Skip to main content
SpringerLink
Log in

Iron- and manganese-assisted cadmium tolerance in Oryza sativa L.: lowering of rhizotoxicity next to functional photosynthesis

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

Abstract

Main conclusion

Cadmium toxicity is alleviated by iron and manganese supplements because of reduction in cadmium accumulation and upholding of redox regulation that prevent cadmium-inducible damage to root growth and photosynthesis.

Cadmium toxicity in Oryza sativa L. MTU 7029 was investigated in the presence of different concentrations of the micronutrients Fe and Mn. It had been observed that these micronutrients reduce Cd uptake and minimize Cd-inducible rhizotoxicity. The photosynthetic electron transport chain, which is the hub of Fe containing metalloproteins, was severely affected by Cd and resulted in reduced bioproductivity under Cd stress. However, exogenous Fe restored the photosynthetic electron transport. Thus, due to the maintenance of the photosynthetic electron transport, the Cd tolerance was improved during Fe supplement. Both antioxidant enzymes and non-enzymatic antioxidant metabolites were found to play important roles in the alleviation of Cd stress under Fe or Mn supplement. It is concluded that the presence of excess Fe and Mn protects rice plants from Cd stress.

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
Fig. 5

Similar content being viewed by others

Abbreviations

LHCII:

Light-harvesting complex II

MDA:

Malondialdehyde

NADPH:

Nicotinamide adenine dinucleotide phosphate

NPQ:

Nonphotochemical quenching

PQ:

Plastoquinone

ROS:

Reactive oxygen species

References

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

    Article  CAS  PubMed  Google Scholar 

  • Asada K (2006) Production and scavenging of reactive oxygen species in chloroplasts and their function. Plant Physiol 141:391–396

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Beadle CL, Long SP (1985) Photosynthesis—is it limiting to biomass production? Biomass 8:119–168

    Article  CAS  Google Scholar 

  • Beauchamp C, Fridovich I (1971) Superoxide dismutase: improved assays and an assay applicable to acrylamide gels. Anal Biochem 44:276–287

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Cappa JJ, Pilon-Smits EAH (2014) Evolutionary aspects of elemental hyperaccumulation. Planta 239:267–275

    Article  CAS  PubMed  Google Scholar 

  • Dubios M, Gilles KA, Hamilton JK, Rebers PA, Smith F (1956) Colorimetric method for determination of sugars and related substances. Anal Chem 28:350–356

    Article  Google Scholar 

  • Eshaghi S, Andersson B, Barbe J (1999) Isolation of a highly active PSII-LHCII supercomplex from thylakoid membranes by a direct method. FEBS Lett 446:23–26

    Article  CAS  PubMed  Google Scholar 

  • Fidalgo F, Freitas R, FerreiraR Pessoa AM, Teixeira J (2011) Solanum nigrum L. antioxidant defence system isozymes are regulated transcriptionally and posttranslationally in Cd-induced stress. Environ Exp Bot 72:312–319

    Article  CAS  Google Scholar 

  • Gill SS, Tuteja N (2011) Cadmium stress tolerance in crop plants-probing the role of sulfur. Plant Signal Behav 6:215–222

    Article  CAS  PubMed  Google Scholar 

  • Guha A, Sengupta D, Reddy AR (2013) Polyphasic chlorophyll a fluorescence kinetics and leaf protein analyses to track dynamics of photosynthetic performance in mulberry during progressive drought. J Photochem Photobiol B Biol 119:71–83

    Article  CAS  Google Scholar 

  • Hall JL, Williams LE (2003) Transition metal transporters in plants. J Exp Bot 54:2601–2613

    Article  CAS  PubMed  Google Scholar 

  • Heath RL, Packer L (1968) Photoperoxidation in isolated chloroplasts. 1. Kinetics and stoichiometry of fatty acid peroxidation. Arch Biochem Biophys 125:189–198

    Article  CAS  PubMed  Google Scholar 

  • Hissin PJ, Hilf R (1976) A fluorimetric method for determination of oxidized and reduced glutathione in tissues. Anal Biochem 74:214–226

