Abstract
Cadmium (Cd) is a non-essential and highly toxic element for plant growth while zinc (Zn) becomes toxic at elevated levels. Presence of these heavy metals (HMs) in soils has negative impact on rhizobial symbiosis in legumes leading to reduced agricultural productivity. Role of silicon (Si) amendment and Rhizophagus irregularis in mitigating HM stress has gained importance in recent years. Present study evaluated the individual and cumulative effects of Si and/or AM on Cd (25, 50 mg/kg) or Zn (600, 1000 mg/kg) induced responses in terms of nitrogen fixing efficiency, trehalose biosynthesis, antioxidant defense and phytochelatin (PC) synthesis in pigeon pea genotypes (Tolerant-Pusa 2002, Sensitive-Pusa 991). Results indicated that although mycorrhizal colonization (MC) declined with increase in metal concentration in both genotypes, Pusa 2002 was able to form significant colonization even under stress. Cadmium and zinc stress negatively affected plant biomass and rhizobial symbiosis, with Cd more toxic than Zn. The decline in nodulation potential under both HMs was much more significant in Pusa 991 than Pusa 2002 which could be correlated with proportionately reduced MC, nutrient uptake and ultimate N accumulation. Individual application of AM was much more effective in improving nitrogen fixing efficiency by increasing trehalose biosynthesis, PC production and strengthening antioxidant defense than Si. Restoration of rhizobial symbiosis under combined applications of Si and AM could be correlated with enhanced Si uptake through mycorrhization. Thus, study suggested use of AM as a tool in enhancing benefits of Si nutrition in terms of restoration of nodule senescence and N-fixing competence in pigeon pea under HMs stress.
Similar content being viewed by others
References
Abd-Alla MH, El-Enany AW, Nafady NA, Khalaf DM, Morsy FM (2014) Synergistic interaction of Rhizobium leguminosarum bv. viciae and arbuscular mycorrhizal fungi as a plant growth promoting biofertilizers for faba bean (Vicia faba L.) in alkaline soil. Microbiol Res 169(1):49–58
Aebi H (1984) Catalase in vitro. In: Packer L (ed) Methods in enzymology, vol 105. Academic Press, Orlando, pp 121–126
Ahmad E, Zaidi A, Khan MS, Oves M (2012) Heavy metal toxicity to symbiotic nitrogen-fixing microorganism and host legumes. In: Zaidi A, Wani P, Khan M (eds) Toxicity of heavy metals to legumes and bioremediation. Springer, Vienna
Almeida JPF, Hartwig UA, Frehner M, Nösberger J, Lüscher A (2000) Evidence that P deficiency induces N feedback regulation of symbiotic N2 fixation in white clover (Trifolium repens L.). J Exp Bot 51:1289–1297
Anda CCO, Opfergelt S, Declerck S (2016) Silicon acquisition by bananas (c.V. Grande Naine) is increased in presence of the arbuscular mycorrhizal fungus Rhizophagus irregularis MUCL 41833. Plant Soil 409:77–85
Anderson ME (1985) Determination of glutathione and glutathione disulfides in biological samples. Methods Enzymol 113:548–570
Balestrasse KB, Gardey L, Gallego SM, Tomaro ML (2001) Response of antioxidant defence system in soybean nodules and roots subjected to cadmium stress. Funct Plant Biol 28:497–504
Balestrasse KB, Gallego SM, Tomaro ML (2006) Oxidation of the enzymes involved in nitrogen assimilation plays an important role in the cadmium-induced toxicity in soybean plants. Plant Soil 284(1–2):187–194
