Skip to main content
SpringerLink
Log in

Relative effectiveness of arbuscular mycorrhiza and polyamines in modulating ROS generation and ascorbate-glutathione cycle in Cajanus cajan under nickel stress

  • Research Article
  • Published:
Environmental Science and Pollution Research Aims and scope Submit manuscript

Abstract

Nickel (Ni) is a fundamental micronutrient in plants but hampers plant growth and metabolism at elevated levels in the soil by inducing oxidative stress. In the recent years, use of polyamines (PAs) and arbuscular mycorrhiza (AM) have gained importance for their roles in enabling plants to withstand Ni toxicity. However, information about their comparative effectiveness in alleviating Ni stress is scanty. Therefore, the current study was designed to evaluate relative impacts of three PAs (Put, Spd, and Spm) and AM (Rhizoglomus intraradices) in reducing Ni uptake, ROS generation, and modulating antioxidant defense machinery in two pigeonpea genotypes (Pusa 2001-tolerant and AL 201-sensitive). Roots of Ni supplied plants accumulated significantly more Ni than the leaves, more in AL 201 than Pusa 2001, which was proportionate to reduced dry weights and enhanced oxidative burst. Although all the three PAs as well as AM inoculations upsurge plant growth by remarkably lowering Ni transport as well as the sequential oxidative burden, AM was most effective, followed by Put, Spd with least positive impact of Spm. The combined applications of AM and Put were able to strengthen antioxidant defense mechanisms, including those of ascorbate-glutathione cycle, most strongly when compared with + Spd + AM and + Spm + AM. Pusa 2001 was more responsive to PAs priming because of its proficiency to develop better effective mycorrhizal symbiosis with R. intraradices when compared with AL201. Hence, the results suggest use of combined applications of PAs (mainly Put) and R. intraradices as an effective strategy for mitigating Ni toxicity in pigeonpea genotypes.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Aebi H (1984) Catalase in vitro. In: Packer L (ed) Methods in enzymology, 105th edn. Academic Press, Orlando, pp 121–126

    Google Scholar 

  • Al Mahmud J, Bhuyan MB, Anee TI, Nahar K, Fujita M, Hasanuzzaman M (2019) Reactive oxygen species metabolism and antioxidant defense in plants under metal/metalloid stress. In: Hasanuzzaman M, Hakeem KR, Nahar K, Alharby HF (eds) Plant abiotic stress tolerance. Springer, Cham, pp 221–257

    Chapter  Google Scholar 

  • Aldesuquy H, Haroun S, Abo-Hamed S, El-Saied AW (2014) Involvement of spermine and spermidine in the control of productivity and biochemical aspects of yielded grains of wheat plants irrigated with waste water. Egypt J Basic Appl Sci 1:16–28

    Article  Google Scholar 

  • Alqarawi AA, Abd Allah EF, Hashem A (2014) Alleviation of salt-induced adverse impact via mycorrhizal fungi in Ephedra aphylla Forssk. J Plant Interact 9:802–810

    Article  CAS  Google Scholar 

  • Amir H, Lagrange A, Hassaïne N, Cavaloc Y (2013) Arbuscular mycorrhizal fungi from New Caledonian ultramafic soils improve tolerance to nickel of endemic plant species. Mycorrhiza 23:585–595

    Article  CAS  Google Scholar 

  • Arakawa N, Tsutsumi K, Sanceda NG, Kurata T, Inagaki C (1981) A rapid and sensitive method for the determination of ascorbic acid using 4, 7-diphenyl-l, 10-phenanthroline. Agric Biol Chem 45:1289–1290

    CAS  Google Scholar 

  • Asada K (1984) Chloroplasts: formation of active oxygen and its scavenging. Methods Enzymol 105:422–429

