Skip to main content
SpringerLink
Log in

Influence of foliar glutathione and putrescine on metabolism and mineral status of genetically diverse rapeseed cultivars under hexavalent chromium stress

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

A Correction to this article was published on 29 May 2021

This article has been updated

Abstract

We studied the physio-biochemical involvement of exogenous signaling compounds, glutathione and putrescine (alone and in combination), on three contrasting genotypes (cvs. Shiralee, Rainbow, and Dunkled) of canola (Brassica napus L.) of plants exposed to chromium stress. Seeds were germinated in Cr-contaminated soil (0 and 50 μg/g Cr6+), and both signaling compounds were applied as a foliar spray to 20-day-old plants. Changes in root, stem, and leaf nitro-oxidative metabolism, endogenous GSH level, secondary metabolites, and mineral nutrients were investigated from 60-day-old plants. Exposure to Cr6+ increased stem GSH and NO concentrations in all cultivars. Maximum root Cr6+ bioaccumulation was recorded in cv. Rainbow and the least in cv. Shiralee. Also, Cr6+ stress decreased number and weight of seeds and pod length. Disturbances in root and shoot mineral profile were evident; however, its magnitude varied in all cultivars. The exogenous GSH improved root and shoot P, Fe, S, and Zn concentrations; however, the effect was cultivar specific. Leaf endogenous GSH was increased by exogenous GSH while NO levels remained unaffected. The GSH application also promoted shoot Cr6+ bioaccumulation while PUT application caused a recovery in seed number and seed weight. Both PUT and GSH differentially affected tissue-specific secondary metabolite profile. Overall, the exogenous GSH was much more effective in alleviating the Cr+6 toxicity in canola.

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
Fig. 4

Similar content being viewed by others

Data availability

Not applicable.

Change history

References

  • Adhikari A, Adhikari S, Ghosh S, Azahar I, Shaw AK, Roy D, Roy D, Saha S, Hossain Z (2020) Imbalance of redox homeostasis and antioxidant defense status in maize under chromium (VI) stress. Environ Exp Bot 169:103873

    Article  CAS  Google Scholar 

  • Aebi H (1984) Catalase in vitro. Methods Enzymol 105:121–126 Academic Press

    Article  CAS  Google Scholar 

  • Al Mahmud J, Hasanuzzaman M, Nahar K, Rahman A, Hossain MS, Fujita M (2017) Maleic acid assisted improvement of metal chelation and antioxidant metabolism confers chromium tolerance in Brassica juncea L. Ecotoxicol Environ Saf 144:216–226

    Article  CAS  Google Scholar 

  • Anjum NA, Ahmad I, Mohmood I, Pacheco M, Duarte AC, Pereira E et al (2012) Modulation of glutathione and its related enzymes in plants responses to toxic metals and metalloids - a review. Environ Exp Bot 75:307–324

    CAS  Google Scholar 

  • Apte AD, Tare V, Bose P (2006) Extent of oxidation of Cr (III) to Cr (VI) under various conditions pertaining to natural environment. J Hazard Mater 128(2-3):164–174

    Article  CAS  Google Scholar 

  • Barton CJ (1948) Photometric analysis of phosphate rock. AnalyChem 20(11):1068–1073

    CAS  Google Scholar 

  • Bashmakova EB, Pashkovskiy PP, Radyukina NL, Kuznetsov VV (2016) Interactive effects of zinc and nickel on the glutathione system state in Mimulusguttatus plants. Russ J Plant Physiol 63(5):626–635

    Article  CAS  Google Scholar 

  • Bates LS, Waldren RP, Teare ID (1973) Rapid determination of free proline for water-stress studies. Plant Soil 39(1):205–207

    Article  CAS  Google Scholar 

  • Belouchrani AS, Mameri N, Abdi N, Grib H, Lounici H, Drouichec N (2016) Phytoremediation of soil contaminated with Zn using Canola (Brassica napus L). EcolEng 95:43–49