Becana M, Dalton DA, Moran JF, Iturbe-Ormaetxe I, Matamoros MA, Rubio MC (2000) Reactive oxygen species and antioxidants in legume nodules. Physiol Plant 109:372–381
Benavides MP, Gallego SM, Tomaro ML (2005) Cadmium toxicity in plants. Braz J Plant Physiol 17(1):21–34
Bhargava P, Srivastava AK, Urmil S, Rai LC (2005) Phytochelatin plays a role in UV-B tolerance in N2-fixing cyanobacterium Anabaena doliolum. J Plant Physiol 162:1220–1225
Bianucci E, Fabra A, Castro S (2008) Growth of Bradyrhizobium sp. SEMIA 6144 in response to methylglyoxal: role of glutathione. Curr Microbiol 56:371–375
Broadley MR, White PJ, Hammond JP, Zelko I, Lux A (2007) Zinc in plants. New Phytol 173:677–702
Castillo FI, Penel I, Greppin H (1984) Peroxidase release induced by ozone in Sedum album leaves. Plant Physiol 74:846–851
Chang C, Nasir F, Ma L, Tian C (2017) Molecular communication and nutrient transfer of arbuscular mycorrhizal fungi, symbiotic nitrogen-fixing bacteria, and host plant in tripartite symbiosis. In: Sulieman S, Tran LS (eds) Legume nitrogen fixation in soils with low phosphorus availability. Springer, Cham
Cuypers A, Smeets K, Ruytinx J, Opdenakker K, Keunen E, Remans T, Horemans N, Vanhoudt N, Sanden SV, Belleghem FV, Guisez Y, Colpaert J, Vangronsveld J (2011) The cellular redox state as a modulator in cadmium and copper responses in Arabidopsis thaliana seedlings. J Plant Physiol 168:309–316
Del Longo OT, Gonzalez CA, Pastori GM, Tripps VS (1993) Antioxidant defenses under hyperoxygenic and hyperosmotic conditions in leaves of two lines of maize with differential sensitivity to drought. Plant Cell Physiol 34:1023–1028
Dhindsa RS, Plumb-Dhindsa P, Throne TA (1981) Leaf senescence: correlated with increased levels of membrane permeability and lipid peroxidation and decreased levels of superoxide dismutase and catalase. J Exp Bot 32:93–101
Divito GA, Sadras VO (2014) How do phosphorus, potassium and sulphur affect plant growth and biological nitrogen fixation in crop and pasture legumes? A meta-analysis. Field Crops Res 156:161–171
Elbein AD, Pan YT, Pastuszak I, Carroll D (2003) New insights on trehalose: a multifunctional molecule. Glycobiology 13:17–27
Elliot CL, Snyder GH (1991) Autoclave-induced digestion for the colorimetric determination of silicon in rice straw. J Agric Food Chem 39:1118–1119
Emamverdian A, Ding Y, Mokhberdoran F, Xie Y (2015) Heavy metal stress and some mechanisms of plant defense response. Sci World https://doi.org/10.1155/2015/756120.
Epstein E (2009) Silicon: its manifold roles in plants. Ann Appl Biol 155:155–160
Epstein E, Bloom AJ (2005) Mineral nutrition of plants: principles and perspectives, 2nd edn. Sinauer Associates, Inc., Sunderland
FAOSTAT (2014) http://www.fao.org/faostat/en/#data/QC. Accessed Sept 2017
Fuentes A, Almonacid L, Ocampo JA, Arriagada C (2016) Synergistic interactions between a saprophytic fungal consortium and Rhizophagus irregularis alleviate oxidative stress in plants grown in heavy metal contaminated soil. Plant Soil 407(1–2):355–366
Gallego SM, Pena LB, Barcia RA, Azpilicueta CE, Lannone MF, Maria F (2012) Unravelling cadmium toxicity and tolerance in plants: insight into regulatory mechanisms. Environ Exp Bot 83:33–46
Garg N, Bhandari P (2012) Influence of cadmium stress and arbuscular mycorrhizal fungi on nodule senescence in Cajanus cajan (L.) Millsp. Int J Phytorem 14(1):62–74
