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An efficient in vitro shoot regeneration through direct organogenesis from seedling-derived petiole and leaf segments and acclimatization of Ficus religiosa

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Abstract

Prolific and rapid in vitro plant organogenesis via direct regeneration has been obtained from axenic seedling-derived petiole and leaf explants of Ficus religiosa in Murashige and Skoog (MS) medium containing different concentrations of cytokinins in combination with indole-3-butyric acid (IBA). MS medium with 1.5 mg/l 6-benzylaminopurine plus 0.15 mg/l IBA produced the highest shoot induction frequency with an average of 6.26 and 10.13 shoots per leaf and petiole explants, respectively. After 4 weeks, the highest root formation frequency (96.7%), root number (5.73), and root length (4.76 cm) were with MS medium containing 2.0 mg/l IBA plus 0.1 mg/l α-naphthalene acetic acid. In addition, the effect of four sodium nitroprusside (SNP) treatments on acclimatization was also studied. Highest morphological traits such as survival rates, fresh and dry root weights as well as antioxidant enzymatic activities such as superoxide dismutase, peroxidase, and catalase was achieved with 125 ppm SNP. The α-amino acid, proline, content was highest with this treatment while the highest H2O2 (hydrogen peroxide) was in the controls. This study introduces a cost-effective, prolific, and efficient in vitro multiplication system to supply pharmaceutical and ornamental needs. It is the first report of an in vitro organogenesis protocol for F. religiosa by direct regeneration through axenic seedling-derived petiole and leaf explants, which can be efficiently employed for the utilization of active biomolecules.

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References

  • Abeles FB, Biles CL (1991) Characterization of peroxidases in lignifying peach fruit endocarp. Plant Physiol 95:269–273

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ahmad N, Anis M (2007) Rapid clonal multiplication of a woody tree, Vitex negundo L. through axillary shoots proliferation. Agrofor Syst 71:195–200

    Article  Google Scholar 

  • 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 

  • Ahmad Z, Shahzad A, Sharma S (2017) Enhanced multiplication and improved ex vitro acclimatization of Decalepis arayalpathra. Biol Plant 61:1–10

    Article  CAS  Google Scholar 

  • Ahmed MR, Anis M (2014) Changes in activity of antioxidant enzymes and photosynthetic machinery during acclimatization of micropropagated Cassia alata L. plantlets. In Vitro Cell Dev Biol Plant 50:601–609

    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 

  • Ali MB, Hahn EJ, Paek KY (2005) Effects of light intensities on antioxidant enzymes and malondialdehyde content during short-term acclimatization on micropropagated Phalaenopsis plantlet. Environ Exp Bot 54:109–120

    Article  CAS  Google Scholar 

  • Ashraf M, Foolad M (2007) Roles of glycine betaine and proline in improving plant abiotic stress resistance. Environ Exp Bot 59:206–216

    Article  CAS  Google Scholar 

  • Bates L, Waldren R, Teare I (1973) Rapid determination of free proline for water-stress studies. Plant Soil 39:205–207

    Article  CAS  Google Scholar 

  • Beligni MAV, Lamattina L (1999) Nitric oxide protects against cellular damage produced by methylviologen herbicides in potato plants. Nitric Oxide 3:199–208

    Article  CAS  PubMed  Google Scholar 

  • Bhangale JO, Acharya NS, Acharya SR (2016) Protective effect of Ficus religiosa (L.) against 3-nitropropionic acid induced Huntington disease. Orient Pharm Exp Med 16:165–174

    Article  CAS  Google Scholar 

  • Bhojwani SS, Dantu PK (2013) Micropropagation. In: Bhojwani SS, Dantu PK (eds) Plant tissue culture: an introductory text. Springer, New Delhi, pp 245–274

    Chapter  Google Scholar 

  • Bosela MJ, Michler C (2008) Media effects on black walnut (Juglans nigra L.) shoot culture growth in vitro: evaluation of multiple nutrient formulations and cytokinin types. In Vitro Cell Dev Biol Plant 44:316–329

    Article  CAS  Google Scholar 

  • Boveris A, Costa LE, Poderoso JJ, Carreras MC, Cadenas E (2000a) Regulation of mitochondrial respiration by oxygen and nitric oxide. Ann N Y Acad Sci 899:121–135

