Skip to main content
SpringerLink
Log in

Evaluation of heme oxygenase 1 (HO 1) in Cd and Ni induced cytotoxicity and crosstalk with ROS quenching enzymes in two to four leaf stage seedlings of Vigna radiata

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

Abstract

Research on heme oxygenase in plants has received consideration in recent years due to its several roles in development, defense, and metabolism during various environmental stresses. In the current investigation, the role of heme oxygenase (HO) 1 was evaluated in reducing heavy metal (Cd and Ni) uptake and alleviating Cd and Ni toxicity effects in the hydroponically grown seedlings of Vigna radiata var. PDM 54. Seedlings were subjected to Cd- and Ni-induced oxidative stress independently at different concentrations ranging from 10 to 100 μM. After 96 h (fourth day) of treatment, the stressed plants were harvested to study the cellular homeostasis and detoxification mechanism by examining the growth, stress parameters (LPX, H2O2 content), and non-enzymatic and enzymatic parameters (ascorbate peroxidase (APX), guaicol peroxidase (GPX), and catalase (CAT)) including HO 1. At 50 μM CdCl2 and 60 μM NiSO4, HO 1 activity was found to be highest in leaves which were 1.39 and 1.16-fold, respectively. The greatest HO 1 activity was reflected from the reduction of H2O2 content at these metal concentrations (50 μM CdCl2 and 60 μM NiSO4) which is correlated with the increasing activity of other antioxidant enzymes (CAT, APX). Thus, HO 1 works within a group that generates the defense machinery for the plant’s survival by scavenging ROS which is confirmed by a time-dependent study. Hence, it is concluded that seedlings of V. radiata were more tolerant towards metal-induced oxidative stress in which HO 1 is localized in its residential area (plastids).

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
Fig. 6
Fig. 7

Similar content being viewed by others

Abbreviations

ROS:

Reactive oxygen species

CAT:

Catalase

APX:

Ascorbate peroxidase

GPX:

Guaicol peroxidase

SOD:

Superoxide dismutase

NPT:

Non-protein thiol

CSI:

Chlorophyll stability index

HO 1:

Heme oxygenase 1

H2O2 :

Hydrogen peroxide

MDA:

Malondialdehyde

DTNB:

5,5′-Dithiobis-(2-nitrobenzoic acid)

References

  • Aebi H (1974) Catalases. In: Bergmeyer HU (ed) Methods of enzymatic analysis, Verlag Chemie, Weinheim. Academic Press Inc, New York, p 680

  • Ahmad P, Sarwat M, Sharma S (2008) Reactive oxygen species, antioxidants and signaling in plants. J Plant Biol 51:167–173

    Article  CAS  Google Scholar 

  • Alexieva V, Sergiev I, Mapelli S, Karanov E (2001) The effect of drought and ultraviolet radiation on growth and stress markers in pea and wheat. Plant Cell Environ 24:1337–1344

    Article  CAS  Google Scholar 

  • Alscher RG, Erturk N, Heath LS (2002) Role of superoxide dismutases [SODs] in controlling oxidative stress in plants. J Exp Bot 53:1331–1341

    Article  CAS  PubMed  Google Scholar 

  • Anderson ME (1985) Determination of glutathione and glutathione disulfides in biological samples. Methods Enzymol 113:548–570

    Article  CAS  PubMed  Google Scholar 

  • Arnon DI (1949) Copper enzymes in isolated chloroplasts: polyphenol oxidases in Beta vulgaris. Plant Physiol 24:1–15

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Arvind P, Prasad MNV (2003) Modulation of cadmium-induced oxidative stress in Ceratophyllum demersum by zinc involves ascorbate–glutathione cycle and glutathione metabolism. Plant Physiol Biochem 43:107–116

    Article  Google Scholar 

  • Bains K, Yang R, Shanmugasundaram S (2003) High iron mung bean recipes for North India, Shanhua, Taiwan. AVRDC Publication 562:34

    Google Scholar 

  • Balestrasse KB, Noriega GO, Batlle A, Tomaro ML (2005) Involvement of heme oxygenase as antioxidant defense in soybean nodules. Free Radic Res 39:145–151

    Article  CAS  PubMed  Google Scholar 

  • Balestrasse KB, Yannarelli GG, Noriega GO, Batlle A, Tomaro ML (2008) Heme oxygenase and catalase gene expression in nodules and roots of soybean plants subjected to cadmium stress. Biometals 21:433–441