Garg N, Bhandari P (2016) Silicon nutrition and mycorrhizal inoculations improve growth, nutrient status, K+/Na+ ratio and yield of Cicer arietinum L. genotypes under salinity stress. Plant Growth Regul 78(3):371–387
Garg N, Chandel S (2011) The effects of salinity on nitrogen fixation and trehalose metabolism in mycorrhizal Cajanus cajan (L.) Millsp. plants. J Plant Growth Regul 30:490–503
Garg N, Chandel S (2012) Role of arbuscular mycorrhizal (AM) fungi on growth, cadmium uptake, osmolyte, and phytochelatin synthesis in Cajanus cajan (L.) Millsp. under NaCl and Cd stresses. J Plant Growth Regul 31(3):292–308
Garg N, Kashyap L (2017) Silicon and Rhizophagus irregularis: potential candidates for ameliorating negative impacts of arsenate and arsenite stress on growth, nutrient acquisition and productivity in Cajanus cajan (L.) Millsp. genotypes. Environ Sci Pollut Res 24(22):18520–18535
Garg N, Kaur H (2012) Influence of zinc on cadmium-induced toxicity in nodules of pigeonpea (Cajanus cajan L. Millsp.) inoculated with arbuscular mycorrhizal (AM) fungi. Acta Physiol Plant 34(4):1363–1380
Garg N, Pandey R (2016) High effectiveness of exotic arbuscular mycorrhizal fungi is reflected in improved rhizobial symbiosis and trehalose turnover in Cajanus cajan genotypes grown under salinity stress. Fungal Ecol 21:57–67
Garg N, Singh S (2017) Arbuscular mycorrhiza Rhizophagus irregularis and silicon modulate growth, proline biosynthesis and yield in Cajanus cajan L. Millsp. (pigeonpea) genotypes under cadmium and zinc stress. J Plant Growth Regul. https://doi.org/10.1007/s00344-017-9708-4
Garg N, Singla P (2016) Stimulation of nitrogen fixation and trehalose biosynthesis by naringenin (Nar) and arbuscular mycorrhiza (AM) in chickpea under salinity stress. Plant Growth Regul 80:5
Gill SS, Tuteja N (2010) Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiol Biochem 48:909–930
Giovannetti M, Mosse B (1980) Evaluation of techniques for measuring vesicular arbuscular mycorrhizal infection in roots. New Phytol 84:489–500
Gómez-Sagasti MT, Marino D (2015) PGPRs and nitrogen-fixing legumes: a perfect team for efficient Cd phytoremediation? Front Plant Sci 6:81
Hall JL (2002) Cellular mechanisms for heavy metal detoxification and tolerance. J Exp Bot 366:1–11
Hammer EC, Nasr H, Pallon J, Olsson PA, Wallander H (2011) Elemental composition of arbuscular mycorrhizal fungi at high salinity. Mycorrhiza 21(2):117–129
Hartree EF (1957) Haemetin compounds. In: Paech K, Tracey MV (eds) Modern methods of plant analysis. Springer, New York, pp 197–245
Heath RL, Packer I (1968) Photoperoxidation in isolated chloroplast: I. Kinetics and stoichiometry of fatty acid peroxidation. Arch Biochem Biophys 125:189–198
Herdina JA, Silsbury JH (1990) Estimating nitrogenase activity of faba bean (Vicia faba L.) by acetylene reduction (ARA) assay. Aust J Plant Physiol 17:489–502
Hernandez LE, Garate A, Carpena-Ruiz R (1995) Effect of cadmium on nitrogen fixing pea plants grown in perlite and vermiculite. J Plant Nutr 18(2):287–303
Hernandez L, Probst A, Probst JL, Ulrich E (2003) Heavy metal distribution in some French forest soils: evidence for atmospheric contamination. Sci Total Environ 312:195–219
Horst WJ, Marschner H (1978) Effect of silicon and manganese tolerance of bean plants (Phaseolus vulgaris L.). Plant Soil 50:287–303
Jackson ML (1973) Soil chemical analysis. Printice Hall, New Delhi, p 485