    Article  CAS  Google Scholar 

  • Barcelos JPQ, Reis HPG, Godoy CV, Gratão PL, Furlani Junior E, Putti FF, Campos M, Reis AR (2018) Impact of foliar nickel application on urease activity, antioxidant metabolism and control of powdery mildew (Microsphaera diffusa) in soybean plants. Plant Pathol 67:1502–1513

    Article  CAS  Google Scholar 

  • Begum N, Qin C, Ahanger MA, Raza S, Khan MI, Ahmed N, Ashraf M, Zhang L (2019) Role of arbuscular mycorrhizal fungi in plant growth regulation, implications in abiotic stress tolerance. Front Plant Sci 10:1068–1083

    Article  Google Scholar 

  • Bhalerao SA, Sharma AS, Poojari AC (2015) Toxicity of nickel in plants. Int J Pure Appl Biosci 3:345–355

    Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Castillo FJ, Greppin H (1988) Extracellular ascorbic acid and enzyme activities related to ascorbic acid metabolism in Sedum album L. leaves after ozone exposure. Environ Exp Bot 28:231–238

    Article  CAS  Google Scholar 

  • Castillo FJ, Penel C, Greppin H (1984) Peroxidase release induced by ozone in Sedum album leaves: involvement of Ca2+. Plant Physiol 74:846–851

    Article  CAS  Google Scholar 

  • Chellamma S, Pillai BV (2013) Approaches to improving salt tolerance in maize. In: Ahmad P, Azooz MM, Prasad MNV (eds) Salt stress in plants. Springer, New York, pp 261–281

    Chapter  Google Scholar 

  • Chen D, Shao Q, Yin L, Younis A, Zheng B (2019) Polyamine function in plants, metabolism, regulation on development, and roles in abiotic stress responses. Front Plant Sci 9:1–13

    Article  Google Scholar 

  • Del Longo OT, González CA, Pastori GM, Trippi VS (1993) Antioxidant defences under hyperoxygenic and hyperosmotic conditions in leaves of two lines of maize with differential sensitivity to drought. Plant Cell Physiol 34:1023–1028

    Google Scholar 

  • Dhalaria R, Kumar D, Kumar H, Nepovimova E, Kuča K, Torequl Islam M, Verma R (2020) Arbuscular mycorrhizal fungi as potential agents in ameliorating heavy metal stress in plants. Agronomy 10:815–837

    Article  CAS  Google Scholar 

  • Dhindsa RS, Plumb-Dhindsa P, Thorpe 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

    Article  CAS  Google Scholar 

  • Doke N (1983) Involvement of superoxide anion generation in the hypersensitive response of potato tuber tissues to infection with an incompatible race of Phytophthora infestans and to the hyphal wall components. Physiol Plant Pathol 23:345–357

    Article  CAS  Google Scholar 

  • El Ghachtouli N, Paynot M, Morandi D, Martin-Tanguy J, Gianinazzi S (1995) The effect of polyamines on endomycorrhizal infection of wild-type Pisum sativum, cv. Frisson (nod+ myc+) and two mutants (nod− myc+ and nod− myc−). Mycorrhiza 5:189–192

    CAS  Google Scholar 

  • Estefan G, Sommer R, Ryan J (2013) Methods of soil, plant, and water analysis. A manual for the West Asia and North Africa region:170–176

  • FAOSTAT (2017) http,//www.fao.org/faostat/en/#data/QC

  • Foyer CH, Noctor G (2011) Ascorbate and glutathione: the heart of the redox hub. Plant Physiol 155:2–18

    Article  CAS  Google Scholar 

  • Gajewska E, Skłodowska M (2007) Effect of nickel on ROS content and antioxidative enzyme activities in wheat leaves. Biometals 20:27–36

    Article  CAS  Google Scholar 

  • Galli U, Schüepp H, Brunold C (1996) Thiols in cadmium-and copper-treated maize (Zea mays L.). Planta 198:139–143

