Issue
Effect of cobalt nanoparticles and cobalt ions on alkaloids production and expression of CrMPK3 gene in Catharanthus roseus suspension cultures
Corresponding Author(s) : Ahmed Sayed Fouad
Cellular and Molecular Biology,
Vol. 64 No. 12: Issue 12
Abstract
The capabilities of cobalt ions (Co2+) and cobalt nanoparticles (CoNPs) in enhancing alkaloids accumulation in Catharanthus roseus suspension cultures were evaluated in relation to the expression of CrMPK3 gene. Four concentrations (5, 10, 15 and 20 mg/L) of each cobalt form were utilized in addition to control. Both forms induced oxidative stress that was more pronounced for Co2+ treatments. A positive correlation was observed between cobalt concentration and expression of CrMPK3 gene. However, a characteristic temporal expression profile was recorded for each cobalt form. Also, positive correlations were detected between both cobalt concentration and expression of CrMPK3 gene on one hand and the activities of antioxidant enzymes (SOD and APX) and alkaloids content on the other hand. Such correlations suggest CrMPK3 gene as a common player in cobalt-induced stress signaling; regardless of cobalt form. Results revealed the higher capability of Co2+, compared with CoNPs, in enhancing alkaloids accumulation. However, results supported CoNPs as a novel tool in manipulating cobalt-induced alkaloids production in C. roseus.
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Endnote/Zotero/Mendeley (RIS)BibTeX
- - Matsuura, HN. and Fett-Neto, AG. Plant alkaloids: main features, toxicity, and mechanisms of action. In: Plant Toxins. Gopalakrishnakone P., Carlini CR., Ligabue-Braun R. (ed.), Dordrecht: Springer, Netherlands 2017, pp. 243-261.
- _____________________________________________________________
- - Pan Q, Mustafa NR, Tang K, Choi YH, Verpoorte R. Monoterpenoid indole alkaloids biosynthesis and its regulation in Catharanthus roseus: a literature review from genes to metabolites. Phytochem Rev 2016; 15: 221–250.
- _____________________________________________________________
- - Zhu W, Yang B, Komatsu S, Lu X, Li X, Tian J. Binary stress induces an increase in indole alkaloid biosynthesis in Catharanthus roseus. Front Plant Sci 2015; 6: 582.
- ____________________________________________________________
- - Ghorbanpour M, Hatami M, Hatami M. Activating antioxidant enzymes, hyoscyamine and scopolamine biosynthesis of Hyoscyamus niger L. plants with nano-sized titanium dioxide and bulk application. Acta Agric Slov 2015; 105: 23–32.
- _____________________________________________________________
- - Van der Heijden R, Jacobs DI, Snoeijer W, Hallard D, Verpoorte R. The Catharanthus alkaloids: Pharmacognosy and biotechnology. Curr Med Chem 2004; 11: 1241–1253.
- _____________________________________________________________
- - Zhao J, Verpoorte R. Manipulating indole alkaloid production by Catharanthus roseus cell cultures in bioreactors: from biochemical processing to metabolic engineering. Phytochem Rev 2007; 6: 435–457.
- _____________________________________________________________
- - Zhao JL, Zhou LG, Wu JY. Effects of biotic and abiotic elicitors on cell growth and tanshinone accumulation in Salvia miltiorrhiza cell cultures. Appl Microbiol Biotechnol 2010; 87: 137–144.
- _____________________________________________________________
- - Hussain MS, Fareed S, Ansari S, Rahman MA, Ahmad IZ, Saeed M. Current approaches toward production of secondary plant metabolites. J Pharm Bioallied Sci 2012; 4: 10-20.
- _____________________________________________________________
- - Van der Heijden R, Verpoorte R, Ten Hoopen HJG. Cell and tissue cultures of Catharanthus roseus (L.) G. Don: A literature survey. Plant Cell Tissue Organ Cult 1989; 18: 231–280.
- _____________________________________________________________
- - Moreno PRH, van der Heijden R, Verpoorte R. Cell and tissue cultures of Catharanthus roseus: A literature survey. Plant Cell Tissue Organ Cult 1995; 42: 1–25.
- _____________________________________________________________
- - Mourato, M., Reis, R., Martins, LL. Characterization of plant antioxidative system in response to abiotic stresses: a focus on heavy metal toxicity: In Advances in Selected Plant Physiology Aspects. Montanaro G. and Dichio B. (ed.), InTech, Vienna, Austria, 2012.