Joner E, Leyval C (2001) Influence of arbuscular mycorrhiza on clover and ryegrass grown together in a soil spiked with polycyclic aromatic hydrocarbons. Mycorrhiza 10:155–159
Jules M, Beltran G, Francois J, Parrou JL (2008) New insights into trehalose metabolism by Saccharomyces cerevisiae: NTH2 encodes a functional cytosolic trehalase, and deletion of TPS1 reveals ATH1p-dependent trehalose mobilization. Appl Environ Microbiol 74:605–614
Juszczuk I, Malusà E, Rychter AM (2001) Oxidative stress during phosphate deficiency in roots of bean plants (Phaseolus vulgaris L.). J Plant Physiol 158:1299–1305
Kabata-Pendias A, Pendias H (2001) Trace elements in soils and plants, 3rd edn. CRC Press, Boca Raton
Kabata-Pendias A, Pendias H (2010) Trace elements in soils and plants, 3rd edn. CRC Press, Boca Raton
Kleinert A, le Roux M, Kang Y, Valentine AJ (2017) Oxygen and the regulation of N2 fixation in legume nodules under P scarcity. In: Sulieman S, Tran LS (eds) Legume nitrogen fixation in soils with low phosphorus availability. Springer, Cham
Krasensky J, Broyart C, Rabanal FA, Jonak C (2014) The redox-sensitive chloroplast trehalose-6-phosphate phosphatase AtTPPD regulates salt stress tolerance. Antioxid Redox Signal 21(9):1289–1304
Latef AAHA., Ahmad P (2015) Legumes and breeding under abiotic stress. In: Azooz MM, Ahmad P (eds) Legumes under environmental stress: yield, improvement and adaptations. Wiley, Chichester
Liang Y, Hua H, Zhu YG, Zhang J, Cheng C, Römheld V (2006) Importance of plant species and external silicon concentration to active silicon uptake and transport. New Phytol 172:63–72
Lin YF, Aarts MGM (2012) The molecular mechanism of zinc and cadmium stress response in plants. Cell Mol Life Sci 69:3187
Lindner RC (1944) Rapid analytical method for some of the more inorganic constituents of plant tissue. Plant Physiol 19:76–89
Lux A, Vaculík M, Martinka M, Lišková D, Kulkarni MG, Stirk WA, Staden VJ (2011) Cadmium induces hypodermal periderm formation in the roots of the monocotyledonous medicinal plant Merwilla plumbea. Ann Bot 107(2):285–292
Ma JF, Yamaji N (2006) Silicon uptake and accumulation in higher plants. Trends Plant Sci 11:392–397
Mali M, Aery NC (2008) Silicon effects on nodule growth, dry-matter production, and mineral nutrition of cowpea (Vigna unguiculata). Z Pflanzenernähr Bodenk 171:835–840
Mantri N, Basker N, Ford R, Pang E, Pardeshi V (2013) The role of miRNAs in legumes with a focus on abiotic stress response. Plant Genome. https://doi.org/10.3835/plantgenome2013.05.0013
Marguí E, Hidalgoa M, Queraltb I (2007) XRF spectrometry for trace element analysis of vegetation samples. Spectrosc Eur 19(3):13–17
Martins LL, Mourato MP, Baptista S, Reis R, Carvalheiro F, Almeida AM (2014) Response to oxidative stress induced by cadmium and copper in tobacco plants (Nicotiana tabacum) engineered with the trehalose-6-phosphate synthase gene (AtTPS1). Acta Physiol Plant 36:755–765
Martins D, Macovei A, Leonetti P, Balestrazzi A, Araújo S (2017) The influence of phosphate deficiency on legume symbiotic N2 fixation. In: Sulieman S, Tran LS (eds) Legume nitrogen fixation in soils with low phosphorus availability. Springer, Cham, pp 41–75
Mhadhbi H, Chihaoui S, Mhamdi R, Mnasri B, Jebara M, Mhamdi R (2011) A highly osmotolerant rhizobial strain confers a better tolerance of nitrogen fixation and enhanced protective activities to nodules of Phaseolus vulgaris under drought stress. Afr Biotechnol 22:4555–4563