    Article  CAS  Google Scholar 

  • Gamalero E, Lingua G, Berta G, Glick BR (2009) Beneficial role of plant growth promoting bacteria and arbuscular mycorrhizal fungi on plant responses to heavy metal stress. Can J Microbiol 55:501–514

    Article  CAS  Google Scholar 

  • Garg N, Bhandari P (2016) Interactive effects of silicon and arbuscular mycorrhiza in modulating ascorbate-glutathione cycle and antioxidant scavenging capacity in differentially salt-tolerant Cicer arietinum L. genotypes subjected to long-term salinity. Protoplasma 253:1325–1345

    Article  CAS  Google Scholar 

  • Garg N, Kashyap L (2019) Joint effects of Si and mycorrhiza on the antioxidant metabolism of two pigeonpea genotypes under As (III) and (V) stress. Environ Sci Pollut Res 26:7821–7839

    Article  CAS  Google Scholar 

  • Garg N, Saroy K (2019) Interactive effects of polyamines and arbuscular mycorrhiza in modulating plant biomass, N2 fixation, ureide, and trehalose metabolism in Cajanus cajan (L.) Millsp. genotypes under nickel stress. Environ Sci Pollut Res 27:3043–3064

    Article  CAS  Google Scholar 

  • Ghosh G, Purohit A, Chaudhuri RK, Chakraborti D (2014) Advances in genetic transformation of important pulse crop pigeonpea. Agro Food Biotechnol 12:1–16

    Google Scholar 

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

    Article  Google Scholar 

  • Gonzalez-Chavez MC, Carrillo-Gonzalez R, Wright SF, Nichols KA (2004) The role of glomalin, a protein produced by arbuscular mycorrhizal fungi, in sequestering potentially toxic elements. Environ Pollut 130:317–323

    Article  CAS  Google Scholar 

  • González-Guerrero M, Oger E, Benabdellah K, Azcón-Aguilar C, Lanfranco L, Ferrol N (2010) Characterization of a Cu-Zn superoxide dismutase gene in the arbuscular mycorrhizal fungus Glomus intraradices. Curr Genet 56:265–274

    Article  CAS  Google Scholar 

  • Hao F, Wang X, Chen J (2006) Involvement of plasma-membrane NADPH oxidase in nickel-induced oxidative stress in roots of wheat seedlings. Plant Sci 170:151–158

    Article  CAS  Google Scholar 

  • Hasanuzzaman M, Nahar K, Anee TI, Fujita M (2017) Glutathione in plants: biosynthesis and physiological role in environmental stress tolerance. Physiol Mol Biol Plants 23:249–268

    Article  CAS  Google Scholar 

  • Heath RL, Packer L (1968) Photoperoxidation in isolated chloroplasts, I. Kinetics and stoichiometry of fatty acid peroxidation. Arch Biochem Biophys 125:189–198

    Article  CAS  Google Scholar 

  • Hetrick BAD, Wilson GWT, Cox TS (1992) Mycorrhizal dependence of modern wheat cultivars and ancestors, a synthesis. Can J Bot 71:512–518

    Article  Google Scholar 

  • Jamal A, Ayub N, Usman M, Khan AG (2002) Arbuscular mycorrhizal fungi enhance zinc and nickel uptake from contaminated soil by soybean and lentil. Int J Phytoremediation 4:205–221

    Article  CAS  Google Scholar 

  • Kubiś J, Floryszak-Wieczorek J, Arasimowicz-Jelonek M (2014) Polyamines induce adaptive responses in water deficit stressed cucumber roots. J Plant Res 127:151–158

    Article  CAS  Google Scholar 

  • Liu GD (2001) A new essential mineral element-nickel. Plant Nutrition and Fertilizer Science 7:101–103

    Google Scholar 

  • Marguí E, Queralt I, Carvalho ML, Hidalgo M (2007) Assessment of metal availability to vegetation (Betula pendula) in Pb-Zn ore concentrate residues with different features. Environ Pollut 145:179–184