    Google Scholar 

  • Bolan NS, Adriano DC, Natesan R, Koo BJ (2003) Effects of organic amendments on the reduction and phytoavailability of chromate in mineral soil. J Environ Qual 32:120–128

    Article  CAS  Google Scholar 

  • Brasili E, Bavasso I, Petruccelli V, Vilardi G, Valletta A, Dal Bosco C et al (2020) Remediation of hexavalent chromium contaminated water through zero-valent iron nanoparticles and effects on tomato plant growth performance. Sci Rep 10(1):1–11

    Article  CAS  Google Scholar 

  • Bruno LB, Karthik C, Ma Y, Kadirvelu K, Freitas H, Rajkumar M (2020) Amelioration of chromium and heat stresses in Sorghum bicolor by Cr6+ reducing-thermotolerant plant growth promoting bacteria. Chemosphere 244:125521

    Article  CAS  Google Scholar 

  • Cao F, Fu M, Wang R, Diaz-Vivancos P, Hossain MA (2017) Exogenous glutathione-mediated abiotic stress tolerance in plants. In: Glutathione in Plant Growth, Development, and Stress Tolerance. Springer, Cham, pp 171–194

    Chapter  Google Scholar 

  • Cervantes C, Campos-García J, Devars S, Gutiérrez-Corona F, Loza-Tavera H, Torres-Guzmán JC, Moreno-Sánchez R (2001) Interactions of chromium with microorganisms and plants. FEMS Microbiol Rev 25:335–347

    Article  CAS  Google Scholar 

  • Christou A, Georgiadou EC, Zissimos AM, Christoforou IC, Christofi C, Neocleous D, Dalias P, Torrado S, Argyraki A, Fotopoulos V (2020) Hexavalent chromium leads to differential hormetic or damaging effects in alfalfa (Medicago sativa L.) plants in a concentration-dependent manner by regulating nitro-oxidative and proline metabolism. Environ Pollut (267):115379

  • Cui J, Pottosin I, Lamade E, Tcherkez G (2020) What is the role of putrescine accumulated under potassium deficiency? Plant Cell Environ 43(6):1331–1347

    Article  CAS  Google Scholar 

  • Datta R, Kumar D, Sultana A, Hazra S, Bhattacharyya D, Chattopadhyay S (2015) Glutathione regulates 1-aminocyclopropane-1-carboxylate synthase transcription via WRKY33 and 1-aminocyclopropane-1-carboxylate oxidase by modulating messenger RNA stability to induce ethylene synthesis during stress. Plant Physiol 169(4):2963–2981

    CAS  Google Scholar 

  • Davies FT, Puryear JD, Newton RJ, Egilla JN, Grossi JAS (2002) Mycorrhizal fungi increase chromium uptake by sunflower plants: influence on tissue mineral concentration, growth and gas exchange. J Plant Nutr 25:2389–2407

    Article  CAS  Google Scholar 

  • Fan WJ, Feng YX, Li YH, Lin YJ, Yu XZ (2020) Unraveling genes promoting ROS metabolism in subcellular organelles of Oryza sativa in response to trivalent and hexavalent chromium. Sci Total Environ 744:140951

    Article  CAS  Google Scholar 

  • Freschi L (2013) Nitric oxide and phytohormone interactions: current status and perspectives. Front Plant Sci 4:398

    Article  Google Scholar 

  • Gao M, Wu Y, She Z et al (2020) Single and combined effects of divalent copper and hexavalent chromium on the performance, microbial community and enzymatic activity of sequencing batch reactor. Sci Total Environ 719:137289

    Article  CAS  Google Scholar 

  • Gopal R, Rizvi AH, Nautiyal N (2009) Chromium alters iron nutrition and water relations of spinach. J Plant Nutr 32:1551–1559

    Article  CAS  Google Scholar 

  • Guo X, Ji Q, Rizwan M, Li H, Li D, Chen G (2020) Effects of biochar and foliar application of selenium on the uptake and subcellular distribution of chromium in Ipomoea aquatica in chromium-polluted soils. EcotoxEnvSaf 206:111184

