Responses of in vitro-cultured Allium hirtifolium to exogenous sodium nitroprusside under PEG-imposed drought stress

  • K. Ghassemi-Golezani
  • N. Farhadi
  • N. Nikpour-Rashidabad
Original Article
  • 145 Downloads

Abstract

Drought stress is a major threat to plant production in semi-arid and arid areas of the world. This research was laid out to asses the effects of sodium nitroprusside (SNP) as a nitric oxide donor on growth, physiological and biochemical changes of in vitro-cultured Allium hirtifolium under polyethylene glycol (PEG) induced drought stress. Basal plate explants of A. hirtifolium were cultured on MS medium containing different levels of PEG (0, 2, 4, 8 and 16 mM) and SNP (0, 10, 40 and 70 µM). After prolonged drought, growth responses, oxidative stress indicators, and phytochemical variations of regenerated plantlets with or without PEG and/or SNP treatments were recorded. Water limitation reduced regeneration potential of explants and consequently number of shoots per explant. Relative water content, total chlorophyll and carotenoid contents of regenerated A. hirtifolium plantlets decreased, but accumulation of malondialdehyde, H2O2 and proline and the activities of superoxide dismutase, ascorbate peroxidase, catalase and peroxidase enzymes increased with decreasing water availability. Total phenol and allicin contents were also increased in response to drought stress. Exogenous SNP in 10 and particularly in 40 µM was effective in enhancing regeneration rate and relative water content as well as protecting photosynthetic pigments under different levels of water availability. SNP also inhibited the hydrogen peroxide (H2O2) accumulation and lipid peroxidation in cell membranes via increasing the activities of superoxide dismutase and ascorbate peroxidase enzymes and accumulating proline and allicin. In general, these results suggest that exogenous SNP at 40 µM not only could somewhat protect A. hirtifolium from drought stress, but also can help to improve the propagation and allicin production of that plant under in vitro condition.

Keywords

Allicin Antioxidant enzyme Carotenoid Chlorophyll Phenol Proline 

Abbreviations

APX

Ascorbate peroxidase

CAT

Catalase

NO

Nitric oxide

PEG

Polyethylene glycol

POX

Peroxidase

PGR

Plant growth regulator

ROS

Reactive oxygen species

RWC

Relative water content

SNP

Sodium nitroprusside

MDA

Malondialdehyde

SOD

Superoxide dismutase

Notes

Acknowledgements

We appreciate the financial support of this work by the University of Tabriz.

Author contributions

The publication of this article is approved by all authors and explicitly by the responsible authorities where the work was carried out.

Compliance with ethical standards

Conflict of interest

We have no conflicts of interest to disclose.

