Abstract
Chemically synthesized silver nanoparticles (AgNP) have been assessed on plant tissue cultures but the impact of biologically synthesized AgNP fabricated by different phytoconstituents has not been sufficiently investigated. In this study biogenic AgNP prepared from leaf extract of Swertia chirata was utilized to address the problems associated with conservation of endangered medicinal plant through plant tissue culture. Endangered as well as economically important medicinal plant considered for this analysis was the same plant S. chirata itself. Excessive deforestation and exploration of this plant had led to complete eradication of the natural reservoir. Thus in vitro plant tissue propagation had attained much importance for maintaining the plant species. Nano-sized particles of diameter 20 nm encapped by different phytochemicals applied on regenerating shoot cultures showed enhanced shoot induction and proliferation. Other forms of silver like AgNO3 (SN) and Ag2S2O3 (STS) showed improved regeneration in comparison to control samples. Ethylene precursors like 1-aminocyclopropane-1-carboxylic acid (ACC) and 2-chloroethylphosphonic acid (CEPA) downregulated the regeneration process considerably. Reactive oxygen species (ROS) status of the treated cultures were evaluated considering hydrogen peroxide and malondialdehyde (MDA) content in treated cells as wells as their antioxidant enzyme activity. Combined manipulation and coordination of ethylene evolution, maintenance of ROS balance and better bio-acceptance of AgNP were responsible for improvement in shoot regeneration of the plant. Phytoencapsulated and nano-dimensioned Ag was capable of changing the chemical reactions of different regulating players of plant regeneration. These findings will facilitate the understanding and future utilization of biofabricated AgNP in agriculture and plant sciences.
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Abbreviations
- AgNP:
-
Silver nanoparticles
- SN:
-
Silver nitrate
- STS:
-
Silver thiosulphate
- ACC:
-
1-Aminocyclopropane-1-carboxylic acid
- CEPA:
-
2-Chloroethylphosphonic acid
- ROS:
-
Reactive oxygen species
- MDA:
-
Malondialdehyde
- SPR:
-
Surface plasmon resonance
- MS:
-
Murashige and Skoog medium
- BAP:
-
6-Benzylaminopurine
- CC:
-
Cobalt chloride
- NaTS:
-
Sodium thiosulphate
- TCA:
-
Trichloroacetic acid
- TBA:
-
Thiobarbituric acid
- SOD:
-
Superoxide dismutase
- CAT:
-
Catalase
- POX:
-
Peroxidase
- APX:
-
Ascorbate peroxidase
- GR:
-
Glutathione reductase
- PMSF:
-
Phenylmethylsulfonyl fluoride
- PVP:
-
Polyvinylpyrrolidone
- EDTA:
-
Ethylene diaminetetraacetic acid
- BSA:
-
Bovine serum albumin
- NBT:
-
Nitro blue tetrazolium chloride
- GSSG:
-
Oxidized glutathione
- NADPH:
-
Nicotinamide adenine dinucleotide phosphate reduced
- ANOVA:
-
One-way analysis of variance
- DMRT:
-
Duncan’s multiple range test
- LSD:
-
Least significant difference
- TEM:
-
Transmission electron microscopy
- FTIR:
-
Fourier-transform infrared spectroscopy.
