Skip to main content
Log in

Aluminium-induced excessive ROS causes cellular damage and metabolic shifts in black gram Vigna mungo (L.) Hepper

  • Original Article
  • Published:
Protoplasma Aims and scope Submit manuscript

Abstract

Aluminium-induced oxidative damage caused by excessive ROS production was evaluated in black gram pulse crop. Black gram plants were treated with different aluminium (Al3+) concentrations (10, 50 and 100 μM with pH 4.7) and further the effects of Al3+ were characterised by means of root growth inhibition, histochemical assay, ROS content analysis, protein carbonylation quantification and 1H-NMR analysis. The results showed that aluminium induces excessive ROS production which leads to cellular damage, root injury, stunt root growth and other metabolic shifts. In black gram, Al3+ induces cellular damage at the earliest stage of stress which was characterised from histochemical analysis. From this study, it was observed that prolonged stress can activate certain aluminium detoxification defence mechanism. Probably excessive ROS triggers such defence mechanism in black gram. Al3+ can induce excessive ROS initially in the root region then transported to other parts of the plant. As much as the Al3+ concentration increases, the rate of cellular injury and ROS production also increases. But after 72 h of stress, plants showed a lowered ROS level and cellular damage which indicates the upregulation of defensive mechanisms. Metabolic shift analysis also showed that the black gram plant under stress has less metabolic content after 24 h of treatment, but gradually, it was increased after 72 h of treatment. It was assumed that ROS played the most important role as a signalling molecule for aluminium stress in black gram.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

Abbreviations

ROS:

Reactive oxygen species

Al3+ :

Aluminium

PC:

Protein carbonylation

H2O2 :

Hydrogen peroxide

FW:

Fresh weight

DW:

Dry weight

References

  • Achary VM, Jena S, Panda KK, Panda BB (2008) Aluminium induced oxidative stress and DNA damage in root cells of Allium cepa L. Ecotoxicol Environ Saf 70(2):300–310

    Article  CAS  PubMed  Google Scholar 

  • Aftab T, Khan MMA, Idress M, Naeem M, Moinuddin (2010) Effects of aluminum exposures on growth, photosynthetic efficiency, lipid peroxidation, antioxidation, antioxidant enzymes and artemisinin content of Artemisia annua L. J Phytol 2:23–37

    Google Scholar 

  • Andrews F, Johan Bjorkten FB, Trenk AS, Koch RB (1965) The reaction of an auto oxidized lipids with proteins. J Am Oil Chem Soc 42:779–781

    Article  CAS  PubMed  Google Scholar 

  • Boscolo PRS, Menossi M, Jorge R a (2003) Aluminum-induced oxidative stress in maize. Phytochemistry 62(2):181–189

    Article  CAS  PubMed  Google Scholar 

  • Cançado GMA, Loguercio LL, Martins PR, Parentoni SN, Paiva E, Borém A, Lopes MA (1999) Hematoxylin staining as a phenotypic index for aluminum tolerance selection in tropical maize (Zea mays L.). TAG Theor Appl Genet 99(5):747–754

    Article  Google Scholar 

  • Carvalho MCS, van Raij B (1997) Calcium sulphate, phosphogypsum and calcium carbonate in the amelioration of acid subsoils for root growth. Plant Soil 192(1):37–48

    Article  CAS  Google Scholar 

  • Elstner EF (1982) Oxygen activation and oxygen toxicity. Annu Rev Plant Physiol 33(1):73–96

    Article  CAS  Google Scholar 

  • Elstner EF, Heupel A (1976) Formation of hydrogen peroxide by isolated cell walls from horseradish (Armoracia lapathifolia Gilib.). Planta 130(2):175–80

    Article  CAS  PubMed  Google Scholar 

  • Elstner EF, Wagner GA, Schutz W (1988) Activated oxygen in green plants in relation to stress situations. Curr Top Plant Biochem Physiol 7:159–187

    Google Scholar 

  • Foy CD (1988) Plant adaptation to acid, aluminium toxic soils. Commun Soil Sci Plant Anal 19:959–987

    Article  CAS  Google Scholar 

  • Hai TV, Nga TT, Laudelout H (1989) Effect of aluminium on the mineral nutrition of rice. Plant Soil 114(2):173–185