    CAS  Google Scholar 

  • Gupta D, Huang H, Yang X, Razafindrabe B, Inouhe M (2010) The detoxification of lead in Sedum alfredii is not related to phytochelatins but the glutathione. J Hazard Mater 177:437–444

    Article  CAS  Google Scholar 

  • Han FX, Sridhar BM, Monts DL, Su Y (2004) Phytoavailability and toxicity of trivalent and hexavalent chromium to Brassica juncea. New Phytol 162(2):489–499

    Article  CAS  Google Scholar 

  • Hasan MK, Liu C, Wang F, Ahammed GJ, Zhou J, Xu MX, Yu JQ, Xia XJ (2016) Glutathione-mediated regulation of nitric oxide, S-nitrosothiol and redox homeostasis confers cadmium tolerance by inducing transcription factors and stress response genes in tomato. Chemosphere 161:536–545

    Article  CAS  Google Scholar 

  • Hendrix S, Jozefczak M, Wójcik M, Deckers J, Vangronsveld J, Cuypers A (2020) Glutathione: A key player in metal chelation, nutrient homeostasis, cell cycle regulation and the DNA damage response in cadmium-exposed Arabidopsis thaliana. Plant Physiol Biochem 154:498–507

    Article  CAS  Google Scholar 

  • Hider RC, Liu ZD, Khodr HH (2001) Metal chelation of polyphenols. Methods Enzymol 335:190–203

    Article  CAS  Google Scholar 

  • International Agency for Research on Cancer (1990) Monographs on the evaluation of carcinogenic risks to humans: chromium nickel and welding. World Health Organization 49:19–527

  • Jahan A (2021) Role of exogenous glutathione and putrescine in the alleviation of hexavalent chromium [Cr(VI)] toxicity in diverse canola (Brassica napus L.) cultivars. PhD Dissertation, Government College University Faisalabad, Pakistan.

  • Kakkar P, Das B, Viswanathan PN (1984) A modified spectrophotometric assay of superoxide dismutase. Indian J Biochem Biophys 21:130–132

    CAS  Google Scholar 

  • Khan I, Iqbal M, Ashraf MY, Ashraf MA, Ali S (2016) Organic chelants-mediated enhanced lead (Pb) uptake and accumulation is associated with higher activity of enzymatic antioxidants in spinach (SpinaceaoleraceaL.). J Hazard Mater 317:352–361

    Article  CAS  Google Scholar 

  • Khanna K, Kohli SK, Ohri P, Bhardwaj R, Al-Huqail AA, Siddiqui MH et al (2019) Microbial fortification improved photosynthetic efficiency and secondary metabolism in Lycopersicon esculentum plants under cd stress. Biomolecules 9(10):581

    Article  CAS  Google Scholar 

  • Kharbech O, Houmani H, Chaoui A, Corpas FJ (2017) Alleviation of Cr(VI)-induced oxidative stress in maize (Zea mays L.) seedlings by NO and H2S donors through differential organ-dependent regulation of ROS and NADPH-recycling metabolisms. J Plant Physiol 219:71–80

    Article  CAS  Google Scholar 

  • Kiełkowska A, Dziurka M (2021) Changes in polyamine pattern mediates sex differentiation and unisexual flower development in monoecious cucumber (CucumissativusL.). Physiol Plant. https://doi.org/10.1111/ppl.13197

  • Kim Y, Bae HJ, Cho E, Kang H (2017) Exogenous glutathione enhances mercury tolerance by inhibiting mercury entry into plant cells. Front Plant Sci 8:683

    Article  Google Scholar 

  • Kisa D, Elmastaş M, Öztürk L, Kayır Ö (2016) Responses of the phenolic compounds of Zea mays under heavy metal stress. Appl Biol Chem 59(6):813–820

    Article  CAS  Google Scholar 

  • Kubo H, Peeters AJ, Aarts MG, Pereira A, Koornneef M (1999) ANTHOCYANINLESS2, a homeobox gene affecting anthocyanin distribution and root development in Arabidopsis. Plant Cell 11(7):1217–1226