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Bates SS, Tessier A, Campbell PGC, Buffle J (1982) Zinc adsorption and transport by Chlamydomonas variabilis and Scenedesmus subspicatus [Chlorophyceae] grown in semicontinuous culture. J Phycol 18:521–529

    Article  CAS  Google Scholar 

  • Cao XY, Xuan W, Liu ZY, Li XN, Zhao N, Xu P, Wang Z, Guan RZ, Shen WB (2007) Carbon monoxide promotes lateral root formation in rapeseed. J Integr Plant Biol 49:1070–1079

    Article  CAS  Google Scholar 

  • Cao Z, Geng B, Xu S, Xuan W, Nie L, Shen W, Liang Y, Guan R (2011) BnHO 1, a haem oxygenase-1 gene from Brassica napus, is required for salinity and osmotic stress-induced lateral root formation. J Exp Bot 62:4675–4689

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cataldo DA, Garland R, Wildung RE (1983) Cadmium uptake kinetics in intact soybean plants. Plant Physiol 73:844–848

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chen GX, Asada K (1989) Ascorbate peroxidase in tea leaves: occurrence of two isozymes and the differences in their enzymatic and molecular properties. Plant Cell Physiol 30:987–998

    Article  CAS  Google Scholar 

  • Chen XY, Ding X, Xu S, Wang R, Xuan W, Cao ZY, Chen J, Wu HH, Ye MB, Shen WB (2009) Endogenous hydrogen peroxide plays a positive role in the upregulation of hemeoxygenase and acclimation to oxidative stress in wheat seedling leaves. J Int Plant Biol 51:951–960

    Article  CAS  Google Scholar 

  • Collard JM, Corbisier P, Diels L, Dong Q, Jeanthon C, Mergeay M, Taghavi S, Van der Lelie D, Wilmotte A, Wuertz S (1994) Plasmids for heavy metal resistance in Alcaligenes eutrophus CH34: mechanisms and applications. FEMS Microbiol Rev 14:405–414

    Article  CAS  PubMed  Google Scholar 

  • Cornejo J, Willows RD, Beale SI (1998) Phytobilin biosynthesis: cloning and expression of a gene encoding soluble ferredoxin-dependent heme oxygenase from Synechocystis sp. PCC 6803. Plant J 15:99–107

    Article  CAS  PubMed  Google Scholar 

  • Cui W, Fu G, Wu H, Shen W (2011) Cadmium-induced heme oxygenase-1 gene expression is associated with the depletion of glutathione in the roots of Medicago sativa. Biometals 24:93–103

    Article  CAS  PubMed  Google Scholar 

  • Cui W, Gao C, Fang P, Lin G, Shen W (2013) Alleviation of cadmium toxicity in Medicago sativa by hydrogen-rich water. J Hazard Mater 260:715–724

    Article  CAS  PubMed  Google Scholar 

  • Daud MK, Sun YQ, Dawood M (2009) Cadmium-induced functional and ultrastructural alterations in roots of two transgenic cotton cultivars. J Hazard Mater 161:463–473

    Article  CAS  PubMed  Google Scholar 

  • Davis SJ, Bhoo SH, Durski AM, Walker JM, Vierstra RD (2001) The heme-oxygenase family required for phytochrome chromophore biosynthesis is necessary for proper photomorphogenesis in higher plants. Plant Physiol 126:656–669

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • De Vos CHR, Schat H, Vooijs R, Ernst WHO (1989) Copper-induced damage to the permeability barrier in roots of silene cuiubalus. J Plant Physiol 135:164–179

    Article  Google Scholar 

  • Demirevska-Kepova K, Simova-Stoilova L, Stoyanova Z, Holzer L, Feller U (2004) Biochemical changes in barley plants after excessive supply of copper and manganese. Environ Exp Bot 52:253–266

    Article  CAS  Google Scholar 

  • Dixit S, Verma K, Shekhawat GS (2014) In vitro evaluation of mitochondrial–chloroplast subcellular localization of heme oxygenase1 [HO 1] in Glycine max. Protoplasma 251:671–675

    Article  CAS  PubMed  Google Scholar 

  • Duarte B, Delgado M, Cacador I (2007) The role of citric acid in cadmium and nickel uptake and translocation, in Halimione portulacoides. Chemosphere 69:836–840