References
Aghdaei M, Salehi H, Sarmast MK (2012) Effects of silver nanoparticles on Tecomella undulata (Roxb.) Seem. micropropagation. Adv Hortic Sci 26:21–24. https://doi.org/10.13128/ahs-12748
Beyer WF, Fridovich I (1987) Assaying for superoxide dismutase activity: some large consequences of minor changes in conditions. Anal Biochem 161:559–566. https://doi.org/10.1016/0003-2697(87)90489-1
Dutta Gupta S (2011) Role of free radicals and antioxidants in in vitro morphogenesis. In: Dutta Gupta S (ed) Reactive oxygen species and antioxidants in higher plants. CRC Press, New York, pp 229–247
Dutta Gupta S, Datta S (2003) Antioxidant enzyme activities during in vitro morphogenesis of gladiolus. Biol Plant 47:179–183. https://doi.org/10.1023/B:BIOP.0000022248.62869.c7
Dutta Gupta S, Karmakar A (2017) Machine vision based evaluation of impact of light emitting diodes (LEDs) on shoot regeneration and the effect of spectral quality on phenolic content and antioxidant capacity in Swertia chirata. J Photochem Photobiol B 174:162–172. https://doi.org/10.1016/j.jphotobiol.2017.07.029
Eapen S, George L (1997) Plant regeneration from peduncle segments of oil seed Brassica species: influence of silver nitrate and silver thiosulfate. Plant Cell Tissue Organ Cult 51:229–232. https://doi.org/10.1023/A:1005926108586
Ewais EA, Desouky SA, Elshazly EH (2015) Evaluation of callus responses of Solanum nigrum L. exposed to biologically synthesized silver nanoparticles. Nanosci Nanotechnol 5:45–56. https://doi.org/10.5923/j.nn.20150503.01
Fazal H, Abbasi BH, Ahmad N, Ali M (2016) Elicitation of medicinally important antioxidant secondary metabolites with silver and gold nanoparticles in callus cultures of Prunella vulgaris L. Appl Biochem Biotechnol 180:1076–1092. https://doi.org/10.1007/s12010-016-2153-1
Foyer CH, Halliwell B (1976) The presence of glutathione and glutathione reductase in chloroplasts: a proposed role in ascorbic acid metabolism. Planta 133:121–125
Girotti AW (1990) Photodynamic lipid peroxidation in biological systems. Photochem Photobiol 51:497–509. https://doi.org/10.1111/j.1751-1097.1990.tb01744.x
Kala CP, Sajwan BS (2007) Revitalizing Indian systems of herbal medicine by the National Medicinal Plants Board through institutional networking and capacity building. Curr Sci 93:797–806
Kar M, Mishra D (1976) Catalase, peroxidase, and polyphenoloxidase activities during rice leaf senescence. Plant Physiol 57:315–319. https://doi.org/10.1104/pp.57.2.315
Khalafalla MM, Hattori K (2000) Ethylene inhibitors enhance in vitro root formation on faba bean shoots regenerated on medium containing thidiazuron. Plant Growth Regul 32:59–63. https://doi.org/10.1023/A:1006305123585
Kim DH, Gopal J, Sivanesan I (2017) Nanomaterials in plant tissue culture: the disclosed and undisclosed. RSC Adv 7:36492–36505. https://doi.org/10.1039/C7RA07025J
Kumar V, Ramakrishna A, Ravishankar GA (2007) Influence of different ethylene inhibitors on somatic embryogenesis and secondary embryogenesis from Coffea canephora P ex Fr. Vitr Cell Dev Biol 43:602–607. https://doi.org/10.1007/s11627-007-9067-0
Kumar V, Parvatam G, Ravishankar GA (2009) AgNO3—a potential regulator of ethylene activity and plant growth modulator. Electron J Biotechnol 12:1–15. https://doi.org/10.2225/vol12-issue2-fulltext-1
Kumar GP, Sivakumar S, Siva G et al (2016) Silver nitrate promotes high-frequency multiple shoot regeneration in cotton (Gossypium hirsutum L.) by inhibiting ethylene production and phenolic secretion. Vitr Cell Dev Biol 52:408–418. https://doi.org/10.1007/s11627-016-9782-5
Kumari M, Khan. S, Pakrashi S et al (2011) Cytogenetic and genotoxic effects of zinc oxide nanoparticles on root cells of Allium cepa. J Hazard Mater 190:613–621. https://doi.org/10.1016/j.jhazmat.2011.03.095
Lowry OH, Rosebrough NJ, Farr ALRR. (1951) Protein measurement with the Folin phenol reagent. J Biol Chem 193:265–275. https://doi.org/10.1016/0304-3894(92)87011-4
Murashige T, Skoog F (1962) A revised medium for rapid growth and bio assays with tobacco tissue cultures. Physiol Plant 15:473–497
Nakano Y, Asada K (1981) Hydrogen peroxide is scavenged by ascorbate-specific peroxidase in spinach chloroplastsle. Plant cell Physiol 22:867–880
Raei M, Angaji SA, Omidi M, Khodayari M (2014) Effect of abiotic elicitors on tissue culture of Aloe vera. Int J Biosci 6655:74–81