    Article  CAS  Google Scholar 

  • Kumar V, Sharma PK, Jatav HS, Singh SK, Rai A, Kant S, Kumar A (2020) Organic amendments application increases yield and nutrient uptake of mustard (Brassica juncea) grown in chromium-contaminated soils. Commun Soil Sci Plant Anal 51(1):149–159

    Article  CAS  Google Scholar 

  • Kusano T, Berberich T, Tateda C, Takahashi Y (2008) Polyamines: essential factors for growth and survival. Planta 228:367–381

    Article  CAS  Google Scholar 

  • Kushwaha BK, Singh VP (2020) Mitigation of chromium (VI) toxicity by additional sulfur in some vegetable crops involves glutathione and hydrogen sulfide. Plant Physiol Biochem 155:952–964

    Article  CAS  Google Scholar 

  • Landi M (2015) Can anthocyanins be part of the metal homeostasis network in plant. Am J Agric Biol Sci 10:170–177

    Article  CAS  Google Scholar 

  • Liang X, Zhang L, Natarajan SK, Becker DF (2013) Proline mechanisms of stress survival. Antioxid Redox Signal 19(9):998–1011

    Article  CAS  Google Scholar 

  • Liu J, Duan CQ, Zhang XH, Zhu YN, Hu C (2011) Characteristics of chromium (III) uptake in hyperaccumulatorLeersiahexandra Swartz. Environ Exp Bot 74:122–126

    Article  CAS  Google Scholar 

  • Michalak A (2006) Phenolic compounds and their antioxidant activity in plants growing under heavy metal stress. Pol J Environ Stud 15(4):523–530

  • Mohammadi AA, Zarei A, Majidi S, Ghaderpoury A, Hashempour Y, Saghi MH, Aliejad A, Yousefi M, Hosseingolizadeih N, Ghaderpoori M (2019) Carcinogenic and non-carcinogenic health risk assessment of heavy metals in drinking water of Khorramabad, Iran. MethodsX 6:1642–1651

    Article  Google Scholar 

  • Montilla-Bascón G, Rubiales D, Hebelstrup KH, Mandon J, Harren FJ, Cristescu SM, Mur J, Prats E (2017) Reduced nitric oxide levels during drought stress promote drought tolerance in barley and is associated with elevated polyamine biosynthesis. Sci Rep 7(1):1–15

    Article  CAS  Google Scholar 

  • Moreira OC, Rios PF, Barrabin H (2005) Inhibition of plasma membrane Ca2+-ATPase by CrATP. LaATP but not Cr ATP stabilizes the Ca2+-occluded state. BBA Bioenerg 3:411–419

    Article  CAS  Google Scholar 

  • Moron MS, Depierre JW, Mannervik B (1979) Levels of glutathione, glutathione reductase and glutathione S-transferase activities in rat lung and liver. Biochim Biophys Acta 582(1):67–78

    Article  CAS  Google Scholar 

  • Moshage H, Kok B, Huizenga JR, Jansen PL (1995) Nitrite and nitrate determinations in plasma: a critical evaluation. ClinChem 41(6):892–896

    CAS  Google Scholar 

  • Mukherjee SP, Choudhuri MA (1983) Implications of water stress induced changes in the levels of endogenous ascorbic acid and hydrogen peroxide in vigna seedlings. Physiol Plant 58(2):166–170

    Article  CAS  Google Scholar 

  • Mutlu F, Yürekli F (2015) Analysis of interactions of nitric oxide and polyamine under cadmium stress in wheat. Turk J Bot 39(5):778–785

    Article  CAS  Google Scholar 

  • Nahar K, Hasanuzzaman M, Rahman A, Alam M, Mahmud JA, Suzuki T, Fujita M (2016) Polyamines confer salt tolerance in mung bean (Vignaradiata L.) by reducing sodium uptake, improving nutrient homeostasis, antioxidant defense, and methylglyoxal detoxification systems. Fron. Plant Sci 7:1104

