Advertisement

Effects of sodium nitroprusside on callus browning of Ficus religiosa: an important medicinal plant

  • Mohsen Hesami
  • Masoud Tohidfar
  • Milad Alizadeh
  • Mohammad Hosein Daneshvar
Original Paper
  • 11 Downloads

Abstract

Tissue browning is a major problem in tissue culturing of woody plants, especially for Ficus religiosa which occurs by the accumulation and oxidation of phenolic compounds. This study aimed to determine the effect of different concentrations of sodium nitroprusside on the appearance of callus browning from leaf explants. The results indicate that callus browning was significantly reduced by supplementation of sodium nitroprusside to the MS medium and supplemented with 2.26 μM of 2,4-dichlorophenoxyacetic acid and 0.22 μM of 6-benzyl amino purine. The accumulation of hydrogen peroxide and phenolic compounds in the callus tissues decreased at the 50 μM concentration of sodium nitroprusside. Although catalase and peroxidase activities decreased at the 50 μM concentration, the activity of superoxide dismutase and polyphenol oxidases, as well as proline content, increased exponentially. Sodium nitroprusside could be useful for the formation of non-embryogenic callus with high levels of metabolic activity for the production and isolation of secondary metabolites.

Keywords

Nitric oxide Oxidative enzymes Proline Reactive oxygen species 

Notes

Authors’ contribution

All authors listed have made substantial, direct and intellectual contribution to the work, and have approved it for publication.