Saha N, Dutta Gupta S (2015) Synthesis, characterization and bioactivity of nanoparticles from medicinal plants. In: Pathak M, Govil JN (eds) Recent progress in medicinal plants. Studium Press, East Rutherford, pp 471–501
Saha N, Dutta Gupta S (2017) Low-dose toxicity of biogenic silver nanoparticles fabricated by Swertia chirata on root tips and flower buds of Allium cepa. J Hazard Mater. https://doi.org/10.1016/j.jhazmat.2017.01.021
Sankhla D, Sankhla N, Davis T (1995) Promotion of in vitro shoot formation from excised roots of silktree (Albizia julibrissin) by an oxime ether derivative and other ethylene inhibitors. Plant Cell Rep 15:143–146. https://doi.org/10.1007/BF01690272
Sarmast MK, Niazi A, Salehi H, Abolimoghadam A (2015) Silver nanoparticles affect ACS expression in Tecomella undulata in vitro culture. Plant Cell Tissue Organ Cult 121:227–236. https://doi.org/10.1007/s11240-014-0697-8
Sergiev I, Alexieva V, Karanov E (1997) Effect of spermine, atrazine and combination between them on some endogenous protective systems and stress markers in plants. Compt Rend Acad Bulg Sci 51:121–124
Sharma P, Bhatt D, Zaidi MGH et al (2012) Silver nanoparticle-mediated enhancement in growth and antioxidant status of Brassica juncea. Appl Biochem Biotechnol 167:2225–2233. https://doi.org/10.1007/s12010-012-9759-8
Shukla JK, Dhakal P, Uniyal RC et al (2017) Ex-situ cultivation at lower altitude and evaluation of Swertia chirayita, a critically endangered medicinal plant of Sikkim Himalayan region, India. S Afr J Bot 109:138–145. https://doi.org/10.1016/j.sajb.2017.01.001
Spinoso-Castillo JL, Chavez-Santoscoy RA, Bogdanchikova N et al (2017) Antimicrobial and hormetic effects of silver nanoparticles on in vitro regeneration of vanilla (Vanilla planifolia Jacks. ex Andrews) using a temporary immersion system. Plant Cell Tissue Organ Cult 129:195–207. https://doi.org/10.1007/s11240-017-1169-8
Steinitz B, Barr N, Tabib Y et al (2010) Control of in vitro rooting and plant development in Corymbia maculata by silver nitrate, silver thiosulfate and thiosulfate ion. Plant Cell Rep 29:1315–1323. https://doi.org/10.1007/s00299-010-0918-5
Syu Y, Hung JH, Chen JC, Chuang H (2014) Impacts of size and shape of silver nanoparticles on Arabidopsis plant growth and gene expression. Plant Physiol Biochem 83:57–64. https://doi.org/10.1016/j.plaphy.2014.07.010
Thakar J, Bhargava S (1999) Seasonal variation in antioxidant enzymes and the sprouting response of Gmelina arborea Roxb. nodal sectors cultured in vitro. Plant Cell Tissue Organ Cult 59:181–187. https://doi.org/10.1023/A:1006433429425
Velikova V, Yordanov I, Edreva A (2000) Oxidative stress and some antioxidant systems in acid rain-treated bean plants. Plant Sci 151:59–66. https://doi.org/10.1016/S0168-9452(99)00197-1
Venkatachalam P, Malar S, Thiyagarajan M et al (2017) Effect of phycochemical coated silver nanocomplexes as novel growth-stimulating compounds for plant regeneration of Alternanthera sessilis L. J Appl Phycol 29:1095–1106. https://doi.org/10.1007/s10811-016-0977-2
Wang P, Lombi E, Zhao FJ, Kopittke PM (2016) Nanotechnology: a new opportunity in plant sciences. Trends Plant Sci 21:699–712. https://doi.org/10.1016/j.tplants.2016.04.005
Zhang B, Zheng LP, Yi Li W, Wen Wang J (2013) Stimulation of artemisinin production in Artemisia annua hairy roots by Ag-SiO2 core-shell nanoparticles. Curr Nanosci 9:363–370
Zuverza-Mena N, Martínez-Fernández D, Du W et al (2017) Exposure of engineered nanomaterials to plants: insights into the physiological and biochemical responses—a review. Plant Physiol Biochem 110:236–264. https://doi.org/10.1016/j.plaphy.2016.05.037
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We gratefully acknowledge the financial support from the Department of Agriculture and Food Engineering, Indian Institute of Technology, Kharagpur.
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Saha, N., Dutta Gupta, S. Promotion of shoot regeneration of Swertia chirata by biosynthesized silver nanoparticles and their involvement in ethylene interceptions and activation of antioxidant activity. Plant Cell Tiss Organ Cult 134, 289–300 (2018). https://doi.org/10.1007/s11240-018-1423-8
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DOI: https://doi.org/10.1007/s11240-018-1423-8