    Google Scholar 

  • Naikoo MI, Dar MI, Raghib F, Jaleel H, Ahmad B, Raina A, Khan FA, Naushin F (2019) Chapter 9 - Role and regulation of plants phenolics in abiotic stress tolerance: an overview. In: Iqbal M, Khan R, Reddy PS, Ferrante A, Khan NA (eds) Plant Signaling Molecules, Woodhead Publishing, p 157–168. https://doi.org/10.1016/B978-0-12-816451-8.00009-5

  • Nematshahi N, Lahouti M, Ganjali A (2012) Accumulation of chromium and its effect on growth of Allium cepa cv. Hybrid. Eur J Exp Biol 2:969–974

    CAS  Google Scholar 

  • Okello VA, Mwilu S, Noah N, Zhou A, Chong J, Knipfing MT, Doetschman D, Sadik OA (2012) Reduction of hexavalent chromium using naturally-derived flavonoids. Environ Sci Technol 46(19):10743–10751

    Article  CAS  Google Scholar 

  • Oliveira H (2012). Chromium as an environmental pollutant: insights on induced plant toxicity. J Bot (2012):375843

  • Patra DK, Pradhan C, Kumar J, Patra HK (2020) Assessment of chromium phytotoxicity, phytoremediation and tolerance potential of Sesbaniasesban and Brachiariamutica grown on chromite mine overburden dumps and garden soil. Chemosphere (252):126553

  • Per TS, Masood A, Khan NA (2017) Nitric oxide improves S-assimilation and GSH production to prevent inhibitory effects of cadmium stress on photosynthesis in mustard (Brassica junceaL.). Nitric Oxide 68:111–124

    Article  CAS  Google Scholar 

  • Repkina N, Talanova V, Ignatenko A, Titov A (2019) Involvement of proline and non-protein thiols in response to low temperature and cadmium stresses in wheat. Biol Plant 63(1):70–77

    Article  CAS  Google Scholar 

  • Shafiq F, Iqbal M, Ali M, Ashraf MA (2021) Fullerenol regulates oxidative stress and tissue ionic homeostasis in spring wheat to improve net-primary productivity under salt-stress. Ecotoxicol Environ Saf 211:111901

    Article  CAS  Google Scholar 

  • Shahid M, Shamshad S, Rafiq M, Khalid S, Bibi I, Niazi NK, Dumat C, Rashid MI (2017) Chromium speciation, bioavailability, uptake, toxicity and detoxification in soil-plant system: a review. Chemosphere 178:513–533

    Article  CAS  Google Scholar 

  • Sharma A, Kapoor D, Wang J, Shahzad B, Kumar V, Bali AS, Jasrotia S, Zheng B, Yuan H, Yan D (2020a) Chromium bioaccumulation and its impacts on plants: an overview. Plants 9(1):100

    Article  CAS  Google Scholar 

  • Sharma A, Soares C, Sousa B, Martins M, Kumar V, Shahzad B et al (2020b) Nitric oxide-mediated regulation of oxidative stress in plants under metal stress: a review on molecular and biochemical aspects. Physiol Plant 168(2):318–344

    CAS  Google Scholar 

  • Soudek P, Ursu M, Petrová Š, Vaněk T (2016) Improving crop tolerance to heavy metal stress by polyamine application. Food Chem 213:223–229

    Article  CAS  Google Scholar 

  • Stambulska UY, Bayliak MM, Lushchak VI (2018) Chromium (VI) toxicity in legume plants: modulation effects of rhizobial symbiosis. BioMed Res Intl 3:1–13

    Article  CAS  Google Scholar 

  • Sundaramoorthy P, Murugan A, Ganesh KS (2018) Effect of chromium on growth and yield of Vignamungo (L.). J Plant Stress Physiol (4):17–21

  • Tabatabai MA, Bremner JM (1970) A simple turbidimetric method of determining total sulfur in plant materials. Agron J 62(6):805–806