Miller GL (1959) Use of dinitrosulphosalicylic acid (DNSA) reagent for determination of reducing sugar. Anal Chem 31(3):426–428
Miransari M (2017) Arbuscular mycorrhizal fungi and heavy metal tolerance in plants. In: Wu QS (ed) Arbuscular mycorrhizas and stress tolerance of plants. Springer, Singapore
Mitani N, Ma JF (2005) Uptake system of silicon in different plant species. J Exp Bot 56(414):1255–1261
Miyake Y, Takahashi E (1985) Effect of silicon on the growth of soybean plants in a solution culture. Soil Sci Plant Nutr 31:625–636
Mostofa MG, Hossain MA, Fujita M, Tran LSP (2015) Physiological and biochemical mechanisms associated with trehalose-induced copper-stress tolerance in rice. Sci Rep 5:11433
Müller J, Xie ZP, Staehelin C, Mellor RB, Boller T, Wiemken A (1994) Trehalose and trehalase in root nodules from various legumes. Physiol Plant 90(1):86–92
Müller J, Aeschbacher RA, Wingler A, Boller T, Wiemken A (2001) Trehalose and trehalase in Arabidopsis. Plant Physiol 125:1086–1093
Nasto MK, Alvarez-Clare S, Lekberg Y, Sullivan BW, Townsend AR, Cleveland CC (2014) Interactions among nitrogen fixation and soil phosphorus acquisition strategies in lowland tropical rain forests. Ecol Lett 17(10):1282–1289
Ocón A, Hampp R, Requena N (2007) Trehalose turnover during abiotic stress in arbuscular mycorrhizal fungi. New Phytol 174:879–891
Owino-Gerroh C, Gascho GJ (2005) Effect of silicon on low pH soil phosphorus sorption and on uptake and growth of maize. Commun Soil Sci Plant Anal 35(15–16):2369–2378
Padilla L, Krämer R, Stephanopoulos G, Agosin E (2004) Overproduction of trehalose: heterologous expression of Escherchia coli trehalose-6-phosphate synthase and trehalose-6-phosphate phosphatase in Corynebacterium glutamicum. Appl Environ Microbiol 70(1):370–376
Pawlowska TE, Charvat I (2004) Heavy-metal stress and developmental patterns of arbuscular mycorrhizal fungi. Appl Environ Microbiol 70:6643–6649
Pérez-Montaño F, Alías-Villegas C, Bellogín RA, del Cerro P, Espuny MR, Jiménez-Guerrero I, López-Baena FJ, Ollero FJ, Cubo T (2014) Plant growth promotion in cereal and leguminous agricultural important plants: from microorganism capacities to crop production. Microbiol Res 169:325–336
Phillips JM, Hayman DS (1970) Improved procedures for clearing and staining parasitic and vesicular-arbuscular mycorrhizal fungi for rapid assessment of infection. Trans Br Mycol Soc 55:158–161
Porter JR, Sheridan RP (1981) Inhibition of nitrogen fixation in alfalfa by arsenate, heavy metals, fluoride, and simulated acid rain. Plant Physiol 68(1):143–148
Püschel D, Janoušková M, Voříšková A, Gryndlerová H, Vosátka M, Jansa J (2017) Arbuscular mycorrhiza stimulates biological nitrogen fixation in two Medicago spp. through improved phosphorus acquisition. Front Plant Sci 8:390
Ratnayake M, Leonard RT, Menge JA (1978) Root exudation in relation to supply of phosphorus and its possible relevance to mycorrhizal formation. New Phytol 81:543–552
Salminen SO, Streeter JG (1986) Enzymes of alpha, alpha-trehalose metabolism in soybean nodules. Plant Physiol 81(2):538–541
Sánchez-Pardo B, Carpena RO, Zornoza P (2013) Cadmium in white lupin nodules: impact on nitrogen and carbon metabolism. J Plant Physiol 170:265–271
Sharma P, Jha AB, Dubey RS, Pessarakli M (2012) Reactive oxygen species, oxidative damage, and antioxidative defense mechanism in plants under stressful conditions. J Bot. https://doi.org/10.1155/2012/217037 2012.