    Article  CAS  Google Scholar 

  • Mehlich A (1953) Determination of P, Ca, Mg, K, Na and NH4. In: Short test methods used in soil testing division. Department of Agriculture, Raleigh, pp 23–89

    Google Scholar 

  • Mir MA, Sirhindi G, Alyemeni MN, Alam P, Ahmad P (2018) Jasmonic acid improves growth performance of soybean under nickel toxicity by regulating nickel uptake, redox balance, and oxidative stress metabolism. J Plant Growth Regul 37:1195–1209

    Article  CAS  Google Scholar 

  • Nahar K, Rahman M, Hasanuzzaman M, Alam MM, Rahman A, Suzuki T, Fujita M (2016) Physiological and biochemical mechanisms of spermine-induced cadmium stress tolerance in mung bean (Vigna radiata L.) seedlings. Environ Sci Pollut Res 23:21206–21218

    Article  CAS  Google Scholar 

  • Nakagawara S, Sagisaka S (1984) Increase in enzyme activities related to ascorbate metabolism during cold acclimation in poplar twigs. Plant Cell Physiol 25:899–906

    CAS  Google Scholar 

  • Nakano Y, Asada K (1981) Hydrogen peroxide is scavenged by ascorbate-specific peroxidase in spinach chloroplasts. Plant Cell Physiol 22:867–880

    CAS  Google Scholar 

  • Nelson DW, Sommers LE (1973) Determination of total nitrogen in plant material. Agron J 65:109–112

    Article  CAS  Google Scholar 

  • Olsen SR, Sommers LE (1982) Phosphorus. In: Page AL (ed) Methods of soil analysis. Agron. No. 9, part 2 - chemical and microbiological properties, 2nd edn, American society agronomy, Madison, pp 403-430

  • Patra A, Dutta A, Jatav SS, Choudhary S, Chattopadhyay A (2019) Horizon of nickel as essential to toxic element. IJCS 7:1185–1191

    CAS  Google Scholar 

  • Paul S, Banerjee A, Roychoudhury A (2018) Role of polyamines in mediating antioxidant defense and epigenetic regulation in plants exposed to heavy metal toxicity. In: Hasanuzzaman M, Nahar K, Fujita M, Alam MM (eds) Plants under metal and metalloid stress. Springer, Singapore, pp 229–247

    Chapter  Google Scholar 

  • Phillips JM, Hayman DS (1970) Improved procedures for clearing roots and staining parasitic and vesicular-arbuscular mycorrhizal fungi for rapid assessment of infection. Trans Br Mycol Soc 55:158–161

    Article  Google Scholar 

  • Rady MM, El-Yazal MAS, Taie HAA, Ahmed SMAM (2016) Response of Triticum aestivum (L.) plants grown under cadmium stress to polyamines pretreatments. Plant 4:29–36

    Article  Google Scholar 

  • Rao KM, Sresty TVS (2000) Antioxidative parameters in the seedlings of pigeonpea (Cajanus cajan (L.) Millspaugh) in response to Zn and Ni stresses. Plant Sci 157:113–128

    Article  Google Scholar 

  • Rezvanypour S, Hatamzadeh A, Elahinia SA, Asghari HR (2015) Exogenous polyamines improve mycorrhizal development and growth and flowering of Freesia hybrida. J Hortic Res 23:17–25

    Article  CAS  Google Scholar 

  • Rucińska-Sobkowiak R (2016) Water relations in plants subjected to heavy metal stresses. Acta Physiol Plant 38:257–270

    Article  CAS  Google Scholar 

  • Saad R, Kobaissi A, Robin C, Echevarria G, Benizri E (2016) Nitrogen fixation and growth of Lens culinaris as affected by nickel availability, a pre-requisite for optimization of agromining. Environ Exp Bot 131:1–9

    Article  CAS  Google Scholar 

  • Sachan P, Lal N (2017) An overview of nickel (Ni2+) essentiality, toxicity and tolerance strategies in plants. Asian J Biol 2:1–15