- _____________________________________________________________
- - Sharma, SS, Dietz, KJ. The relationship between metal toxicity and cellular redox imbalance. Trends Plant Sci. 2009; 14: 43-50.
- _____________________________________________________________
- - Selmar D, Kleinwächter M. Stress enhances the synthesis of secondary plant products: The impact of stress-related over-reduction on the accumulation of natural products. Plant Cell Physiol 2013; 54: 817-826.
- _____________________________________________________________
- - Zheng Z, Wu M. Cadmium treatment enhances the production of alkaloid secondary metabolites of Catharanthus roseus. Plant Sci 2004; 166: 507-14.
- _____________________________________________________________
- - Srivastava NK, Srivastava AK. Influence of some heavy metals on growth, alkaloid content and composition in Catharanthus roseus L. Indian J Pharm Sci 2010; 72: 775-778.
- _____________________________________________________________
- - Fathalla MA, Abd-El Kawy AM, Taha HS. Effect of heavy metal (HgCl2) on accumulation and production of total indole alkaloids, vinblastine and/or vincristine from Egyptian Catharanthus Roseus (L.) G. Don. calli cultures. J Appl Sci Res 2011; 7: 542-549.
- _____________________________________________________________
- - Rai V, Tandon PK, Khatoon S. Effect of chromium on antioxidant potential of Catharanthus roseus varieties and production of their anticancer alkaloids: vincristine and vinblastine. Biomed Res Int 2014; 2014: 1-10.
- _____________________________________________________________
- - Reeves, RD. and Baker, AJM. Metal-accumulating plants. In: Phytoremediation of Toxic Metals: Using Plants to Clean Up the Environment. Raskin I., Ensley BD. (ed.), Wiley, New York, 2000, Pp. 193–229.
- _____________________________________________________________
- - Karuppanapandian T, Kim W. Cobalt-induced oxidative stress causes growth inhibition associated with enhanced lipid peroxidation and activates antioxidant responses in Indian mustard (Brassica juncea L.) leaves. Acta Physiol Plant 2013; 35: 2429–2443.
- _____________________________________________________________
- - Azarakhsh MR, Asrar Z, Mansouri H. Effects of seed and vegetative stage cysteine treatments on oxidative stress response molecules and enzymes in Ocimum basilicum L. under cobalt stress. J Soil Sci Plant Nutr 2015; 15: 651–662.
- _____________________________________________________________
- - Trejo-Tapia G, Jimenez-Aparicio A, Rodriguez-Monroy M, De Jesus-Sanchez A, Gutierrez-Lopez G. Influence of cobalt and other microelements on the production of betalains and the growth of suspension cultures of Beta vulgaris. Plant Cell Tissue Organ Cult 2001; 67: 19–23.
- _____________________________________________________________
- - Cai Z, Kastell A, Speiser C, Smetanska I. Enhanced resveratrol production in Vitis vinifera cell suspension cultures by heavy metals without loss of cell viability. Appl Biochem Biotechnol 2013; 171: 330-340.
- _____________________________________________________________
- - Urdová J, Rexová M, Mućaji P, Balažová A. Elicitation – a tool to improve secondary metabolites production in Melissa officinalis L. suspension cultures. Acta Fac Pharm Univ Comen 2015; 62: 46-50.
- _____________________________________________________________
- - Tammaru I. Effect of high cobalt rates on the accumulation of alkaloids in Datura stramonium. Tartu Ulikooli Toimetised 1980; 523: 65-70.
- _____________________________________________________________
- - Petrishek IA, Lovkova MY, Grinkevich NI, Orlova LP, Poludennyi LV. Effects of cobalt and copper on the accumulation of alkaloids in Atropa belladonna L. Biol Bull Acad Sci USSR 1984;10: 509-516.
- _____________________________________________________________
- - Taj G, Agarwal P, Grant M, Kumar A. MAPK machinery in plants: recognition and response to different stresses through multiple signal transduction pathways. Plant Signal Behav 2010; 5: 1370-1378.
- _____________________________________________________________
- - Raina SK, Wankhede DP, Jaggi M, Singh P, Jalmi SK, Raghuram B, Sheikh AH, Sinha AK. CrMPK3, a mitogen activated protein kinase from Catharanthus roseus and its possible role in stress induced biosynthesis of monoterpenoid indole alkaloids. BMC Plant Biol 2012; 12: 134.
