of vermicompost fertilizer and arbuscular mycorrhiza on physiological and morphological characteristics of soybean (M9 variety) under cadmium chloride toxicity. Adv Environ Biol 8(13):1168–1175Google Scholar
  96. Yu X, Cheng J, Wong MH (2005) Earthworm–mycorrhiza interaction on Cd uptake and growth of ryegrass. Soil Biol Biochem 37(2):195–201CrossRefGoogle Scholar
  97. Zaller JG, Saccani F, Frank T (2011) Effects of earthworms and mycorrhizal fungi on the growth of the medicinal herb Calendula officinalis (Asteraceae). Plant Soil Environ 57(11):499–504Google Scholar
  98. Zayneb C, Bassem K, Zeineb K, Grubb CD, Noureddine D, Hafedh M, Amine E (2015) Physiological responses of fenugreek seedlings and plants treated with cadmium. Environ Sci Poll Res 22(14):10679–10689CrossRefGoogle Scholar
  99. Zhang H, Schrader S (1993) Earthworm effects on selected physical and chemical properties of soil aggregates. Biol Fertil Soil 15:229–234CrossRefGoogle Scholar
  100. Zhang S, Hu F, Li H (2009) Effects of earthworm mucus and amino acids on cadmium subcellular distribution and chemical forms in tomato seedlings. Bioresour Technol 100(17):4041–4046CrossRefGoogle Scholar

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© Springer-Verlag Berlin Heidelberg 2017

Authors and Affiliations

  1. 1.Department of Botanical and Environmental SciencesGuru Nanak Dev UniversityAmritsarIndia

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