Shikhova LN, Lisitsyn EM (2017) Seasonal dynamics in content of some heavy metals and microelements in arable soils of taiga zone of European Russia. In: Bekuzarova S, Lisitsyn E, Weisfeld L, Zaikov G (eds) Heavy metals and other pollutants in the environment. Apple Academic Press, Oakville, pp 63–82
Singh J, Kalamdhad A (2011) Effects of heavy metals on soil, plants, human health and aquatic life. Int J Res Chem Environ 1:15–21
Smith SE, Smith FA, Jakobsen I (2003) Mycorrhizal fungi can dominate phosphate supply to plants irrespective of growth responses. Plant Physiol 133:16–20
Streeter JG, Strimbu CE (1998) Simultaneous extraction and derivatization of carbohydrates from green plant tissues for analysis by gas–liquid chromatography. Anal Biochem 259(2):253–257
Sun Q, Wang XR, Ding SM, Yuan XF (2005) Effects of exogenous organic chelators on phytochelatins production and its relationship with cadmium toxicity in wheat (Triticum aestivum L.) under cadmium stress. Chemosphere 60(1):22–31
Tewari RK, Kumar P, Sharma PN (2007) Oxidative stress and antioxidant responses in young leaves of mulberry plants grown under nitrogen, phosphorus or potassium deficiency. J Integr Plant Biol 49:313–322
Toppi L, Gabbrielli R (1999) Response to cadmium in higher plants. Environ Exp Bot 41(2):105–130
Varennes A, Goss MJ (2007) The tripartite symbiosis between legumes, rhizobia and indigenous mycorrhizal fungi is more efficient in undisturbed soil. Soil Biol Biochem 39(10):2603–2607
Velikova V, Yordanov I, Edreva A (2000) Oxidative stress and some antioxidative systems in acid rain treated bean plants. Plant Sci 151:59–66
Venterink HO (2011) Legumes have a higher root phosphatase activity than other forbs, particularly under low inorganic P and N supply. Plant soil 347(1–2):137–146
Verbruggen N, Hermans C, Schat H (2009) Molecular mechanisms of metal hyperaccumulation in plants. New Phytol 181:759–776
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 76:167–179
Yost RS, Fox RL (1982) Influence of mycorrhizae on the mineral contents of cowpea and soybean grown in an oxisol. Agron J 74:475–481
Zahran HH (2010) Legumes–microbes interactions under stressed environments. In: Khan MS, Zaidi A, Musarrat J (eds) Microbes for legume improvement. Springer, Cham, pp 353–387
Zhu JK (2002) Salt and drought stress signal transduction in plants. Annu Rev Plant Biol 53:247–273
Zornoza P, Vàzquez S, Esteban E, Fernàndez-Pascual M, Carpena R (2002) Cadmium-stress in nodulated white lupin: strategies to avoid toxicity. Plant Physiol Biochem 40:1003–1009
Zwiazek JJ, Blake TJ (1991) Early detection of membrane injury in black spruce (Picea mariana). Can J For Res 21:401–404
Acknowledgements
Financial support provided by Department of Biotechnology (DBT), University Grants Commission (UGC, New Delhi), Government of India in undertaking the present research is gratefully acknowledged. We are also grateful to Pulse laboratory, IARI and TERI (The Energy and Resources Institute), New Delhi for providing the research material.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors have no conflict of interest.
Rights and permissions
About this article
Cite this article
Garg, N., Singh, S. Mycorrhizal inoculations and silicon fortifications improve rhizobial symbiosis, antioxidant defense, trehalose turnover in pigeon pea genotypes under cadmium and zinc stress. Plant Growth Regul 86, 105–119 (2018). https://doi.org/10.1007/s10725-018-0414-4
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10725-018-0414-4