- _____________________________________________________________
- - Pan YJ, Liu J, Guo XR, Zu YG, Tang ZH. Gene transcript profiles of the TIA biosynthetic pathway in response to ethylene and copper reveal their interactive role in modulating TIA biosynthesis in Catharanthus roseus. Protoplasma 2015; 252: 813-24.
- _____________________________________________________________
- - Schmid, G. Nanoparticles: From Theory to Application. Wiley, Weinheim 2010.
- _____________________________________________________________
- - Ghasemi B, Hosseini R, Nayeri FD. Effects of cobalt nanoparticles on artemisinin production and gene expression in Artemisia annua. Turk J Bot 2015; 39: 769-777.
- _____________________________________________________________
- - Murashige T, Skoog F. A revised medium for rapid growth and bioassay with tobacco tissue cultures. Plant Physiol 1962; 15: 473–497.
- _____________________________________________________________
- - Stewart RC, Bewley JD. Lipid peroxidation associated with accelerated aging of soybean axes. Plant Physiol 1980; 65: 245–248.
- _____________________________________________________________
- - Gong H, Chen G, Li F, Wang X, Hu Y, Bi Y. Involvement of G6PDH in heat stress tolerance in the calli from Przewalskia tangutica and Nicotiana tabacum . Biol Plant 2012; 56: 422–430.
- _____________________________________________________________
- - Beauchami C, Fridovich I. Superoxide dismutase: improved assays and an assay applicable to acrylamide gels. Anal Biochem 1971; 44: 276–287.
- _____________________________________________________________
- - Elkahouia S, Hernández JA, Abdellyc C, Ghrira R, Limama F. Effects of salt on lipid peroxidation and antioxidant enzyme activities of Catharanthus roseus suspension cells. Plant Sci 2005; 168: 607–613.
- _____________________________________________________________
- - Nakano Y, Asada K. Hydrogen peroxide is scavenged by ascorbate specific peroxidase in spinach chloroplasts. Plant Cell Physiol 1981; 22: 867-880
- _____________________________________________________________
- - Lowry OH, Rosebrough NJ, Farr AL, Randall RJ. Protein measurement with the folin phenol reagent. J biol Chem 1951; 193: 265–275.
- _____________________________________________________________
- - Lee SL, Cheng KD, Scott, AI. Effects of bioregulators on indole alkaloid biosynthesis in Catharanthus roseus cell culture. Phytochemistry 1981; 20: 1841–1843.
- _____________________________________________________________
- - George, EF., Puttock, DJM., George, HJ. Plant culture media (vol 2), Exegetics Co, Ltd., Westbury, 1988.
- _____________________________________________________________
- - Hilmy LM, Gad N. Effect of cobalt fertilization on the yield, quality and the essential oil composition of parsley leaves. Arab Univ J agr Sci 2002; 10: 803–829.
- _____________________________________________________________
- - Javed SB, Anis M. Cobalt induced augmentation of in vitro morphogenic potential in Erythrina variegata L.: a multipurpose tree legume. Plant Cell Tissue Organ Cult 2015; 120: 463–474.
- _____________________________________________________________
- - Sharma P, Jha AB, Dubey RS, Pessarakli M. Reactive oxygen species, oxidative damage, and antioxidative defense mechanism in plants under stressful conditions. J Bot 2012; doi:10.1155/2012/217037.
- _____________________________________________________________
- - Kovtun Y, Chiu WL, Tena G, Sheen J. Functional analysis of oxidative stress-activated mitogen-activated protein kinase cascade in plats. Proc nat Acad. Sci USA 2000; 97: 2940–2945.
- _____________________________________________________________
- - Jonak C, Nakagami H, Hirt H. Heavy metal stress. Activation of distinct mitogen-activated protein kinase pathways by copper and cadmium. Plant Physiol 2004; 136: 3276–3283.
- ____________________________________________________________ M, Hu X. Mitogen-activated protein kinase is involved in abscisic acid-induced antioxidant defense and acts downstream of reactive oxygen species production in leaves of maize plants. Plant Physiol 2006; 141: 475-487.
- _____________________________________________________________
- - Amarasinghe A. Effects of copper sulphate and cobalt chloride on in vitro performances of traditional indica rice (Oryza sativa L.) varieties in Sri Lanka. J agr Sci 2009; 4: 132-141.