    Article  CAS  PubMed  Google Scholar 

  • Emborg TJ, Walker JM, Noh B, Vierstra RD (2006) Multiple heme oxygenase family members contribute to the biosynthesis of the phytochrome chromophore in Arabidopsis. Plant Physiol 140:856–868

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ermler U, Grabarse W, Shima S, Goubeaud M, Thauer RK (1998) Active sites of transition-metal enzymes with a focus on nickel. Curr Opin Struct Biol 8:749–758

    Article  CAS  PubMed  Google Scholar 

  • Ferreira RR, Fornazier RF, Vitoria AP, Lea PJ, Azevedo RA (2002) Changes in antioxidant enzyme activities in soybean under cadmium stress. J Plant Nutr 25:327–342

    Article  CAS  Google Scholar 

  • Foyer CH, Lelandais M, Kunert KJ (1994) Photooxidative stress in plants. Physiol Plant 92:696–717

    Article  CAS  Google Scholar 

  • Fu GQ, Xu S, Xie YJ, Han B, Nie L, Shen WB, Wang R (2011) Molecular cloning, characterization, and expression of an alfalfa [Medicago sativa L.] heme oxygenase-1 gene, MsHO1, which is prooxidants regulated. Plant Physiol Biochem 49:792–799

    Article  CAS  PubMed  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 

  • Gill SS, Khan NA, Tuteja N (2011) Differential cadmium stress tolerance in five Indian mustard [Brassica juncea L.] cultivars: an evaluation of the role of antioxidant machinery. Plant Signal Behav 6:293–300

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gill SS, Khan NA, Tuteja N (2012) Cadmium at high dose perturbs growth, photosynthesis and nitrogen metabolism while at low dose it up regulates sulfur assimilation and antioxidant machinery in garden cress [Lepidium sativum L.] Plant Sci 182:112–120

    Article  CAS  PubMed  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 

  • Hsu YT, Kao CH (2004) Cadmium toxicity is reduced by nitric oxide in rice leaves. Plant Growth Regul 42:227–238

    Article  CAS  Google Scholar 

  • Hu J, Deng Z, Wang B, Zhi Y, Pei B, Zhang G, Luo M, Huang B, Wu W, Huang B (2015) Influence of heavy metals on seed germination and early seedling growth in Crambe abyssinica, a potential industrial oil crop for phytoremediation. Am J Plant Sci 6:150–156

    Article  Google Scholar 

  • Kupper H, Kroneck PMH (2007) Nickel in the environment and its role in metabolism of plants and cyanobacteria. Met Ions Life Sci 2:31–62

    Google Scholar 

  • Laloi CH, Apel K, Danon A (2004) Reactive oxygen signaling: the latest news. Curr Opin Plant Biol 7:323–328

    Article  CAS  PubMed  Google Scholar 

  • Li Q, Zhu F, Gao X, Sun Y, Li S, Tao Y, Lo C, Liu H (2014) Young leaf chlorosis 2 encodes the stroma-localized heme oxygenase 2 which is required for normal tetrapyrrole biosynthesis in rice. Planta 240:701–712

    Article  CAS  PubMed  Google Scholar 

  • Li J, Zhu D, Wang R, Shen W, Guo Y, Ren Y, Shen W, Huang L (2015) β-Cyclodextrin–hemin complex-induced lateral root formation in tomato: involvement of nitric oxide and heme oxygenase 1. Plant Cell Rep 34:381–393

    Article  CAS  PubMed  Google Scholar 

  • Linley PJ, Landsberger M, Kohchi T, Cooper JB, Terry MJ (2006) The molecular basis of heme oxygenase deficiency in the pcd1 mutant of pea. FEBS J 273:2594–2606

    Article  CAS  PubMed  Google Scholar 

  • Liu D, Zou J, Meng Q, Zou J, Wusheng J (2009) Uptake and accumulation and oxidative stress in garlic [Allium sativum L.] under lead phytotoxicity. Ecotoxicology 18:134–143

    Article  CAS  PubMed  Google Scholar 

  • Lowry OH, Rosenberg NJ, Farr AL, Randall RJ (1951) Protein measurement with folin phenol reagent. J Biol Chem 193:265–275

    CAS  PubMed  Google Scholar 

  • Maier T, Jacobi A, Sauter M, Bock A (1993) The product of the hypb gene, which is required for nickel incorporation into hydrogenases, is a novel guanine nucleotide-binding protein. J Bacteriol 175:630–635