    Article  Google Scholar 

  • Sairam RK, Deshmukh PS, Shukla DS (1997) Tolerance of drought and temperature stress in relation to increased antioxidant enzyme activity in wheat. J Agron Crop Sci 178:171–178

    Article  CAS  Google Scholar 

  • Salloum MS, Menduni MF, Benavides MP, Larrauri M, Luna CM, Silvente S (2018) Polyamines and flavonoids: key compounds in mycorrhizal colonization of improved and unimproved soybean genotypes. Symbiosis 76:265–275

    Article  CAS  Google Scholar 

  • Sannazzaro AI, Álvarez CL, Menéndez AB, Pieckenstain FL, Albertó EO, Ruiz OA (2004) Ornithine and arginine decarboxylase activities and effect of some polyamine biosynthesis inhibitors on Gigaspora rosea germinating spores. FEMS Microbiol Lett 230:115–121

    Article  CAS  Google Scholar 

  • Saxena KB, Kumar RV, Sultana R (2010) Quality nutrition through pigeonpea-a review. Health 2:1335–1344

    Article  Google Scholar 

  • Shevyakova NI, Il'ina EN, Stetsenko LA, Kuznetsov VV (2011) Nickel accumulation in rape shoots (Brassica napus L.) increased by putrescine. Int J Phytoremediation 13:345–356

    Article  CAS  Google Scholar 

  • Sirhindi G, Mir MA, Abd-Allah EF, Ahmad P, Gucel S (2016) Jasmonic acid modulates the physio-biochemical attributes, antioxidant enzyme activity, and gene expression in Glycine max under nickel toxicity. Front Plant Sci 7:591–603

    Article  Google Scholar 

  • Smith IK, Vierheller TL, Thorne CA (1988) Assay of glutathione reductase in crude tissue homogenates using 5, 5′-dithiobis (2-nitrobenzoic acid). Anal Biochem 175:408–413

    Article  CAS  Google Scholar 

  • Soares C, de Sousa A, Pinto A, Azenha M, Teixeira J, Azevedo RA, Fidalgo F (2016) Effect of 24-epibrassinolide on ROS content, antioxidant system, lipid peroxidation and Ni uptake in Solanum nigrum L. under Ni stress. Environ Exp Bot 122:115–125

    Article  CAS  Google Scholar 

  • Sreekanth TVM, Nagajyothi PC, Lee KD, Prasad TNVKV (2013) Occurrence, physiological responses and toxicity of nickel in plants. Int J Sci Environ Technol 10:1129–1140

    Article  CAS  Google Scholar 

  • Stark G (1991) The effect of ionizing radiation on lipid membranes. Biochim Biophys Acta Biomembr 1071:103–122

    Article  CAS  Google Scholar 

  • Szalai G, Tajti J, Hamow KÁ, Ildikó D, Khalil R, Vanková R, Dobrev P, Misheva SP, Janda T, Pál M (2020) Molecular background of cadmium tolerance in Rht dwarf wheat mutant is related to a metabolic shift from proline and polyamine to phytochelatin synthesis. Environ Sci Pollut Res 27:23664–23676

    Article  CAS  Google Scholar 

  • Tang W, Newton RJ (2005) Polyamines reduce salt-induced oxidative damage by increasing the activities of antioxidant enzymes and decreasing lipid peroxidation in Virginia pine. Plant Growth Regul 46:31–43

    Article  CAS  Google Scholar 

  • Tiburcio AF, Altabella T, Bitrián M, Alcázar R (2014) The roles of polyamines during the lifespan of plants, from development to stress. Planta 240:1–18

    Article  CAS  Google Scholar 

  • Twanabasu BR, Stevens KJ, Venables BJ (2013) The effects of triclosan on spore germination and hyphal growth of the arbuscular mycorrhizal fungus Glomus intraradices. Sci Total Environ 454:51–60