- _____________________________________________________________
- - Shi BEN, Ni LAN, Liu Y, Zhang A, Tan M, Jiang M. OsDMI3-mediated activation of OsMPK1 regulates the activities of antioxidant enzymes in abscisic acid signalling in rice. Plant Cell Environ 2014; 37: 341–352.
- _____________________________________________________________
- - Gill SS, Tuteja N. Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiol and Biochem 2010; 48: 909–930.
- _____________________________________________________________
- - Tewari RK, Kumar P, Sharma PN, Bisht SS: Modulation of oxidative stress responsive enzymes by excess cobalt. Plant Sci 2002; 162: 381–388.
- _____________________________________________________________
- - Pandey N, Pathak GC, Pandey DK, Pandey R. Heavy metals, Co, Ni, Cu, Zn and Cd, produce oxidative damage and evoke differential antioxidant responses in spinach. Braz J Plant Physiol 2009; 21: 103-111.
- _____________________________________________________________
- - Sinha P, Nautiyal N. Excessive cobalt induced oxidative stress in groundnut. Indian J Plant Physiol 2012; 17: 71-74.
- _____________________________________________________________
- - Arora P, Bhardwaj R, Kanwar MK. Effect of 24-epibrassinolide on growth, protein content and antioxidative defense system of Brassica juncea L. subjected to cobalt ion toxicity. Acta Physiol Plant 2012; 34: 2007–2017.
- _____________________________________________________________
- - Liu Y, Meng Q, Duan X, Zhang Z, Li D. Effects of PEG-induced drought stress on regulation of indole alkaloid biosynthesis in Catharanthus roseus. J Plant Interact 2017; 12: 87–9.
- _____________________________________________________________
- - Pandey, SS, Singh, S, Babu, CSV, Shanker, K, Srivastava, NK, Shukla, AK, Kalra, A. Fungal endophytes of Catharanthus roseus enhance vindoline content by modulating structural and regulatory genes related to terpenoid indole alkaloid biosynthesis. Sci Rep 2016; 6: 26583.
- _____________________________________________________________
- - Faisal M, Saquib Q, Alatar AA, Al-Khedhairy AA, Ahmed M, Ansari SM, Praveen S. Cobalt oxide nanoparticles aggravate DNA damage and cell death in eggplant via mitochondrial swelling and NO signaling pathway. Biol Res 2016; 49: 20.
- _____________________________________________________________
- - Nymark P, Catalán J, Suhonen S, Järventaus H, Birkedal R, Clausen PA, Jensen KA, Vippola M, Savolainen K, Norppa H. Genotoxicity of polyvinylpyrrolidone coated silver nanoparticles in BEAS 2B cells. Toxicology 2013; 8: 38-48.
- _____________________________________________________________
- - Fouad, AS, Hafez, RM. The effects of silver ions and silver nanoparticles on cell division and expression of cdc2 gene in Allium cepa root tips.Biol Plant 2018; 62: 166-172.
References
- Matsuura, HN. and Fett-Neto, AG. Plant alkaloids: main features, toxicity, and mechanisms of action. In: Plant Toxins. Gopalakrishnakone P., Carlini CR., Ligabue-Braun R. (ed.), Dordrecht: Springer, Netherlands 2017, pp. 243-261.
_____________________________________________________________
- Pan Q, Mustafa NR, Tang K, Choi YH, Verpoorte R. Monoterpenoid indole alkaloids biosynthesis and its regulation in Catharanthus roseus: a literature review from genes to metabolites. Phytochem Rev 2016; 15: 221–250.
_____________________________________________________________
- Zhu W, Yang B, Komatsu S, Lu X, Li X, Tian J. Binary stress induces an increase in indole alkaloid biosynthesis in Catharanthus roseus. Front Plant Sci 2015; 6: 582.
____________________________________________________________
- Ghorbanpour M, Hatami M, Hatami M. Activating antioxidant enzymes, hyoscyamine and scopolamine biosynthesis of Hyoscyamus niger L. plants with nano-sized titanium dioxide and bulk application. Acta Agric Slov 2015; 105: 23–32.
_____________________________________________________________
- Van der Heijden R, Jacobs DI, Snoeijer W, Hallard D, Verpoorte R. The Catharanthus alkaloids: Pharmacognosy and biotechnology. Curr Med Chem 2004; 11: 1241–1253.