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Maines MD (1988) Heme oxygenase: function, multiplicity, regulatory mechanism and clinical applications. FASEB J 2:2557–2568

    Article  CAS  PubMed  Google Scholar 

  • Mehrag AA (1994) Integrated tolerance mechanisms: constitutive and adaptive plant responses to elevated metal concentrations in the environment. Plant Cell Environ 17:989–993

    Article  Google Scholar 

  • Mulrooney SB, Hausinger RP (2003) Nickel uptake and utilization by microorganisms. FEMS Microbiol Rev 27:239–261

    Article  CAS  PubMed  Google Scholar 

  • Muramoto T, Kohchi T, Yokota A, Hwang I, Goodman HM (1999) The Arabidopsis photomorphogenic mutant hy1 is deficient in phytochrome chromophore biosynthesis as a result of a mutation in a plastid heme oxygenase. Plant Cell 11:335–348

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mwegoha WJS, Kihampa C (2010) Heavy metal contamination in agricultural soils and water in Dares Salaam city, Tanzania. Afr J Environ Sci Technol 4:763–769

    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 

  • Noctor G, Foyer CH (1998) Ascorbate and glutathione: keeping active oxygen under control. Annu Rev Plant Physiol Plant Mol Biol 49:249–279

    Article  CAS  PubMed  Google Scholar 

  • Noriega G, Cruz DS, Batlle A, Tomaro M, Balestrasse K (2012) Heme Oxygenase is involved in the protection exerted by jasmonic acid against cadmium stress in soybean roots. J Plant Growth Regul 31:79–89

    Article  CAS  Google Scholar 

  • Ona LF, Alberto AM, Prudente JA, Sigua GC (2006) Levels of lead in urban soils from selected cities in a central region of the Philippines. Environ Sci Pollut Res 13:177–183

    Article  CAS  Google Scholar 

  • Otterbein LE, Soares MP, Yamashita K, Bach FH (2003) Heme oxygenase-1: unleashing the protective properties of heme. Trends Immunol 24:449–455

    Article  CAS  PubMed  Google Scholar 

  • Pietrini F, Iannelli MA, Pasqualini S, Massacci A (2003) Interaction of cadmium with glutathione and photosynthesis in developing leaves and chloroplasts of Phragmites australis [Cav.] Trin ex Steudel. Plant Physiol 133:829–837

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Putter J (1974) Peroxidase. In: Bergemeyer HU (ed) Methods of enzymatic analysis. Academic Press, London, pp 685–690

    Chapter  Google Scholar 

  • Ragsdale SW (1998) Nickel biochemistry. Curr Opin Chem Biol 2:208–215

    Article  CAS  PubMed  Google Scholar 

  • Reinheckel T, Noack H, Lorenz S, Wissedel I, Augustin W (1998) Comparison of protein oxidation and aldehyde formation during oxidative stress in isolated mitochondria. Free Radic Res 29:297–305

    Article  CAS  PubMed  Google Scholar 

  • Romero-Puertas MC, Palma JM, Gomez M, Del Rio LA, Sandalio LM (2002) Cadmium causes the oxidative modification of proteins in pea plants. Plant Cell Environ 25:677–686

    Article  CAS  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

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

    Article  Google Scholar 

  • Santa-Cruz D, Pacienza N, Zilli C, Pagano E, Balestrasse K, Yannarelli G (2017) Heme oxygenase up-regulation under ultraviolet-B radiation is not epigenetically restricted and involves specific stress-related transcriptions factors. Redox Biol 12:549–557

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schutzendubel A, Polle A (2002) Cadmium and H2O2 induced oxidative stress in Populus canecens roots. Plant Physiol Biochem 40:577–584

    Article  CAS  Google Scholar 

  • Schutzendubel A, Schwanz P, Teichmann T, Gross K, Lanhenfeld-Heyser R, Godbold DL, Polle A (2001) Cadmium induced changes in antioxidative system, hydrogen peroxide content and differentiation in scots pine roots. Plant Physiol 127:887–898

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sedlak J, Lindsay RH (1968) Estimation of total, protein-bound and non protein sulphydryl groups in tissue with Ellman’s reagent. Anal Biochem 25:192–205

    Article  CAS  PubMed  Google Scholar 

  • Sethy SK, Ghosh S (2013) Effect of heavy metals on germination of seeds. J Nat Sci Biol Med 4:272–275