References

  1. Arasimowicz M, Floryszak-Wieczorek J (2007) Nitric oxide as a bioactive signalling molecule in plant stress responses. Plant Sci 172:876–887CrossRefGoogle Scholar
  2. Beauchamp C, Fridovich I (1971) Superoxide dismutase: improved assays and an assay applicable to acrylamide gels. Anal Biochem 44:276–287CrossRefGoogle Scholar
  3. Cakmak I, Horst WJ (1991) Effect of aluminium on lipid peroxidation, superoxide dismutase, catalase, and peroxidase activities in root tips of soybean (Glycine max). Physiol Plant 83:463–468CrossRefGoogle Scholar
  4. Chugh S, Guha S, Rao IU (2009) Micropropagation of orchids: a review on the potential of different explants. Sci Hortic 122:507–520CrossRefGoogle Scholar
  5. Corpas FJ, Barroso JB (2017) Lead-induced stress, which triggers the production of nitric oxide (NO) and superoxide anion (O2·−) in Arabidopsis peroxisomes, affects catalase activity. Nitric Oxide 68:103–110CrossRefGoogle Scholar
  6. de Pinto MC, De Gara L (2004) Changes in the ascorbate metabolism of apoplastic and symplastic spaces are associated with cell differentiation. J Exp Bot 55:2559–2569CrossRefGoogle Scholar
  7. de Pinto MC, Tommasi F, De Gara L (2002) Changes in the antioxidant systems as part of the signaling pathway responsible for the programmed cell death activated by nitric oxide and reactive oxygen species in tobacco Bright-Yellow 2 cells. Plant Physiol 130:698–708CrossRefGoogle Scholar
  8. Dehon L, Macheix J, Durand M (2002) Involvement of peroxidases in the formation of the brown coloration of heartwood in Juglans nigra. J Exp Bot 53:303–311CrossRefGoogle Scholar
  9. Duncan DB (1955) Multiple range and multiple F tests. Biometrics 11:1–42CrossRefGoogle Scholar
  10. Errabii T, Gandonou CB, Essalmani H, Abrini J, Idaomar M, Senhaji NS (2007) Effects of NaCl and mannitol induced stress on sugarcane (Saccharum sp.) callus cultures. Acta Physiol Plant 29:95CrossRefGoogle Scholar
  11. Flora SJ (2009) Structural, chemical and biological aspects of antioxidants for strategies against metal and metalloid exposure. Oxid Med Cell Longev 2:191–206CrossRefGoogle Scholar
  12. Foyer C, Descourvieres P, Kunert K (1994) Protection against oxygen radicals: an important defence mechanism studied in transgenic plants. Plant Cell Environ 17:507–523CrossRefGoogle Scholar
  13. Gill SS, Tuteja N (2010) Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiol Biochem 48:909–930CrossRefGoogle Scholar
  14. Guo Y, Tian Z, Yan D, Zhang J, Qin P (2009) Effects of nitric oxide on salt stress tolerance in Kosteletzkya virginica. Life Sci J 6:67–75Google Scholar
  15. Han X, Yang H, Duan K, Zhang X, Zhao H, You S, Jiang Q (2009) Sodium nitroprusside promotes multiplication and regeneration of Malus hupehensis in vitro plantlets. Plant Cell Tiss Organ Cult 96:29–34CrossRefGoogle Scholar
  16. Hayat S, Alyemeni MN, Hasan SA (2012) Foliar spray of brassinosteroid enhances yield and quality of Solanum lycopersicum under cadmium stress. Saudi J Biol Sci 19:325–335CrossRefGoogle Scholar
  17. Hesami M, Daneshvar MH (2018a) In vitro adventitious shoot regeneration through direct and indirect organogenesis from seedling-derived hypocotyl segments of Ficus religiosa L.: an important medicinal plant. HortScience 53:55–61CrossRefGoogle Scholar
  18. Hesami M, Daneshvar MH (2018b) Indirect organogenesis through seedling-derived leaf segments of Ficus religiosa—a multipurpose woody medicinal plant. J Crop Sci Biotechnol 21:129–136CrossRefGoogle Scholar
  19. Hesami M, Daneshvar MH, Lotfi A (2017a) In vitro shoot proliferation through cotyledonary node and shoot tip explants of Ficus religiosa L. Plant Tissue Cult Biotechnol 27:85–88CrossRefGoogle Scholar
  20. Hesami M, Naderi R, Yoosefzadeh-Najafabadi M, Rahmati M (2017b) Data-driven modeling in plant tissue culture. J Appl Environ Biol Sci 7:37–44Google Scholar
  21. Hesami M, Daneshvar MH, Yoosefzadeh-Najafabadi M (2018a) An efficient in vitro shoot regeneration through direct organogenesis from seedling-derived petiole and leaf segments and acclimatization of Ficus religiosa. J For Res.  https://doi.org/10.1007/s11676-018-0647-0 CrossRefGoogle Scholar
  22. Hesami M, Daneshvar MH, Yoosefzadeh-Najafabadi M (2018b) Establishment of a protocol for in vitro seed germination and callus formation of Ficus religiosa L., an important medicinal plant. Jundishapur J Nat Pharm Prod 13(e62682):1–8Google Scholar