_____________________________________________________________
- Zhao J, Verpoorte R. Manipulating indole alkaloid production by Catharanthus roseus cell cultures in bioreactors: from biochemical processing to metabolic engineering. Phytochem Rev 2007; 6: 435–457.
_____________________________________________________________
- Zhao JL, Zhou LG, Wu JY. Effects of biotic and abiotic elicitors on cell growth and tanshinone accumulation in Salvia miltiorrhiza cell cultures. Appl Microbiol Biotechnol 2010; 87: 137–144.
_____________________________________________________________
- Hussain MS, Fareed S, Ansari S, Rahman MA, Ahmad IZ, Saeed M. Current approaches toward production of secondary plant metabolites. J Pharm Bioallied Sci 2012; 4: 10-20.
_____________________________________________________________
- Van der Heijden R, Verpoorte R, Ten Hoopen HJG. Cell and tissue cultures of Catharanthus roseus (L.) G. Don: A literature survey. Plant Cell Tissue Organ Cult 1989; 18: 231–280.
_____________________________________________________________
- Moreno PRH, van der Heijden R, Verpoorte R. Cell and tissue cultures of Catharanthus roseus: A literature survey. Plant Cell Tissue Organ Cult 1995; 42: 1–25.
_____________________________________________________________
- Mourato, M., Reis, R., Martins, LL. Characterization of plant antioxidative system in response to abiotic stresses: a focus on heavy metal toxicity: In Advances in Selected Plant Physiology Aspects. Montanaro G. and Dichio B. (ed.), InTech, Vienna, Austria, 2012.
_____________________________________________________________
- Sharma, SS, Dietz, KJ. The relationship between metal toxicity and cellular redox imbalance. Trends Plant Sci. 2009; 14: 43-50.
_____________________________________________________________
- Selmar D, Kleinwächter M. Stress enhances the synthesis of secondary plant products: The impact of stress-related over-reduction on the accumulation of natural products. Plant Cell Physiol 2013; 54: 817-826.
_____________________________________________________________
- Zheng Z, Wu M. Cadmium treatment enhances the production of alkaloid secondary metabolites of Catharanthus roseus. Plant Sci 2004; 166: 507-14.
_____________________________________________________________
- Srivastava NK, Srivastava AK. Influence of some heavy metals on growth, alkaloid content and composition in Catharanthus roseus L. Indian J Pharm Sci 2010; 72: 775-778.
_____________________________________________________________
- Fathalla MA, Abd-El Kawy AM, Taha HS. Effect of heavy metal (HgCl2) on accumulation and production of total indole alkaloids, vinblastine and/or vincristine from Egyptian Catharanthus Roseus (L.) G. Don. calli cultures. J Appl Sci Res 2011; 7: 542-549.
_____________________________________________________________
- Rai V, Tandon PK, Khatoon S. Effect of chromium on antioxidant potential of Catharanthus roseus varieties and production of their anticancer alkaloids: vincristine and vinblastine. Biomed Res Int 2014; 2014: 1-10.
_____________________________________________________________
- Reeves, RD. and Baker, AJM. Metal-accumulating plants. In: Phytoremediation of Toxic Metals: Using Plants to Clean Up the Environment. Raskin I., Ensley BD. (ed.), Wiley, New York, 2000, Pp. 193–229.
_____________________________________________________________
- Karuppanapandian T, Kim W. Cobalt-induced oxidative stress causes growth inhibition associated with enhanced lipid peroxidation and activates antioxidant responses in Indian mustard (Brassica juncea L.) leaves. Acta Physiol Plant 2013; 35: 2429–2443.
_____________________________________________________________
- Azarakhsh MR, Asrar Z, Mansouri H. Effects of seed and vegetative stage cysteine treatments on oxidative stress response molecules and enzymes in Ocimum basilicum L. under cobalt stress. J Soil Sci Plant Nutr 2015; 15: 651–662.
_____________________________________________________________
- Trejo-Tapia G, Jimenez-Aparicio A, Rodriguez-Monroy M, De Jesus-Sanchez A, Gutierrez-Lopez G. Influence of cobalt and other microelements on the production of betalains and the growth of suspension cultures of Beta vulgaris. Plant Cell Tissue Organ Cult 2001; 67: 19–23.