    Article  PubMed  PubMed Central  Google Scholar 

  • Sharma SS, Dietz KJ (2009) The relationship between metal toxicity and cellular redox imbalance. Trends Plant Sci 14:43–50

    Article  CAS  PubMed  Google Scholar 

  • Shekhawat GS, Verma K (2010) Heme oxygenase [HO]: an overlooked enzyme of plant metabolism and defence. J Exp Bot 61:2255–2270

    Article  CAS  PubMed  Google Scholar 

  • Shekhawat GS, Prasad A, Verma K, Sharma A (2008) Changes in growth, lipid peroxidation and antioxidant system in seedlings of Brassica juncea (L.) czern. Biochem Cell Arch 8:145–149

  • Shekhawat GS, Verma K, Jana S, Singh K, Teotia P, Prasad A (2009) In vitro biochemical evaluation of cadmium tolerance mechanism in callus and seedlings of Brassica juncea. Protoplasma 239:31–38

    Article  Google Scholar 

  • Shekhawat GS, Dixit S, Verma K, Nasybullina EI, Kosmachevskaya OV, Topunov AF (2011) Heme oxygenase: enzyme with functional diversity. J Stress Physiol Biochem 7:88–94

    Google Scholar 

  • Siddiqui MH, Al-Whaibi MH, Basalah MO (2011) Interactive effect of calcium and gibberellin on nickel tolerance in relation to antioxidant systems in Triticum aestivum L. Protoplasma 248:503–511

    Article  CAS  PubMed  Google Scholar 

  • Sidlecka A, Baszynsky T (1993) Inhibition of electron flow around photosystem I in chloroplasts of cadmium-treated maize plants in due to cadmium-induced iron deficiency. Physiol Plant 87:199–202

    Article  Google Scholar 

  • Siripornadulsil S, Traina S, Verma DPS, Sayre RT (2002) Molecular mechanisms of proline mediated tolerance to toxic heavy metals in transgenic micro algae. Plant Cell 14:2837–2847

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Skórzynska-Polit E, Pawlikowska-Pawlega B, Szczuka E, Drazkiewicz M, Krupa Z (2006) The activity and localization of lipoxygenases in Arabidopsis thaliana under cadmium and copper stress. Plant Growth Regul 48:29–39

    Article  Google Scholar 

  • Smirnoff N (1998) Plant resistance to environmental stress. Curr Opin Biotechnol 9:214–219

    Article  CAS  PubMed  Google Scholar 

  • Somashekaraiah BV, Padmaja K, Prasad ARK (1992) Phytotoxicity of cadmium ions on germinating seedlings of mung bean [Phaseolus vulgaris]: involvement of lipid peroxides in chlorophyll degradation. Physiol Plantarum 85:85–89

    Article  CAS  Google Scholar 

  • Stoltz E, Greger M (2002) Accumulation properties of As, Cd, Cu, Pb and Zn by four wetland plant species growing on submerged mine tailings. Environ Exp Bot 47:271–280

    Article  CAS  Google Scholar 

  • Tausz M, Sircelji H, Grill D (2004) The glutathione system as a stress marker in plant ecophysiology: is a stress response concept valid. J Exp Bot 55:1955–1962

    Article  CAS  PubMed  Google Scholar 

  • Tenhunen R, Marver HS, Schmid R (1968) The enzymatic conversion of heme to bilirubin by microsomal heme oxygenase. PNAS 61:748–755

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Terry MJ, Kendrick RE (1999) Feedback inhibition of chlorophyll synthesis in the phytochrome chromophore-deficient aurea and yellow-greeen-2 mutants of tomato. Plant Physiol 119:143–152

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Terry MJ, Ryberg M, Raitt CE, Page A (2001) Altered etioplast development in phytochrome chromophore-deficient mutants. Planta 214:314–325

    Article  CAS  PubMed  Google Scholar 

  • Tomaro ML, Batlle A (2002) Bilirubin: its role in cytoprotection against oxidative stress. Int J Biochem Cell Biol 34:216–220

    Article  CAS  PubMed  Google Scholar 

  • Tripathi BN, Mehta SK, Gaur JP (2004) Recovery of uptake and assimilation of nitrate in Scendesmus sp. previously exposed to elevated leaves of Cu+2 and Zn+2. J Plant Physiol 161:543–549