References

  1. Aazami MA, Torabi M, Jalili E (2010) In vitro response of promising tomato genotypes for tolerance to osmotic stress. Afr J Biotechnol 9:4014–4017.  https://doi.org/10.5897/AJB10.1452 Google Scholar
  2. Aebi H (1983) Catalase. In: Bergmeyer H (ed) Methods of enzymatic analysis, vol. 3. Wiley, Weinheim, pp 273–277Google Scholar
  3. Ahmad MA, Murali PV, Marimuthu G (2014) Impact of salicylic acid on growth, photosynthesis and compatible solute accumulation in Allium cepa L. subjected to drought stress. Int J Res Agric Food Sci 4:22–30Google Scholar
  4. Asili A, Behravan J, Naghavi MR, Asili J (2010) Genetic diversity of Persian shallot (Allium hirtifolium) ecotypes based on morphological traits, allicin content and RAPD markers. Med Aromat Plants 1:1–6Google Scholar
  5. Barrs HD, Weatherley PE (1962) A re-examination of the relative turgidity technique for estimating water deficits in leaves. Aust J Biol Sci 15:413–428CrossRefGoogle Scholar
  6. Bates LE, Waldren RP, Teare ID (1973) Rapid determination of free proline for water stress studies. Plant Soil 39:205–207CrossRefGoogle Scholar
  7. Bettaieb I, Hamrouni-Sellami I, Bourgou S, Limam F, Marzouk B (2011) Drought effects on polyphenol composition and antioxidant activities in aerial parts of Salvia officinalis L. Acta Physiol Plant 33:1103–1111.  https://doi.org/10.1007/s11738-010-0638-z CrossRefGoogle Scholar
  8. Bradford MM (1976) A rapid and sensitive method for the quantification of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Chem 72:248–254Google Scholar
  9. Bray EA (1997) Plant responses to water deficit. Trends Plant Sci 2:48–54CrossRefGoogle Scholar
  10. Cakmak I, Horst J (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
  11. Cechin I, Cardoso GS, Fumis TF, Corniani N (2015) Nitric oxide reduces oxidative damage induced by water stress in sunflower plants. Plant Prot 74:200–206.  https://doi.org/10.1590/1678-4499.353 Google Scholar
  12. Chance B, Maehly AC (1955) Assay of catalases and peroxidases. In: Collowick SP, Kapplan NO (eds) Methods in enzymology, vol. 2. Academic Press, New York, pp 764–775Google Scholar
  13. Csiszar J, Lantos E, Tari I, Madosa E, Wodala B, Vashegyi A, Horvath F, Pecsvaradi A, Szabo M, Bartha B, Galle A, Lazar A, Coradini G, Staicu M, Postelnicu S, Mihacea S, Nedelea G, Erdei L (2007) Antioxidant enzyme activities in Allium species and their cultivars under water stress. Plant Soil Environ 53:517–523CrossRefGoogle Scholar
  14. Elmaghrabi AM, Rogers HJ, Francis D, Ochatt SJ (2017) PEG induces high expression of the cell cycle checkpoint gene WEE1 in embryogenic callus of Medicago truncatula: potential link between cell cycle checkpoint regulation and osmotic stress. Front Plant Sci 8:1479.  https://doi.org/10.3389/fpls.2017.01479 CrossRefPubMedPubMedCentralGoogle Scholar
  15. Farhadi N, Panahandeh J, Motallebi Azar A, Alizadeh Salte S (2017) Effects of explant type, growth regulators and light intensity on callus induction and plant regeneration in four ecotypes of Persian shallot (Allium hirtifolium). Sci Hort 218:80–86.  https://doi.org/10.1016/j.scienta.2016.11.056 CrossRefGoogle Scholar
  16. Farooq M, Wahid A, Kobayashi N, Fujita D, Basra SMA (2009) Plant drought stress: effects, mechanisms and management. Agron Sustain Dev 29:185–212.  https://doi.org/10.1051/agro:2008021 CrossRefGoogle Scholar
  17. Freschi L (2013) Nitric oxide and phytohormone interactions: current status and perspectives. Front Plant Sci 4:1–22.  https://doi.org/10.3389/fpls.2013.00398 CrossRefGoogle Scholar
  18. Giannopolitis C, Ries S (1977) Superoxide dismutase. I. Occurrence in higher plants. Plant Physiol 59:309–314CrossRefPubMedPubMedCentralGoogle Scholar
  19. Gill SS, Tuteja N (2010) Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiol Biochem 48:909–930CrossRefPubMedGoogle Scholar
  20. Hao GP, Du XH, Hai RJ (2007) Exogenous nitric oxide accelerates soluble sugar, proline and secondary metabolite synthesis in Ginkgo biloba under drought stress. Physiol Mol Biol Plants 33:499–506Google Scholar
  21. Hassan HAM, Haiping W, Xinyan L, Xixiang L (2015) Impact of genetic factor and geographical location on allicin content of garlic (Allium sativum) germplasm from Egypt and China. Int J Agric Biol 17:156–162Google Scholar