_____________________________________________________________
- Cai Z, Kastell A, Speiser C, Smetanska I. Enhanced resveratrol production in Vitis vinifera cell suspension cultures by heavy metals without loss of cell viability. Appl Biochem Biotechnol 2013; 171: 330-340.
_____________________________________________________________
- Urdová J, Rexová M, Mućaji P, Balažová A. Elicitation – a tool to improve secondary metabolites production in Melissa officinalis L. suspension cultures. Acta Fac Pharm Univ Comen 2015; 62: 46-50.
_____________________________________________________________
- Tammaru I. Effect of high cobalt rates on the accumulation of alkaloids in Datura stramonium. Tartu Ulikooli Toimetised 1980; 523: 65-70.
_____________________________________________________________
- Petrishek IA, Lovkova MY, Grinkevich NI, Orlova LP, Poludennyi LV. Effects of cobalt and copper on the accumulation of alkaloids in Atropa belladonna L. Biol Bull Acad Sci USSR 1984;10: 509-516.
_____________________________________________________________
- Taj G, Agarwal P, Grant M, Kumar A. MAPK machinery in plants: recognition and response to different stresses through multiple signal transduction pathways. Plant Signal Behav 2010; 5: 1370-1378.
_____________________________________________________________
- Raina SK, Wankhede DP, Jaggi M, Singh P, Jalmi SK, Raghuram B, Sheikh AH, Sinha AK. CrMPK3, a mitogen activated protein kinase from Catharanthus roseus and its possible role in stress induced biosynthesis of monoterpenoid indole alkaloids. BMC Plant Biol 2012; 12: 134.
_____________________________________________________________
- Pan YJ, Liu J, Guo XR, Zu YG, Tang ZH. Gene transcript profiles of the TIA biosynthetic pathway in response to ethylene and copper reveal their interactive role in modulating TIA biosynthesis in Catharanthus roseus. Protoplasma 2015; 252: 813-24.
_____________________________________________________________
- Schmid, G. Nanoparticles: From Theory to Application. Wiley, Weinheim 2010.
_____________________________________________________________
- Ghasemi B, Hosseini R, Nayeri FD. Effects of cobalt nanoparticles on artemisinin production and gene expression in Artemisia annua. Turk J Bot 2015; 39: 769-777.
_____________________________________________________________
- Murashige T, Skoog F. A revised medium for rapid growth and bioassay with tobacco tissue cultures. Plant Physiol 1962; 15: 473–497.
_____________________________________________________________
- Stewart RC, Bewley JD. Lipid peroxidation associated with accelerated aging of soybean axes. Plant Physiol 1980; 65: 245–248.
_____________________________________________________________
- Gong H, Chen G, Li F, Wang X, Hu Y, Bi Y. Involvement of G6PDH in heat stress tolerance in the calli from Przewalskia tangutica and Nicotiana tabacum . Biol Plant 2012; 56: 422–430.
_____________________________________________________________
- Beauchami C, Fridovich I. Superoxide dismutase: improved assays and an assay applicable to acrylamide gels. Anal Biochem 1971; 44: 276–287.
_____________________________________________________________
- Elkahouia S, Hernández JA, Abdellyc C, Ghrira R, Limama F. Effects of salt on lipid peroxidation and antioxidant enzyme activities of Catharanthus roseus suspension cells. Plant Sci 2005; 168: 607–613.
_____________________________________________________________
- Nakano Y, Asada K. Hydrogen peroxide is scavenged by ascorbate specific peroxidase in spinach chloroplasts. Plant Cell Physiol 1981; 22: 867-880
_____________________________________________________________
- Lowry OH, Rosebrough NJ, Farr AL, Randall RJ. Protein measurement with the folin phenol reagent. J biol Chem 1951; 193: 265–275.
_____________________________________________________________
- Lee SL, Cheng KD, Scott, AI. Effects of bioregulators on indole alkaloid biosynthesis in Catharanthus roseus cell culture. Phytochemistry 1981; 20: 1841–1843.
_____________________________________________________________
- George, EF., Puttock, DJM., George, HJ. Plant culture media (vol 2), Exegetics Co, Ltd., Westbury, 1988.
_____________________________________________________________
- Hilmy LM, Gad N. Effect of cobalt fertilization on the yield, quality and the essential oil composition of parsley leaves. Arab Univ J agr Sci 2002; 10: 803–829.