    Article  CAS  PubMed  Google Scholar 

  • Tripathi BN, Singh V, Ezaki B, Sharma V, Gaur JP (2013) Mechanism of Cu and Cd induced proline hyperaccumulation in Triticum aestivum [wheat]. J Plant Growth Regul 32:799–808

    Article  CAS  Google Scholar 

  • Verma K, Shekhawat GS, Sharma A, Mehta SK, Sharma V (2008) Cadmium induced oxidative stress and changes in soluble and ionically bound cell wall peroxidase activities in roots of seedling and 3–4 leaf stage plants of Brassica juncea [L.] Czern. Plant Cell Rep 27:1261–1269

    Article  CAS  PubMed  Google Scholar 

  • Verma K, Mehta SK, Shekhawat GS (2013) Nitric oxide [NO] counteracts cadmium induced cytotoxic processes mediated by reactive oxygen species [ROS] in Brassica juncea: cross-talk between ROS, NO and antioxidant responses. Biometals 26:255–269

    Article  CAS  PubMed  Google Scholar 

  • Vranova E, Inze D, Breusegem FV (2002) Signal transduction during oxidative stress. J Exp Bot 53:1227–1236

    Article  CAS  PubMed  Google Scholar 

  • Wilkins DA (1978) The measurement of tolerance to edaphic factors by means of root growth. New Phytol 80:623–633

    Article  CAS  Google Scholar 

  • Xie Y, Mao Y, Xu S, Zhou H, Duan X, Cui W, Zhang J, Xu G (2015) Heme-heme oxygenase 1 system is involved in ammonium tolerance by regulating antioxidant defence in Oryza sativa. Plant Cell Environ 38:129–143

    Article  CAS  PubMed  Google Scholar 

  • Xu S, Zhang B, Cao ZY, Ling TF, Shen WB (2011) Heme oxygenase is involved in cobalt chloride-induced lateral root development in tomato. Biometals 24:181–191

    Article  CAS  PubMed  Google Scholar 

  • Yannarelli GG, Noriega GO, Batlle A, Tomaro ML (2006) Heme oxygenase up regulation in ultraviolet-B irradiated soybean plants involves reactive oxygen species. Planta 224:1154–1162

    Article  CAS  PubMed  Google Scholar 

  • Zayed A, Gowthaman S, Terry N (1998) Phytoaccumulation of trace elements by wetlands plants: I. Duckweed J Environ Qual 27:715–721

    Article  CAS  Google Scholar 

  • Zhang YY, Liu J, Liu YL (2004) Nitric oxide alleviates the growth inhibition of maize seedlings under salt stress. J Plant Physiol Mol Biol 30:455–459

    CAS  Google Scholar 

  • Zhu L, Yang Z, Zeng X, Gao J, Liu J, Yi B, Ma C, Shen J, Tu J, Fu T, Wen J (2017) Heme oxygenase 1 defects lead to reduced chlorophyll in Brassica napus. Plant Mol Biol 93:579–592

    Article  CAS  PubMed  Google Scholar 

  • Zilli CG, Santa-Cruz DM, Yannarelli CG, Noriega GO, Tomaro ML, Balestrasse KB (2009) Heme oxygenase contributes to alleviate salinity damage in Glycine max L. leaves. Int J Cell Bio 1–9. https://doi.org/10.1155/2009/848516

Download references

Acknowledgements

We gratefully acknowledge University Grants Commission, New Delhi, for providing financial assistance through Centre for Advanced Study program.

Author information

Authors and Affiliations

  1. Department of Botany, Jai Narain Vyas University, Jodhpur, Rajasthan, 342001, India

    Lovely Mahawar & Gyan Singh Shekhawat

  2. Water Quality Management Group Defense Laboratory, Jodhpur, 342001, India

    Rajesh Kumar

Authors
  1. Lovely Mahawar
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Rajesh Kumar
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Gyan Singh Shekhawat
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Gyan Singh Shekhawat.

Additional information

Handling Editor: Bhumi Nath Tripathi

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Mahawar, L., Kumar, R. & Shekhawat, G.S. Evaluation of heme oxygenase 1 (HO 1) in Cd and Ni induced cytotoxicity and crosstalk with ROS quenching enzymes in two to four leaf stage seedlings of Vigna radiata . Protoplasma 255, 527–545 (2018). https://doi.org/10.1007/s00709-017-1166-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00709-017-1166-0

Keywords

Search

Navigation