  23. Hesami M, Daneshvar MH, Yoosefzadeh-Najafabadi M, Alizadeh M (2018c) Effect of plant growth regulators on indirect shoot organogenesis of Ficus religiosa through seedling derived petiole segments. J Gen Eng Biotechnol 16:175–180CrossRefGoogle Scholar
  24. Jedinák A, Faragó J, Psenakova I, Maliar T (2004) Approaches to flavonoid production in plant tissue cultures. Biologia 59:697–710Google Scholar
  25. Jimenez-Quesada MJ, Carmona R, Lima-Cabello E, Traverso JÁ, Castro AJ, Claros MG, de Dios Alché J (2017) Generation of nitric oxide by olive (Olea europaea L.) pollen during in vitro germination and assessment of the S-nitroso-and nitro-proteomes by computational predictive methods. Nitric Oxide 68:23–37CrossRefGoogle Scholar
  26. Kalra C, Babbar SB (2010) Nitric oxide promotes in vitro organogenesis in Linum usitatissimum L. Plant Cell Tiss Organ Cult 103:353–359CrossRefGoogle Scholar
  27. Ko W, Su C, Chen C, Chao C (2009) Control of lethal browning of tissue culture plantlets of Cavendish banana cv. Formosana with ascorbic acid. Plant Cell Tissue Organ Cult 96:137–141CrossRefGoogle Scholar
  28. Kolbert Z, Bartha B, Erdei L (2008) Exogenous auxin-induced NO synthesis is nitrate reductase-associated in Arabidopsis thaliana root primordia. J Plant Physiol 165:967–975CrossRefGoogle Scholar
  29. Kratsch H, Wise RR (2000) The ultrastructure of chilling stress. Plant, Cell Environ 23:337–350CrossRefGoogle Scholar
  30. Laspina N, Groppa M, Tomaro M, Benavides M (2005) Nitric oxide protects sunflower leaves against Cd-induced oxidative stress. Plant Sci 169:323–330CrossRefGoogle Scholar
  31. Leng P, Su S, Wei F, Yu F, Duan Y (2009) Correlation between browning, total phenolic content, polyphenol oxidase and several antioxidation enzymes during pistachio tissue culture. Acta Hortic Sin 829:127–132CrossRefGoogle Scholar
  32. Ling A, Yap C, Shaib JM, Vilasini P (2007) Induction and morphogenesis of Phalaenopsis callus. J Trop Agric Food Sci 35:147–152Google Scholar
  33. Liu F, Chen L (2010) Redox dynamics during embryogenic callus induction of Phalaenopsis spp. J Wuhan Bot Res 28:737–743Google Scholar
  34. Maggio A, Miyazaki S, Veronese P, Fujita T, Ibeas JI, Damsz B, Narasimhan ML, Hasegawa PM, Joly RJ, Bressan RA (2002) Does proline accumulation play an active role in stress-induced growth reduction? Plant J 31:699–712CrossRefGoogle Scholar
  35. Mayer AM (2006) Polyphenol oxidases in plants and fungi: going places? A review. Phytochemistry 67:2318–2331CrossRefGoogle Scholar
  36. Mittler R (2002) Oxidative stress, antioxidants and stress tolerance. Trends Plant Sci 7:405–410CrossRefGoogle Scholar
  37. Mondal T, Aditya S, Banerjee N (2014) In vitro axillary shoot regeneration and direct protocorm-like body induction from axenic shoot tips of Doritis pulcherrima Lindl. Plant Tissue Cult Biotechnol 23:251–261CrossRefGoogle Scholar
  38. Naz S, Ali A, Iqbal J (2008) Phenolic content in vitro cultures of chick pea (Cicer arietinum L.) during callogenesis and organogenesis. Pak J Bot 40:2525–2539Google Scholar
  39. Neill SJ, Desikan R, Hancock JT (2003) Nitric oxide signalling in plants. New Phytol 159:11–35CrossRefGoogle Scholar
  40. 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 97:330–337CrossRefGoogle Scholar
  41. Nickel KS, Cunningham B (1969) Improved peroxidase assay method using leuco 2, 3′, 6-trichloroindophenol and application to comparative measurements of peroxidatic catalysis. Anal Biochem 27:292–299CrossRefGoogle Scholar
  42. Parani M, Rudrabhatla S, Myers R, Weirich H, Smith B, Leaman DW, Goldman SL (2004) Microarray analysis of nitric oxide responsive transcripts in Arabidopsis. Plant Biotechnol J 2:359–366CrossRefGoogle Scholar
  43. Park S-Y, Shin KS, Paek KY (2006) Increased ethylene and decreased phenolic compounds stimulate somatic embryo regeneration in leaf thin section cultures of Doritaenopsis hybrid. J Plant Biol 49:358–363CrossRefGoogle Scholar
  44. Pitzschke A, Djamei A, Bitton F, Hirt H (2009) A major role of the MEKK1–MKK1/2–MPK4 pathway in ROS signalling. Mol Plant 2:120–137CrossRefGoogle Scholar
  45. Qiao W, Fan LM (2008) Nitric oxide signaling in plant responses to abiotic stresses. Integr Plant Biol 50:1238–1246CrossRefGoogle Scholar
  46. Ramamoorthy V, Raguchander T, Samiyappan R (2002) Induction of defense-related proteins in tomato roots treated with Pseudomonas fluorescens Pf1 and Fusarium oxysporum f. sp. lycopersici. Plant Soil 239:55–68CrossRefGoogle Scholar