_____________________________________________________________
- Javed SB, Anis M. Cobalt induced augmentation of in vitro morphogenic potential in Erythrina variegata L.: a multipurpose tree legume. Plant Cell Tissue Organ Cult 2015; 120: 463–474.
_____________________________________________________________
- Sharma P, Jha AB, Dubey RS, Pessarakli M. Reactive oxygen species, oxidative damage, and antioxidative defense mechanism in plants under stressful conditions. J Bot 2012; doi:10.1155/2012/217037.
_____________________________________________________________
- Kovtun Y, Chiu WL, Tena G, Sheen J. Functional analysis of oxidative stress-activated mitogen-activated protein kinase cascade in plats. Proc nat Acad. Sci USA 2000; 97: 2940–2945.
_____________________________________________________________
- Jonak C, Nakagami H, Hirt H. Heavy metal stress. Activation of distinct mitogen-activated protein kinase pathways by copper and cadmium. Plant Physiol 2004; 136: 3276–3283.
____________________________________________________________ M, Hu X. Mitogen-activated protein kinase is involved in abscisic acid-induced antioxidant defense and acts downstream of reactive oxygen species production in leaves of maize plants. Plant Physiol 2006; 141: 475-487.
_____________________________________________________________
- Amarasinghe A. Effects of copper sulphate and cobalt chloride on in vitro performances of traditional indica rice (Oryza sativa L.) varieties in Sri Lanka. J agr Sci 2009; 4: 132-141.
_____________________________________________________________
- Shi BEN, Ni LAN, Liu Y, Zhang A, Tan M, Jiang M. OsDMI3-mediated activation of OsMPK1 regulates the activities of antioxidant enzymes in abscisic acid signalling in rice. Plant Cell Environ 2014; 37: 341–352.
_____________________________________________________________
- Gill SS, Tuteja N. Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiol and Biochem 2010; 48: 909–930.
_____________________________________________________________
- Tewari RK, Kumar P, Sharma PN, Bisht SS: Modulation of oxidative stress responsive enzymes by excess cobalt. Plant Sci 2002; 162: 381–388.
_____________________________________________________________
- Pandey N, Pathak GC, Pandey DK, Pandey R. Heavy metals, Co, Ni, Cu, Zn and Cd, produce oxidative damage and evoke differential antioxidant responses in spinach. Braz J Plant Physiol 2009; 21: 103-111.
_____________________________________________________________
- Sinha P, Nautiyal N. Excessive cobalt induced oxidative stress in groundnut. Indian J Plant Physiol 2012; 17: 71-74.
_____________________________________________________________
- Arora P, Bhardwaj R, Kanwar MK. Effect of 24-epibrassinolide on growth, protein content and antioxidative defense system of Brassica juncea L. subjected to cobalt ion toxicity. Acta Physiol Plant 2012; 34: 2007–2017.
_____________________________________________________________
- Liu Y, Meng Q, Duan X, Zhang Z, Li D. Effects of PEG-induced drought stress on regulation of indole alkaloid biosynthesis in Catharanthus roseus. J Plant Interact 2017; 12: 87–9.
_____________________________________________________________
- Pandey, SS, Singh, S, Babu, CSV, Shanker, K, Srivastava, NK, Shukla, AK, Kalra, A. Fungal endophytes of Catharanthus roseus enhance vindoline content by modulating structural and regulatory genes related to terpenoid indole alkaloid biosynthesis. Sci Rep 2016; 6: 26583.
_____________________________________________________________
- Faisal M, Saquib Q, Alatar AA, Al-Khedhairy AA, Ahmed M, Ansari SM, Praveen S. Cobalt oxide nanoparticles aggravate DNA damage and cell death in eggplant via mitochondrial swelling and NO signaling pathway. Biol Res 2016; 49: 20.
_____________________________________________________________
- Nymark P, Catalán J, Suhonen S, Järventaus H, Birkedal R, Clausen PA, Jensen KA, Vippola M, Savolainen K, Norppa H. Genotoxicity of polyvinylpyrrolidone coated silver nanoparticles in BEAS 2B cells. Toxicology 2013; 8: 38-48.
_____________________________________________________________
- Fouad, AS, Hafez, RM. The effects of silver ions and silver nanoparticles on cell division and expression of cdc2 gene in Allium cepa root tips.Biol Plant 2018; 62: 166-172.