    Article  CAS  PubMed  Google Scholar 

  • Boveris A, Galatro A, Puntarulo S (2000b) Effect of nitric oxide and plant antioxidants on microsomal content of lipid radicals. Biol Res 33:159–165

    Article  CAS  PubMed  Google Scholar 

  • Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254

    Article  CAS  Google Scholar 

  • Cagno V, Civra A, Kumar R, Pradhan S, Donalisio M, Sinha BN, Ghosh M, Lembo D (2015) Ficus religiosa L. bark extracts inhibit human rhinovirus and respiratory syncytial virus infection in vitro. J Ethnopharmacol 176:252–257

    Article  PubMed  Google Scholar 

  • Caro A, Puntarulo S (1998) Nitric oxide decreases superoxide anion generation by microsomes from soybean embryonic axes. Physiol Plant 104:357–364

    Article  CAS  Google Scholar 

  • Chakrabarty D, Datta SK (2008) Micropropagation of gerbera: lipid peroxidation and antioxidant enzyme activities during acclimatization process. Acta Physiol Plant 30:325–331

    Article  CAS  Google Scholar 

  • Chandra S, Bandopadhyay R, Kumar V, Chandra R (2010) Acclimatization of tissue cultured plantlets: from laboratory to land. Biotechnol Lett 32:1199–1205

    Article  CAS  Google Scholar 

  • Deb C, Imchen T (2010) An efficient in vitro hardening technique of tissue culture raised plants. Biotechnology 9:79–83

    Article  Google Scholar 

  • Deshpande S, Josekutty P, Prathapasenan G (1998) Plant regeneration from axillary buds of a mature tree of Ficus religiosa. Plant Cell Rep 17:571–573

    Article  CAS  PubMed  Google Scholar 

  • Dias M, Pinto G, Guerra C, Jesus C, Amaral J, Santos C (2013) Effect of irradiance during acclimatization on content of proline and phytohormones in micropropagated Ulmus minor. Biol Plant 57:769–772

    Article  CAS  Google Scholar 

  • Durner J, Klessig DF (1999) Nitric oxide as a signal in plants. Curr Opin Plant Biol 2:369–374

    Article  CAS  PubMed  Google Scholar 

  • Dwivedi P, Narvi SS, Tewari RP (2014) Phytofabrication characterization and comparative analysis of Ag nanoparticles by diverse biochemicals from Elaeocarpus ganitrus Roxb., Terminalia arjuna Roxb., Pseudotsuga menzietii, Prosopis spicigera, Ficus religiosa, Ocimum sanctum, Curcuma longa. Ind Crops Prod 54:22–31

    Article  CAS  Google Scholar 

  • Farooq M, Wahid A, Kobayashi N, Fujita D, Basra S (2009) Plant drought stress: effects, mechanisms and management. In: Lichtfouse E (ed) Sustainable agriculture. Springer, Dordrecht, pp 153–188

    Chapter  Google Scholar 

  • Feng JC, Yu XM, Shang XL, Li JD, Wu YX (2010) Factors influencing efficiency of shoot regeneration in Ziziphus jujuba Mill. ‘Huizao’. Plant Cell Tissue Organ Cult 101:111–117

    Article  CAS  Google Scholar 

  • Giannopolitis CN, Ries SK (1977) Superoxide dismutases I. Occurrence in higher plants. Plant Physiol 59:309–314

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gill SS, Tuteja N (2010) Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiol Biochem 48:909–930

    Article  CAS  PubMed  Google Scholar 

  • Gonçalves S, Martins N, Romano A (2017) Physiological traits and oxidative stress markers during acclimatization of micropropagated plants from two endangered Plantago species: P. algarbiensis Samp. and P. almogravensis Franco. In Vitro Cell Dev Biol Plant 54:1–7

    Google Scholar 

  • Han XJ, Yang HQ, Duan KX, Zhang XR, Zhao HZ, You SZ, Jiang QQ (2009) Sodium nitroprusside promotes multiplication and regeneration of Malus hupehensis in vitro plantlets. Plant Cell Tissue Org Cult 96:29–34

    Article  CAS  Google Scholar 

  • Hassan AS, Afroz F, Jahan MAA, Khatun R (2009) In vitro regeneration through apical and axillary shoot proliferation of Ficus religiosa l.-a multi-purpose woody medicinal plant. Plant Tissue Cult Biotechnol 19:71–78