  47. Rico-Lemus M, Rodríguez-Garay B (2014) SNP as an effective donor of nitric oxide for in vitro plant cell and tissue culture. J Plant Biochem Physiol 2:127–128CrossRefGoogle Scholar
  48. 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 6:124–132Google Scholar
  49. Sarropoulou V, Maloupa E (2017) Effect of the NO donor “sodium nitroprusside”(SNP), the ethylene inhibitor “cobalt chloride”(CoCl2) and the antioxidant vitamin E “α-tocopherol” on in vitro shoot proliferation of Sideritis raeseri Boiss. & Heldr. subsp. raeseri. Plant Cell Tiss Organ Cult 128:619–629CrossRefGoogle Scholar
  50. 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. Vitro Cell Dev Biol Plant 50:226–234CrossRefGoogle Scholar
  51. Sarropoulou V, Dimassi-Theriou K, Therios I (2016) Effect of the ethylene inhibitors silver nitrate, silver sulfate, and cobalt chloride on micropropagation and biochemical parameters in the cherryrootstocks CAB-6P and Gisela 6. Turk J Biol 40:670–683CrossRefGoogle Scholar
  52. Sharma P, Jha AB, Dubey RS, Pessarakli M (2012) Reactive oxygen species, oxidative damage, and antioxidative defense mechanism in plants under stressful conditions. J Bot 217037:1–26Google Scholar
  53. Singh D, Singh B, Goel RK (2011) Traditional uses, phytochemistry and pharmacology of Ficus religiosa: a review. J Ethnopharmacol 134:565–583CrossRefGoogle Scholar
  54. Tripathy BC, Oelmüller R (2012) Reactive oxygen species generation and signaling in plants. Plant Signal Behav 7:1621–1633CrossRefGoogle Scholar
  55. Tun NN, Holk A, Scherer GF (2001) Rapid increase of NO release in plant cell cultures induced by cytokinin. FEBS Lett 509:174–176CrossRefGoogle Scholar
  56. Uchida A, Jagendorf AT, Hibino T, Takabe T, Takabe T (2002) Effects of hydrogen peroxide and nitric oxide on both salt and heat stress tolerance in rice. Plant Sci 163:515–523CrossRefGoogle Scholar
  57. Velikova V, Yordanov I, Edreva A (2000) Oxidative stress and some antioxidant systems in acid rain-treated bean plants: protective role of exogenous polyamines. Plant Sci 151:59–66CrossRefGoogle Scholar
  58. Wahid A, Gelani S, Ashraf M, Foolad MR (2007) Heat tolerance in plants: an overview. Environ Exp Bot 61:199–223CrossRefGoogle Scholar
  59. Wang X-D, Nolan KE, Irwanto RR, Sheahan MB, Rose RJ (2011) Ontogeny of embryogenic callus in Medicago truncatula: the fate of the pluripotent and totipotent stem cells. Ann Bot 107:599–609CrossRefGoogle Scholar
  60. Wi SG, Chung BY, Kim J-H, Baek M-H, Yang DH, Lee J-W, Kim J-S (2005) Ultrastructural changes of cell organelles in Arabidopsis stems after gamma irradation. J Plant Biol 48:195–200CrossRefGoogle Scholar
  61. Xu CJ, Li L, Li H, Zhang M (2005) Preliminary studies on the elements of browning and the changes in cellular texture of leaf explant browning in Phalaenopsis. Acta Hortic Sin 32:1111–1113Google Scholar
  62. Xu J, Yin H, Wang W, Mi Q, Liu X (2009) Effects of sodium nitroprusside on callus induction and shoot regeneration in micropropagated Dioscorea opposita. Plant Growth Regul 59:279–285CrossRefGoogle Scholar
  63. Yingsanga P, Srilaong V, Kanlayanarat S, Noichinda S, McGlasson W (2008) Relationship between browning and related enzymes (PAL, PPO and POD) in rambutan fruit (Nephelium lappaceum Linn.) cvs. Rongrien and See-Chompoo. Postharvest Biol Technol 50:164–168CrossRefGoogle Scholar
  64. Yoruk R, Marshall MR (2003) Physicochemical properties and function of plant polyphenol oxidase: a review. J Food Biochem 27:361–422CrossRefGoogle Scholar
  65. Zamani M, Hakimi M, Mosleh Arany A, Kiani B, Rashtian A (2014) The effects of salicylic acid (SA) and sodium nitroprusside (SNP) on physical and growth characteristics of Pinus eldarica. Bull Environ Pharmacol Life Sci 3:31–35Google Scholar

Copyright information

© Northeast Forestry University 2018

Authors and Affiliations

  • Mohsen Hesami
    • 1
  • Masoud Tohidfar
    • 2
  • Milad Alizadeh
    • 2
  • Mohammad Hosein Daneshvar
    • 3
  1. 1.Department of Horticultural Science, Faculty of AgricultureUniversity of TehranKarajIran
  2. 2.Department of Plant Biotechnology, Faculty of Life Science and BiotechnologyShahid Beheshti UniversityTehranIran
  3. 3.Department of Horticultural Science, Faculty of AgricultureKhuzestan Agricultural Sciences and Natural Resources UniversityMollasaniIran

Personalised recommendations