  22. Hayat S, Yadav S, Wani AS, Irfan M, Ahmad A (2011) Nitric oxide effects on photosynthetic rate growth, and antioxidant activity in tomato. Int J Veg Sci 17:333–348.  https://doi.org/10.1080/19315260.2011.563275 CrossRefGoogle Scholar
  23. Iberl B, Winkler G, Muller B, Knobloch K (1990) Quantitative determination of allicin and alliin from garlic by HPLC. Planta Med 56:320–326CrossRefPubMedGoogle Scholar
  24. Ismail S, Jalilian FA, Talebpour AH, Zargar M, Shameli K, Sekawi Z (2012) Chemical composition and antibacterial and cytotoxic activities of Allium hirtifolium Boiss. Bio Med Res Int 2013:696–835.  https://doi.org/10.1155/2013/696835 Google Scholar
  25. Jariteh M, Ebrahimzadeh H, Niknam V, Mirmasoumi M, Vahdati K (2015) Developmental changes of protein, proline and some antioxidant enzymes activities in somatic and zygotic embryos of Persian walnut (Juglans regia L.). Plant Cell Tiss Organ Cult 122:101–115.  https://doi.org/10.1007/s11240-015-0753-z CrossRefGoogle Scholar
  26. Kielkowska A, Adamus A, Oleksyk A (2012) In vitro selection of Allium cepa for water stress. Proc. 6th IS on Edible Alliaceae Acta Hort. ISHS, 969:117–120Google Scholar
  27. Kovacs I, Lindermayr C (2013) Nitric oxide-based protein modification: formation and site-specificity of protein S-nitrosylation. Front Plant Sci 4:1–10.  https://doi.org/10.3389/fpls.2013.00137 Google Scholar
  28. Li J-B, Luan Y-S, Liu Z (2015) SpWRKY1 mediates resistance to Phytophthora infestans and tolerance to salt and drought stress by modulating reactive oxygen species homeostasis and expression of defense-related genes in tomato. Plant Cell Tiss Organ Cult 123:67–81.  https://doi.org/10.1007/s11240-015-0815-2 CrossRefGoogle Scholar
  29. Liao WB, Huang GB, Yu JH, Zhang ML (2012) Nitric oxide and hydrogen peroxide alleviate drought stress in marigold explants and promote its adventitious root development. Plant Physiol Biochem 58:6–15.  https://doi.org/10.1016/j.plaphy.2012.06.012 CrossRefPubMedGoogle Scholar
  30. Lichtenthaler HK (1987) Chlorophylls and carotenoids: pigments of photosynthetic biomembranes. Methods Enzymol 148:350–382CrossRefGoogle Scholar
  31. Liu F, Guo FQ (2013) Nitric oxide deficiency accelerates chlorophyll breakdown and stability loss of thylakoid membranes during dark-induced leaf senescence in Arabidopsis. Plos One 8:e56345.  https://doi.org/10.1371/journal.pone.0056345 CrossRefPubMedPubMedCentralGoogle Scholar
  32. 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 31:699–712.  https://doi.org/10.1046/j.1365-313X.2002.01389.x CrossRefPubMedGoogle Scholar
  33. Mahboubi M, Kazempour N (2015) The anti-dermatophyte activity of Allium hirtifolium Boiss aqueous extract. J Mycol Med 25:e10–e14.  https://doi.org/10.1016/j.mycmed.2014.10.010 CrossRefPubMedGoogle Scholar
  34. Manuel Beato V, Orgaz F, Mansilla F, Montano A (2011) Changes in phenolic compounds in garlic (Allium sativum L.) owing to the cultivar and location of growth. Plant Foods Hum Nutr 66:218–223.  https://doi.org/10.1007/s11130-011-0236-2 CrossRefGoogle Scholar
  35. Mozafari A, Havas F, Ghaderi N (2017) Application of iron nanoparticles and salicylic acid in in vitro culture of strawberries (Fragaria × ananassa Duch.) to cope with drought stress. Plant Cell Tiss Organ Cult.  https://doi.org/10.1007/s11240-017-1347-8 Google Scholar
  36. Murashige T, Skoog F (1962) A revised medium for rapid growth and bioassays with tobacco tissue culture. Physiol Plant 15:473–497CrossRefGoogle Scholar
  37. Nakano Y, Asada K (1981) Hydrogen peroxide is scavenged by ascorbate-specific peroxidase in spinach chloroplasts. Plant Cell Physiol 22:867–880Google Scholar
  38. Nalousi AM, Ahmadiyan S, Hatamzadeh A, Ghasemnezhad M (2013) Protective role of exogenous nitric oxide against oxidative stress induced by salt stress in bell-pepper (Capsicum annum L.). Am Eurasian J Agric Environ Sci 8:1085–1090.  https://doi.org/10.5829/idosi.aejaes.2012.12.08.1938 Google Scholar
  39. Nazar R, Umar S, Khan NA, Sareer O (2015) Salicylic acid supplementation improves photosynthesis and growth in mustard through changes in proline accumulation and ethylene formation under drought stress. S Afr J Bot 98:84–94.  https://doi.org/10.1016/j.sajb.2015.02.005 CrossRefGoogle Scholar