    Article  CAS  PubMed  Google Scholar 

  • Imsande J, Touraine B (1994) Demand and the regulation of nitrate uptake. Plant Physiol 105:3–7

    PubMed Central  CAS  PubMed  Google Scholar 

  • Jiang M, Zhang J (2001) Effect of abscisic acid on active oxygen species, antioxidative defence system and oxidative damage in leaves of maize seedlings. Plant Cell Physiol 42:1265–1273

    Article  CAS  PubMed  Google Scholar 

  • Keller T, Schwager H (1977) Air pollution and ascorbic acid. Eur J Forest Pathol 7:338–350

    Article  CAS  Google Scholar 

  • Lichtenthaler HK, Wellburn AR (1983) Determinations of total carotenoids and chlorophylls a and b of leaf extracts in different solvents. Biochem Soc Trans 11:591–592

    CAS  Google Scholar 

  • Lopez-Bucio J, Cruz-Ramírez A, Herrera-Estrella L (2003) The role of nutrient availability in regulating root architecture. Curr Opin Plant Biol 6:280–287

    Article  CAS  PubMed  Google Scholar 

  • Lowry OH, Rosebrough NJ, Farr AL, Randall RJ (1951) Protein measurements with Folin-phenol reagent. J Biol Chem 193:265–275

    CAS  PubMed  Google Scholar 

  • Lui H, Zhang J, Christie P, Zhang F (2008) Influence of iron plaque on uptake and accumulation of Cd by rice (Oryza sativa L.) seedling grown in soil. Sci Total Environ 394:361–368

    Article  Google Scholar 

  • Luo Y, Tang H, Zhang Y (2011) Production of reactive oxygen species and antioxidant metabolism about strawberry leaves to low temperatures. J Agric Sci 3:89–96

    Google Scholar 

  • Lux A, Martinka M, Vaculik M, White PJ (2011) Root responses to cadmium in the rhizosphere: a review. J Exp Bot 62:21–37

    Article  CAS  PubMed  Google Scholar 

  • Merchant S (2006) Trace metal utilization in chloroplasts. In: Wise RR, Hoober JK (eds) The structure and function of plastids. Springer, Dordrecht, pp 199–218

    Chapter  Google Scholar 

  • Muller P, Li X, Niyogi KK (2001) Non-photochemical quenching. A response to excess light energy. Plant Physiol 125:1558–1566

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Murata Y, Pei ZM, Mori IC, Schroeder J (2001) Abscisic acid acti-vation of plasma membrane Ca2+channels in guard cells requires cytosolic NAD(P)H and is differentially disrupted upstream and downstream of reactive oxygen species production in abi1–1 and abi2–1 protein phosphatase 2C mutants. Plant Cell 13:2513–2552

    PubMed Central  CAS  PubMed  Google Scholar 

  • Ohnishi N, Allakhverdiev SI, Takahashi S, Higashi S, Watanabe M, Nishiyama Y, Murata N (2005) Two-step mechanism of photodamage to photosystem II: step 1 occurs at the oxygen-evolving complex and step 2 occurs at the photochemical reaction center. Biochemistry 44:8494–8499

    Article  CAS  PubMed  Google Scholar 

  • Ololade IA, Ologundudu A (2007) Concentration and bioavailability of cadmium by some plants. Afr J Biotech 6:1916–1921

    CAS  Google Scholar 

  • Padmaja M, Sravanthi M, Hemalatha KPJ (2011) Evaluation of antioxidant activity of two Indian medicinal plants. J Phytol 3:86–91

    CAS  Google Scholar 

  • Pandey N, Singh GK (2012) Studies on antioxidative enzymes induced by cadmium in pea plants (Pisum sativum). J Environ Biol 33:201–206

    CAS  PubMed  Google Scholar 

  • Prasad MNV (1995) Cadmium toxicity and tolerance in vascular plants. Environ Exp Bot 35:525–545