    Article  Google Scholar 

  • Havir EA, McHale NA (1987) Biochemical and developmental characterization of multiple forms of catalase in tobacco leaves. Plant Physiol 84:450–455

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hesami M, Daneshvar MH, Lotfi A (2017) In vitro shoot proliferation through cotyledonary node and shoot tip Explants of Ficus religiosa L. Plant Tissue Cult Biotech 27:85–88

    Article  Google Scholar 

  • Huang DQ, Dai WH (2011) Direct regeneration from in vitro leaf and petiole tissues of Populus tremula ‘Erecta’. Plant Cell Tissue Organ Cult 107:169–174

    Article  Google Scholar 

  • Inthima P, Nakano M, Otani M, Niki T, Nishijima T, Koshioka M, Supaibulwatana K (2017) Overexpression of the gibberellin 20-oxidase gene from Torenia fournieri resulted in modified trichome formation and terpenoid metabolities of Artemisia annua L. Plant Cell Tissue Organ Cult 112:1–14

    Google Scholar 

  • Jaiswal V, Narayan P (1985) Regeneration of plantlets from the callus of stem segments of adult plants of Ficus religiosa L. Plant Cell Rep 4:256–258

    Article  CAS  PubMed  Google Scholar 

  • Karami O, Piri K, Bahmani R (2009) Plant regeneration through callus cultures derived from immature-cotyledon explants of oleaster (Elaeagnus angustifolia L.). Trees 23:335–338

    Article  CAS  Google Scholar 

  • Kaur A, Sandhu JS (2015) High throughput in vitro micropropagation of sugarcane (Saccharum officinarum L.) from spindle leaf roll segments: cost analysis for agri-business industry. Plant Cell Tissue Org Cult 120:339–350

    Article  CAS  Google Scholar 

  • Kavas M, Baloğlu MC, Akça O, Köse FS, Gökçay D (2013) Effect of drought stress on oxidative damage and antioxidant enzyme activity in melon seedlings. Turk J Biol 37:491–498

    Article  CAS  Google Scholar 

  • Leterrier M, Valderrama R, Chaki M, Airaki M, Palma JM, Barroso JB, Corpas FJ (2012) Function of nitric oxide under environmental stress conditions. In: Iqbal N, Nazar R (eds) Phytohormones and abiotic stress tolerance in plants. Springer, Berlin, pp 99–113

    Chapter  Google Scholar 

  • Mali AM, Chavan NS (2016) In vitro rapid regeneration through direct organogenesis and ex-vitro establishment of Cucumis trigonus Roxb.—an underutilized pharmaceutically important cucurbit. Ind Crops Prod 83:48–54

    Article  CAS  Google Scholar 

  • Mallurwar V, Pathak A (2008) Studies on immunomodulatory activity of Ficus religiosa. Indian J Pharm Educ Res 42:341–343

    Google Scholar 

  • Mansouri K, Preece JE (2009) The influence of plant growth regulators on explant performance, bud break, and shoot growth from large stem segments of Acer saccharinum L. Plant Cell Tissue Organ Cult 99:313

    Article  CAS  Google Scholar 

  • Neill SJ, Desikan R, Hancock JT (2003) Nitric oxide signalling in plants. New Phytol 159:11–35

    Article  CAS  Google Scholar 

  • Niazian M, Noori SAS, Galuszka P, Tohidfar M, Mortazavian SMM (2017) Genetic stability of regenerated plants via indirect somatic embryogenesis and indirect shoot regeneration of Carum copticum L. Ind Crops Prod 97:330–337

    Article  CAS  Google Scholar 

  • Noctor G, Mhamdi A, Foyer CH (2014) The roles of reactive oxygen metabolism in drought: not so cut and dried. Plant Physiol 164:1636–1648

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Osório ML, Osório J, Gonçalves S, David MM, Correia MJ, Romano A (2012) Carob trees (Ceratonia siliqua L.) regenerated in vitro can acclimatize successfully to match the field performance of seed-derived plants. Trees 26:1837–1846

    Article  CAS  Google Scholar 

  • Pandey S, Fartyal D, Agarwal A, Shukla T, James D, Kaul T, Negi YK, Arora S, Reddy MK (2017) Abiotic Stress tolerance in plants: myriad roles of ascorbate peroxidase. Front Plant Sci 8:1–12