    Article  CAS  Google Scholar 

  • Vallino M, Massa N, Lumini E, Bianciotto V, Berta G, Bonfante P (2006) Assessment of arbuscular mycorrhizal fungal diversity in roots of Solidago gigantea growing in a polluted soil in Northern Italy. Environ Microbiol 8:971–983

    Article  Google Scholar 

  • Velikova V, Yordanov I, Edreva A (2000) Oxidative stress and some antioxidant systems in acid rain-treated bean plants, protective role of exogenous polyamines. Plant Sci 151:59–66

    Article  CAS  Google Scholar 

  • Wen XP, Ban Y, Inoue H, Matsuda N, Moriguchi T (2010) Spermidine levels are implicated in heavy metal tolerance in a spermidine synthase overexpressing transgenic European pear by exerting antioxidant activities. Transgenic Res 19:91–103

    Article  CAS  Google Scholar 

  • Wright SF, Upadhyaya A (1998) A survey of soils for aggregate stability and glomalin, a glycoprotein produced by hyphae of arbuscular mycorrhizal fungi. Plant Soil 198:97–107

    Article  CAS  Google Scholar 

  • Wu Q, Zou Y, He X (2010) Exogenous putrescine, not spermine or spermidine, enhances root mycorrhizal development and plant growth of trifoliate orange (Poncirus trifoliata) seedlings. Int J Agric Biol 12:576–580

    Google Scholar 

  • Zagorchev L, Seal CE, Kranner I, Odjakova M (2013) A central role for thiols in plant tolerance to abiotic stress. Int J Mol Sci 14:7405–7432

    Article  CAS  Google Scholar 

  • Zhang Y, Hu J, Bai J, Wang J, Yin R, Wang J, Lin X (2018) Arbuscular mycorrhizal fungi alleviate the heavy metal toxicity on sunflower (Helianthus annuus L.) plants cultivated on a heavily contaminated field soil at a WEEE-recycling site. Sci Total Environ 628:282–290

    Article  CAS  Google Scholar 

  • Zhao J, Shi G, Yuan Q (2008) Polyamines content and physiological and biochemical responses to ladder concentration of nickel stress in Hydrocharis dubia (Bl.) Backer leaves. Biometals 21:665–674

    Article  CAS  Google Scholar 

  • Zwiazek JJ, Blake TJ (1991) Early detection of membrane injury in black spruce (Picea mariana). Can J For Res 21:401–404

    Article  Google Scholar 

Download references

Acknowledgements

We gratefully acknowledge the UGC and DBT for providing financial support in undertaking this research work. We are also thankful to PAU, Panjab; IARI, New Delhi, India; and The Energy and Resource Institute (TERI), New Delhi for providing the biological research materials. The authors are also thankful to Sophisticated Analytical Instrumentation Facility (SAIF), Panjab University, Chandigarh, India for WD-XRF analysis.

Availability of data and materials

All data analyzed during this study are included in this article and supplementary materials.

Funding

We would like to thank to University Grants Commission (UGC) and the Department of Biotechnology (DBT), Government of India, for providing financial support in undertaking this research work.

Author information

Authors and Affiliations

  1. Department of Botany, Panjab University, Chandigarh, 160014, India

    Kiran Saroy & Neera Garg

Authors
  1. Kiran Saroy
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Neera Garg
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

The corresponding author (NG) planned and designed the research experiments. The first author (KS) performed the experiments. The both authors (KS, NG) contributed to the analysis and interpretation of the results and to the writing of the manuscript as well as gave final shape to the manuscript.

Corresponding author

Correspondence to Neera Garg.

Ethics declarations

Ethics approval and consent to participate

Not applicable.

Consent for publication

Both authors agreed and consented to publish this manuscript in present form.

Competing interests

The authors declare no competing interests.

Additional information

Responsible Editor: Philipp Gariguess

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Highlights

•Ni stress had negative correlation with growth, mycorrhizal colonization, and ROS.