    Article  Google Scholar 

  • Hare PD, Cress WA (1997) Metabolic implications of stress-induced proline accumulation in plants. Plant Growth Regul 21:79–102

    Article  CAS  Google Scholar 

  • Hippeli S, Heiser I, Elstner EF (1999) Activated oxygen and free oxygen radicals in pathology: new insights and analogies between animals and plants. Plant Physiol Biochem 37(3):167–178

    Article  CAS  Google Scholar 

  • Ikegawa H, Yamamoto Y, Matsumoto H (1998) Cell death caused by a combination of aluminum and iron in cultured tobacco cells. Physiol Plant 104(3):474–478

    Article  CAS  Google Scholar 

  • Ikegawa H, Yamamoto Y, Matsumoto H (2000) Responses to aluminum of suspension-cultured tobacco cells in a simple calcium solution. Soil Sci Plant Nutr 46:503–514

    CAS  Google Scholar 

  • Juszczuk IM, Tybura A, Rychter AM (2008) Protein oxidation in the leaves and roots of cucumber plants (Cucumis sativus L.), mutant MSC16 and wild type. J Plant Physiol 165(4):355–365

    Article  CAS  PubMed  Google Scholar 

  • Kim C, Meskauskiene R, Apel K, Laloi C (2008) No single way to understand singlet oxygen signalling in plants. EMBO Rep 9(5):435–9

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kim HK, Choi YH, Verpoote R (2010) NMR based metabolomic analysis of plants. Nat Protoc 5:536–549

    Article  CAS  PubMed  Google Scholar 

  • Kruger NJ, Troncoso-Ponce MA, Ratcliffe RG (2008) 1H NMR metabolite fingerprinting and metabolomic analysis of perchloric acid extracts from plant tissues. Nat Protoc 3(6):1001–12

    Article  CAS  PubMed  Google Scholar 

  • Levine RL, Williams JA, Stadtman ER, Shacter E (1994) Carbonyl assays for determination of oxidatively modified proteins. Methods Enzymol 233:346–357

    Article  CAS  PubMed  Google Scholar 

  • Meriga B, Krishna Reddy B, Rajender Rao K, Ananda Reddy L, Kavi Kishor PB (2003) Alleviating effect of citrate on aluminium toxicity of rice (Oryza sativa L.) seedling. Curr Sci 85(3):63–68

    Google Scholar 

  • Meriga B, Krishna Reddy B, Rajender Rao K, Ananda Reddy L, Kavi Kishor PB (2004) Aluminium-induced production of oxygen radicals, lipid peroxidation and DNA damage in seedlings of rice (Oryza sativa). J Plant Physiol 161(1):63–68

    Article  CAS  PubMed  Google Scholar 

  • Ohki K (1987) Aluminum stress on sorghum growth and nutrient relationships. Plant Soil 98(2):195–202

    Article  CAS  Google Scholar 

  • Ownby JD (1993) Mechanisms of reaction of hematoxylin with aluminium-treated wheat roots. Physiol Plant 87(3):371–380

    Article  CAS  Google Scholar 

  • Panda SK, Matsumoto H (2010) Changes in antioxidant gene expression and induction of oxidative stress in pea (Pisum sativum L.) under Al stress. BioMetals 23(4):753–762

    Article  CAS  PubMed  Google Scholar 

  • Panda SK, Singha LB, Khan MH (2003) Does aluminium phytotoxicity induce oxidative stress in greengram (Vigna radiata)? Bulg J Plant Physiol 29(1–2):77–86

    Google Scholar 

  • Panda SK, Baluska F, Matsumoto H (2009) Aluminum stress signaling in plants. Plant Signal Behav 4(7):592–7

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pollard A, Wyn Jones RG (1979) Enzyme activities in concentrated solutions of glycinebetaine and other solutes. Planta 144:291–298

    Article  CAS  PubMed  Google Scholar 

  • Pompella A, Maellaro E, Casini AF, Comporti M (1987) Histochemical detection of lipid peroxidation in the liver of bromobenzene-poisoned mice. Am J Pathol 129(2):295–301