  40. Otvos K, Pasternak TP, Miskolczi P, Domoki M, Dorjgotov D, Szucs A, Bottka S, Dudits D, Feher A (2005) Nitric oxide is required for, and promotes auxin-mediated activation of, cell division and embryogenic cell formation but does not influence cell cycle progression in alfafa cell cultures. Plant J 43:849–860.  https://doi.org/10.1111/j.1365-313X.2005.02494.x CrossRefPubMedGoogle Scholar
  41. Pérez-Clemente RM, Gómez-Cadenas A (2012) In vitro tissue culture, a tool for the study and breeding of plants subjected to abiotic stress conditions. In: Leva A, Rinaldi LMR (eds) Recent advances in plant in vitro culture. Intech Open Access Publisher, Rijeka, pp 91–108Google Scholar
  42. Piwowarczyk B, Kamińska I, Rybiński W (2014) Influence of PEG generated osmotic stress on shoot regeneration and some biochemical parameters in Lathyrus culture. Czech J Genet Plant Breed 50:77–83CrossRefGoogle Scholar
  43. Qiao W, Fan LM (2008) Nitric oxide signaling in plant responses to abiotic stresses. J Integr Plant Biol 50:1238–1246.  https://doi.org/10.1111/j.1744-7909.2008.00759.x CrossRefPubMedGoogle Scholar
  44. Rahimian Boogar A, Salehi H, Jowkar A (2014) Exogenous nitric oxide alleviates oxidative damage in turf grasses under drought stress. S Afr J Bot 92:78–82.  https://doi.org/10.1016/j.sajb.2014.02.005 CrossRefGoogle Scholar
  45. Rao S, FTZ J (2013) In vitro selection and characterization of polyethylene glycol (PEG) tolerant callus lines and regeneration of plantlets from the selected callus lines in sugarcane (Saccharum officinarum L.). Physiol Mol Biol Plants 19:261–268.  https://doi.org/10.1007/s12298-013-0162-x CrossRefPubMedPubMedCentralGoogle Scholar
  46. Santisree P, Bhatnagar-Mathur P, Sharma KK (2015) NO to drought-multifunctional role of nitric oxide in plant drought: do we have all the answers? Plant Sci 239:44–55.  https://doi.org/10.1016/j.plantsci.2015.07.012 CrossRefPubMedGoogle Scholar
  47. 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 128:619–629.  https://doi.org/10.1007/s11240-016-1139-6 CrossRefGoogle Scholar
  48. Shallan MA, Hassan HMM, Namich AAM, Ibrahim AA Eurasian (2012) Effect of sodium niroprusside, putrescine and glycine betaine on alleviation of drought stress in Cotton plant. American-. J Agric Environ Sci 12:1252–1265.  https://doi.org/10.5829/idosi.aejaes.2012.12.09.1902 Google Scholar
  49. Siddiqui MH, Al-Whaibi MH, Basalah MO (2011) Role of nitric oxide in tolerance of plants to abiotic stress. Protoplasma 248:447–455.  https://doi.org/10.1007/s00709-010-0206-9 CrossRefPubMedGoogle Scholar
  50. Slinkard K, Singleton VL (1977) Total phenol analyses: automation and comparison with manual methods. Am J Enol Vitic 28:49–55Google Scholar
  51. Taran M, Izaddoost M (2010) Nematocidal activity of Allium hirtifolium (Persian shallot) against Rhabditis sp. Vet Res 3:27–28.  https://doi.org/10.3923/vr.2010.27.28 Google Scholar
  52. Tubic L, Savic J, Mitic N, Milojevic J, Janosevic D, Budimir S, Zdravkovic-Korac S (2016) Cytokinins differentially affect regeneration, plant growth and antioxidative enzymes activity in chive (Allium schoenoprasum L.). Plant Cell Tiss Organ Cult 124:1–14.  https://doi.org/10.3389/fpls.2017.01479 CrossRefGoogle Scholar
  53. Velikova V, Yordanov I, Edreva A (2000) Oxidative stress and some antioxidant system in acid rain treated bean plants: protective role of exogenous poly ammines. Plant Sci 151:59–66.  https://doi.org/10.1016/S0168-9452(99)00197-1 CrossRefGoogle Scholar
  54. Xu J, Yin H, Wang W, Mi Q, Liu X (2009) Effects of sodium nitroprusside on callus induction and shoot regeneration in micropropagated Dioscorea opposite. Plant Growth Regul 59:279–285.  https://doi.org/10.1007/s10725-009-9410-z CrossRefGoogle Scholar
  55. Yuan Y, Qi L, Yang J, Wu C, Liu Y, Huang L (2015) A Scutellaria baicalensis R2R3-MYB gene, SbMYB8, regulates flavonoid biosynthesis and improves drought stress tolerance in transgenic tobacco. Plant Cell Tiss Organ Cult 120:961–972.  https://doi.org/10.1007/s11240-014-0650-x CrossRefGoogle Scholar

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Authors and Affiliations

  1. 1.Department of Plant Eco-physiology, Faculty of AgricultureUniversity of TabrizTabrizIran
  2. 2.Department of Horticulture, Faculty of AgricultureUniversity of TabrizTabrizIran

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