    Article  CAS  Google Scholar 

  • Reugsegger A, Schmutz D, Brunold C (1992) Effect of cadmium on γ glutamylcysteine synthesis in maize seedlings. Plant Physiol 99:428–433

    Article  Google Scholar 

  • Rochaix JD (2011) Assembly of the photosynthetic apparatus. Plant Physiol 155:1493–1500

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Sandalio LM, Dalruzo HC, Gomez M, Romero-Puetras MC, del-Ri LA (2001) Cadmium-induced changes in the growth and oxidative metabolism of pea plants. J Exp Bot 52:2115–2126

    CAS  PubMed  Google Scholar 

  • Sanita di Toppi L, Gabbrielli R (1999) Response to cadmium in higher plants. Environ Exp Bot 41:105–130

    Article  Google Scholar 

  • Sebastian A, Prasad MNV (2014a) Red and blue lights induced oxidative stress tolerance promote cadmium rhizocomplexationin Oryza sativa. J Photochem Photobiol B Biol 137:135–143

    Article  CAS  Google Scholar 

  • Sebastian A, Prasad MNV (2014b) Cadmium minimization in rice. A review. Agron Sus Dev 34:155–173

    Article  CAS  Google Scholar 

  • Silva IR, Smyth TJ, Moxley DF, Carter TE, Allen NS, Rufty TW (2000) Aluminum accumulation at nuclei of cells in the root tip. Fluorescence detection using lumogallion and confocal laser scanning microscopy. Plant Physiol 123:543–552

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Stirbet A, Govindjee (2011) On the relation between the Kautsky effect (chlorophyll a fluorescence induction) and photosystem II: basics and applications. J Photochem Photobiol B Biol 104:236–257

    Article  CAS  Google Scholar 

  • Strasser RJ, Tsimilli-Michael M, Srivastava A (2004) Analysis of the chlorophyll fluorescence transient. In: Papageorgiou GC, Govindjee (eds) Chlorophyll fluorescence: a signature of photosynthesis. Advances in photosynthesis and respiration, vol 19. Springer, Dordrecht, pp 321–362

    Chapter  Google Scholar 

  • Uraguchi S, Kiyono M, Sakamoto T, Watanabe I, Kuno K (2009) Contributions of apoplasmic cadmium accumulation, antioxidative enzymes and induction of phytochelatins in cadmium tolerance of the cadmium-accumulating cultivar of black oat (Avena strigosa Schreb.). Planta 230:267–276

    Article  CAS  PubMed  Google Scholar 

  • Xiong J, Lu H, Lu K, Duan Y, An L, Zhu C (2009) Cadmium decreases crown root number by decreasing endogenous nitric oxide which is indispensable for crown root primordia initiation in rice seedlings. Planta 230:599–610

    Article  CAS  PubMed  Google Scholar 

  • Zou J, Yue J, Jiang W, Liu D (2012) Effects of cadmium stress on root tip cells and some physiological indexes in Allium cepa var. agrogarum L. Acta Biol Cracov Bot 54:129–141

    Google Scholar 

Download references

Acknowledgements

Authors acknowledge help received from Central Instrument Laboratory and School of Physics; University of Hyderabad for confocal laser scanning microscopy and scanning electron microscopic analysis, respectively. Abin Sebastian pleased to acknowledge senior research fellowship award received through CSIR-UGC NET.

Author information

Authors and Affiliations

  1. Department of Plant Sciences, University of Hyderabad, Hyderabad, 500046, Telangana, India

    Abin Sebastian & M. N. V. Prasad

Authors
  1. Abin Sebastian
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. M. N. V. Prasad
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to M. N. V. Prasad.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Sebastian, A., Prasad, M.N.V. Iron- and manganese-assisted cadmium tolerance in Oryza sativa L.: lowering of rhizotoxicity next to functional photosynthesis. Planta 241, 1519–1528 (2015). https://doi.org/10.1007/s00425-015-2276-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00425-015-2276-6

Keywords

Search

Navigation