    Article  CAS  Google Scholar 

  • Tai Y, Yang Y, Li Z, Yang Y, Wang J, Zhuang P, Zou B (2018) Phytoextraction of 55-year-old wastewater-irrigated soil in a Zn–Pb mine district: effect of plant species and chelators. Environ Technol 39:2138–2150

    Article  CAS  Google Scholar 

  • Wang W, Paschalidis K, Feng JC, Song J, Liu JH (2019) Polyamine catabolism in plants: a universal process with diverse functions. Front Plant Sci 10:561

    Article  CAS  Google Scholar 

  • Wolfe KL, Liu RH (2003) Apple peels as a value-added food ingredient. J Agric Food Chem 6:1676–1683

    Article  CAS  Google Scholar 

  • Xu Z, Wang M, Xu D, Xia Z (2020) The Arabidopsis APR2 positively regulates cadmium tolerance through glutathione-dependent pathway. Ecotoxicol Environ Saf 187:109819

    Article  CAS  Google Scholar 

  • Yang H, Shi G, Wang H, Xu Q (2010) Involvement of polyamines in adaptation of Potamogetoncrispus L. to cadmium stress. AquatToxicol 100:282–288

    Google Scholar 

  • Yin Y, Gu J, Wang X, Song W, Zhang K, Zhang X et al (2017) Effects of chromium (III) on enzyme activities and bacterial communities during swine manure composting. Bioresour Technol 243:693–699

    Article  CAS  Google Scholar 

  • Yu Q, Sun L, Jin H, Chen Q, Chen Z, Xu M (2012) Lead-induced nitric oxide generation plays a critical role in lead uptake by Pogonatherumcrinitum root cells. Plant Cell Physiol 53(10):1728–1736

    Article  CAS  Google Scholar 

  • Zhang Y, Chen J, Shi W, Zhang D, Zhu T, Li X (2017) Establishing a human health risk assessment methodology for metal species and its application of Cr6+ in groundwater environments. Chemosphere 189:525–537

    Article  CAS  Google Scholar 

  • Zhishen J, Mengcheng T, Jianming W (1999) The determination of flavonoid contents in mulberry and their scavenging effects on superoxide radicals. Food Chem 64(4):555–559

    Article  CAS  Google Scholar 

  • Zhu X, Wang L, Yang R, Han Y, Hao J, Liu C, Fan S (2019) Effects of exogenous putrescine on the ultrastructure of and calcium ion flow rate in lettuce leaf epidermal cells under drought stress. Hortic Environ Biotechnol 60(4):479–490

    Article  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Botany, Government College University Faisalabad, Faisalabad, Pakistan

    Almas Jahan, Muhammad Iqbal & Muhammad Tariq Javed

  2. Institute of Molecular Biology and Biotechnology, The University of Lahore, Lahore, Pakistan

    Fahad Shafiq & Arif Malik

Authors
  1. Almas Jahan
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Muhammad Iqbal
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Fahad Shafiq
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Arif Malik
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Muhammad Tariq Javed
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

Almas Jahan conducted the experiments, conducted various biochemical analyses, and wrote the initial draft of this manuscript. Muhammad Iqbal designed the research, supervised the study, and edited the manuscript draft. Fahad Shafiq assisted in ion analyses, manuscript preparation, and data presentation. Arif Malik and Muhammad Tariq Javed critically revised and updated the manuscript.

Corresponding authors

Correspondence to Almas Jahan or Fahad Shafiq.

Ethics declarations

Ethics approval and consent to participate

Not applicable.

Conflict of interest

The authors declare no competing interests.

Consent for publication

All the authors agreed with the submission of this article in this journal and subsequent publication.

Additional information

Responsible Editor: Gangrong Shi

Publisher’s note

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

Supplementary Information

ESM 1

(DOCX 108 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Jahan, A., Iqbal, M., Shafiq, F. et al. Influence of foliar glutathione and putrescine on metabolism and mineral status of genetically diverse rapeseed cultivars under hexavalent chromium stress. Environ Sci Pollut Res 28, 45353–45363 (2021). https://doi.org/10.1007/s11356-021-13702-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11356-021-13702-2

Keywords

Search

Navigation