    PubMed  PubMed Central  Google Scholar 

  • Piwowarczyk B, Tokarz K, Makowski W, Łukasiewicz A (2017) Different acclimatization mechanisms of two grass pea cultivars to osmotic stress in in vitro culture. Acta Physiol Plant 39:96

    Article  CAS  Google Scholar 

  • Prajapati SK, Tripathi B (2008) Anticipated Performance Index of some tree species considered for green belt development in and around an urban area: a case study of Varanasi city, India. J Environ Manag 88:1343–1349

    Article  Google Scholar 

  • Salmi MS, Hesami M (2016) Time of collection, cutting ages, auxin types and concentrations influence rooting Ficus religiosa L. stem cuttings. J Appl Environ Biol Sci 6:124–132

    Google Scholar 

  • Sarropoulou V, Dimassi-Theriou K, Therios I (2014) Ιn vitro plant regeneration from leaf explants of the cherry rootstocks CAB-6P, Gisela 6, and MxM 14 using sodium nitroprusside. In Vitro Cell Dev Biol Plant 50:226–234

    Article  CAS  Google Scholar 

  • Scalet M, Federico R, Guido M, Manes F (1995) Peroxidase activity and polyamine changes in response to ozone and simulated acid rain in Aleppo pine needles. Env Exp Bot 35:417–425

    Article  CAS  Google Scholar 

  • Shigeoka S, Ishikawa T, Tamoi M, Miyagawa Y, Takeda T, Yabuta Y, Yoshimura K (2002) Regulation and function of ascorbate peroxidase isoenzymes. J Exp Bot 53:1305–1319

    Article  CAS  PubMed  Google Scholar 

  • Singh D, Singh B, Goel RK (2011) Traditional uses, phytochemistry and pharmacology of Ficus religiosa: a review. J Ethnopharmacol 134:565–583

    Article  CAS  PubMed  Google Scholar 

  • Singh C, Raj SR, Jaiswal P, Patil V, Punwar B, Chavda J, Subhash N (2016) Effect of plant growth regulators on in vitro plant regeneration of sandalwood (Santalum album L.) via organogenesis. Agrofor Syst 90:281–288

    Article  Google Scholar 

  • Sivanesan I, Song JY, Hwang SJ, Jeong BR (2011) Micropropagation of Cotoneaster wilsonii Nakai—a rare endemic ornamental plant. Plant Cell Tissue Organ Cult 105:55–63

    Article  Google Scholar 

  • Siwach P, Gill AR (2011) Enhanced shoot multiplication in Ficus religiosa L. in the presence of adenine sulphate, glutamine and phloroglucinol. Physiol Mol Biol Plants 17:271

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Siwach P, Gill AR (2014) Micropropagation of Ficus religiosa L. via leaf explants and comparative evaluation of acetylcholinesterase inhibitory activity in the micropropagated and conventionally grown plants. Biotech 4:477–491

    Google Scholar 

  • Xiao Z, Fu RP, Li JY, Fan ZQ, Yin HF (2016) Overexpression of the gibberellin 2-oxidase gene from Camellia lipoensis induces dwarfism and smaller flowers in Nicotiana tabacum. Plant Mol Biol Rep 34:182–191

    Article  CAS  Google Scholar 

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Authors and Affiliations

  1. Department of Horticulture Science, University of Tehran, Karaj, Alborz, 14176-14418, Iran

    Mohsen Hesami & Mohsen Yoosefzadeh-Najafabadi

  2. Department of Horticulture Science, Ramin University of Agriculture and Natural Resources, Ahwaz, Khuzestan, 63417-73637, Iran

    Mohammad Hosein Daneshvar

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  1. Mohsen Hesami
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  2. Mohammad Hosein Daneshvar
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  3. Mohsen Yoosefzadeh-Najafabadi
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Correspondence to Mohsen Hesami.

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Corresponding editor: Tao Xu.

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Hesami, M., Daneshvar, M.H. & Yoosefzadeh-Najafabadi, M. An efficient in vitro shoot regeneration through direct organogenesis from seedling-derived petiole and leaf segments and acclimatization of Ficus religiosa. J. For. Res. 30, 807–815 (2019). https://doi.org/10.1007/s11676-018-0647-0

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