•Put seed priming was more effective in reducing oxidative stress than Spd and Spm.

•AM was more effective than PAs in modulating ascorbate-glutathione (AsA-GSH) cycle.

•Functional complementarity between AM and PAs in reducing Ni uptake was recorded.

•+Put + AM was most promising in imparting Ni tolerance to pigeonpea genotypes

Supplementary information

Supplementary Fig. 1

Effect of PAs (Put, Spd, Spm) and arbuscular mycorrhiza (AM-Rhizoglomus intraradices) inoculation on a) SOD, b) CAT, c) GPOX, d) APOX, e) MDHAR and f) DHAR activities in leaves (nkat mg-1 protein) of Pusa 2001 and AL 201 pigeonpea genotypes under Ni stress. Values are the mean of six replicates ± standard error (SE). Different letters above each bar indicate significant differences among the treatments, assessed by Duncan multiple range test, at p ≤ 0.05. C=PAs and AM absent; Spm=0.5mM Spm added; Spd=0.5mM Spd added; Put=0.5mM Put added; AM=AM added; Ni100=100mg/kg Ni added; Ni200=200mg/kg Ni added; Spm+AM=Spm and AM added; Spd+AM=Spd and AM added; Put+AM=Put and AM added. (PNG 2806 kb)

High resolution image (TIF 35386 kb)

Supplementary Fig. 2

Effect of PAs (Put, Spd, Spm) and arbuscular mycorrhiza (AM-Rhizoglomus intraradices) inoculation on a) total ascorbate, b) ascorbate, c) dehydroascorbate in leaves (μmole g-1 FW), d) reduced glutathione (nmoles g-1 FW), e) oxidized glutathione (nmoles g-1 FW), f) GR activity in leaves (nkat mg-1 protein), of Pusa 2001 and AL 201 pigeonpea genotypes under Ni stress. Values are the mean of six replicates ± standard error (SE). Different letters above each bar indicate significant differences among the treatments, assessed by Duncan multiple range test, at p ≤ 0.05. C=PAs and AM absent; Spm=0.5mM Spm added; Spd=0.5mM Spd added; Put=0.5mM Put added; AM=AM added; Ni100=100mg/kg Ni added; Ni200=200mg/kg Ni added; Spm+AM=Spm and AM added; Spd+AM=Spd and AM added; Put+AM=Put and AM added (PNG 2915 kb)

High resolution image (TIF 36542 kb)

Supplementary Fig. 3

Effect of PAs (Put, Spd, Spm) and arbuscular mycorrhiza (AM-Rhizoglomus intraradices) inoculation on a) total glutathione, b) non-protein thiols, c) phytochelatins in leaves (nmol g-1 FW), of Pusa 2001 and AL 201 pigeonpea genotypes under Ni stress. Values are the mean of six replicates ± standard error (SE). Different letters above each bar indicate significant differences among the treatments, assessed by Duncan multiple range test, at p ≤ 0.05. C=PAs and AM absent; Spm=0.5mM Spm added; Spd=0.5mM Spd added; Put=0.5mM Put added; AM=AM added; Ni100=100mg/kg Ni added; Ni200=200mg/kg Ni added; Spm+AM=Spm and AM added; Spd+AM=Spd and AM added; Put+AM=Put and AM added. (PNG 1421 kb)

High resolution image (TIF 19355 kb)

ESM 1

(DOC 117 kb)

ESM 2

(DOC 71 kb)

ESM 3

(DOC 215 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Saroy, K., Garg, N. Relative effectiveness of arbuscular mycorrhiza and polyamines in modulating ROS generation and ascorbate-glutathione cycle in Cajanus cajan under nickel stress. Environ Sci Pollut Res 28, 48872–48889 (2021). https://doi.org/10.1007/s11356-021-13878-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11356-021-13878-7

Keywords

Search

Navigation