    CAS  PubMed  PubMed Central  Google Scholar 

  • R Core Team (2013) A language and environment for statstical computing. R foundation for statstical computing, Vienna, Austria. URL http://www.R-project.org/

  • Ryan PR, Shaff JE, Kochian LV (1992) Aluminum toxicity in roots: correlation among ionic currents, ion fluxes, and root elongation in aluminum-sensitive and aluminum-tolerant wheat cultivars. Plant Physiol 99(3):1193–1200

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sagisaka S (1976) The occurrence of peroxide in a perennial plant Populas gelrica. Plant Physiol 57:308–309

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shao HB, Chu LY, Lu ZH, Kang CM (2008) Primary antioxidant free radical scavenging and redox signaling pathways in higher plant cells. Int J Biol Sci 4(1):8–14

    Article  CAS  Google Scholar 

  • Sharma M, Trofimova M, Sharma V, Tripathi BN (2015) Genotypic variation to aluminium sensitivity in chickpea depends on its ability to efficiently accumulate nitrate. Adv Agron Plant Sci 01(01):1–12

    Google Scholar 

  • Singh D, Singh NP, Chauhan SK, Singh P (2011) Developing aluminium-tolerant crop plants using biotechnological tools. Curr Sci 100(12):1807–1814

    CAS  Google Scholar 

  • Smirnoff N, Cumbes QJ (1989) Hydroxyl radical scavenging activity of compatible solutes. Phytochemistry 28:1057–1060

    Article  CAS  Google Scholar 

  • Song H, Xu X, Wang H, Wang H, Tao Y (2010) Exogenous gamma-aminobutyric acid alleviates oxidative damage caused by aluminium and proton stresses on barley seedlings. J Sci Food Agric 90(9):1410–6

    Article  CAS  PubMed  Google Scholar 

  • Taylor GJ (1995) Overcoming barriers to understanding the cellular basis of aluminium resistance. Plant Soil 171(1):89–103

    Article  CAS  Google Scholar 

  • Van HL, Kuraishi S, Sakuraj N (1994) Aluminium-induced rapid root inhibition and changes in cell-wall components of squash seedlings. Plant Physiol 106:971–976

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Von Uexküll HR, Mutert E (1995) Global extent, development and economic impact of acid soils. Plant Soil 171(1):1–15

    Article  Google Scholar 

  • Wang YS, Wang J, Yang ZM, Wang QY, Lu B, Li SQ, Lu YP, Wang SH, Sun X (2004) Salicylic acid modulates aluminum-induced oxidative stress in roots of Cassia tora. Acta Bot Sin-Eng Edn 46:819–828

    CAS  Google Scholar 

  • Wang L, Fan X-W, Pan J-L, Huang Z-B, Li Y-Z (2015) Physiological characterization of maize tolerance to low dose of aluminum, highlighted by promoted leaf growth. Planta. doi:10.1007/s00425-015-2376-3

    Google Scholar 

  • Wickham H (2009) ggplot2: Elegant graphics for data analysis. Springer-Verlag New York

  • Wu K, Xiao S, Chen Q, Wang Q, Zhang Y, Li K, Chen L (2012) Changes in the activity and transcription of antioxidant enzymes in response to Al stress in black soybeans. Plant Mol Biol Report 31(1):141–150

    Article  CAS  Google Scholar 

  • Yamamoto Y (2001) Lipid peroxidation is an early symptom triggered by aluminum, but not the primary cause of elongation inhibition in pea roots. Plant Physiol 125(1):199–208

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgments

We sincerely thank DBT, Govt. of India, for providing the facility for the research work. We thank IIPR, Kanpur, for providing black gram seeds for the present research work. We also sincerely thank DBT-Biotech Hub, Assam University, Silchar, for providing the facility for the research work.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Umakanta Chowra.

Ethics declarations

Conflict of interest

The authors declare that they have no competing interests.

Additional information

Handling Editor: Néstor Carrillo

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Chowra, U., Yanase, E., Koyama, H. et al. Aluminium-induced excessive ROS causes cellular damage and metabolic shifts in black gram Vigna mungo (L.) Hepper. Protoplasma 254, 293–302 (2017). https://doi.org/10.1007/s00709-016-0943-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00709-016-0943-5

Keywords

Navigation