Advertisement

Effect of Salinity Stress on Enzymes’ Activity, Ions Concentration, Oxidative Stress Parameters, Biochemical Traits, Content of Sulforaphane, and CYP79F1 Gene Expression Level in Lepidium draba Plant

  • Kiarash Jamshidi GoharriziEmail author
  • Ali Riahi-Madvar
  • Fatemeh Rezaee
  • Rambod Pakzad
  • Fereshteh Jadid Bonyad
  • Mahshid Ghazizadeh Ahsaei
Article
  • 14 Downloads

Abstract

In the first step in this study, the effect of 50 mM NaCl was studied on germination percentage of five different Lepidium draba (L. draba) ecotypes, and Rafsanjan ecotype was selected as experimental material as it had the highest germination percentage. In the second step, some biochemical, physiological, and morphological traits along with content of sulforaphane (SFN) as well as the expression level of Cytochorome P450 79F1 (CYP79F1) were evaluated in 14-day-old L. draba sprouts that grew 9 days in the presence of various concentrations of NaCl including 0, 25, 50, 75, and 100 mM. According to the results of this study, germination percentage of Rafsanjan ecotype along with lengths of stem and root were declined with increasing concentrations of NaCl. Ascorbate peroxidase, guaiacol peroxidase, and superoxide dismutase enzymes activity increased up to 75 mM NaCl and then decreased. With increasing the doses of NaCl, concentrations of Na+ and Cl increased, whereas P, Ca2+, and K+ decreased. Also, accumulation of some oxidative stress parameters including electrolyte leakage, malondialdehyde, other aldehydes, and hydrogen peroxide increased with increasing NaCl concentrations in all samples. Furthermore, contents of total phenolic, total flavonoid, total anthocyanin, total free amino acids, and total soluble carbohydrate were induced with the induction of NaCl concentrations. In this study, SFN formation increased with increasing concentration of sodium chloride up to 75 mM and decreased at higher concentration. In the last step, a partial CYP79F1 mRNA and its protein sequence were identified and registered in GenBank and then changes in the CYP79F1 gene expression levels under 0, 25, 50, 75, and 100 mM NaCl were calculated. The gene expression levels of CYP79F1 also showed the same pattern as was seen for SFN formation under salinity stress.

Keywords

L. draba Sulforaphane CYP79F1 Oxidative stress Biochemical traits Ions concentration 

Notes

Acknowledgements

The authors gratefully acknowledge the Barafza Keshavarz Pars Company for financial support.

Compliance with Ethical Standards

Conflict of interest

The authors declare no conflict of interest.

References

  1. Abogadallah GM (2010) Insights into the significance of antioxidative defense under salt stress. Plant Signal Behav 5(4):369–374.  https://doi.org/10.4161/psb.5.4.10873 CrossRefPubMedPubMedCentralGoogle Scholar
  2. Ahmad P, Jaleel CA, Salem MA, Nabi G, Sharma S (2010a) Roles of enzymatic and nonenzymatic antioxidants in plants during abiotic stress. Crit Rev Biotechnol 30(3):161–175.  https://doi.org/10.3109/07388550903524243 CrossRefPubMedGoogle Scholar
  3. Ahmad P, Jaleel CA, Sharma S (2010b) Antioxidant defense system, lipid peroxidation, proline-metabolizing enzymes, and biochemical activities in two Morus alba genotypes subjected to NaCl stress. Russ J Plant Physiol 57(4):509–517.  https://doi.org/10.1134/S1021443710040084 CrossRefGoogle Scholar
  4. Ahmad P, Ozturk M, Sharma S, Gucel S (2014) Effect of sodium carbonate-induced salinity–alkalinity on some key osmoprotectants, protein profile, antioxidant enzymes, and lipid peroxidation in two mulberry (Morus alba L.) cultivars. J Plant Interact 9(1):460–467.  https://doi.org/10.1080/17429145.2013.855271 CrossRefGoogle Scholar
  5. Ahmad P, Hashem A, Abd-Allah EF, Alqarawi AA, John R, Egamberdieva D, Gucel S (2015) Role of Trichoderma harzianum in mitigating NaCl stress in Indian mustard (Brassica juncea L.) through antioxidative defense system. Front Plant Sci 6:868.  https://doi.org/10.3389/fpls.2015.00868 CrossRefPubMedPubMedCentralGoogle Scholar
  6. Ahmad P, Abdel Latef AA, Hashem A, Abd Allah EF, Gucel S, Tran L-SP (2016) Nitric oxide mitigates salt stress by regulating levels of osmolytes and antioxidant enzymes in chickpea. Front Plant Sci 7:347–347.  https://doi.org/10.3389/fpls.2016.00347 CrossRefPubMedPubMedCentralGoogle Scholar
  7. Ahmad P, Ahanger MA, Alyemeni MN, Wijaya L, Egamberdieva D, Bhardwaj R, Ashraf M (2017) Zinc application mitigates the adverse effects of NaCl stress on mustard [Brassica juncea (L.) Czern & Coss] through modulating compatible organic solutes, antioxidant enzymes, and flavonoid content. J Plant Interact 12(1):429–437.  https://doi.org/10.1080/17429145.2017.1385867 CrossRefGoogle Scholar
  8. Ahmad P, Abass Ahanger M, Nasser Alyemeni M, Wijaya L, Alam P, Ashraf M (2018) Mitigation of sodium chloride toxicity in Solanum lycopersicum L. by supplementation of jasmonic acid and nitric oxide. J Plant Interact 13(1):64–72.  https://doi.org/10.1080/17429145.2017.1420830 CrossRefGoogle Scholar
  9. Ahmad P, Ahanger MA, Alam P, Alyemeni MN, Wijaya L, Ali S, Ashraf M (2019) Silicon (Si) supplementation alleviates NaCl toxicity in Mung bean [Vigna radiata (L.) Wilczek] through the modifications of physio-biochemical attributes and key antioxidant enzymes. J Plant Growth Regul 38(1):70–82.  https://doi.org/10.1007/s00344-018-9810-2 CrossRefGoogle Scholar
  10. Akbari M, Mahna N, Ramesh K, Bandehagh A, Mazzuca S (2018) Ion homeostasis, osmoregulation, and physiological changes in the roots and leaves of pistachio rootstocks in response to salinity. Protoplasma 255(5):1349–1362.  https://doi.org/10.1007/s00709-018-1235-z CrossRefPubMedGoogle Scholar
  11. Almansouri M, Kinet JM, Lutts S (2001) Effect of salt and osmotic stresses on germination in durum wheat (Triticum durum Desf.). Plant Soil 231(2):243–254.  https://doi.org/10.1023/A:1010378409663 CrossRefGoogle Scholar
  12. Almodares A, Hadi M, Dosti B (2007) Effects of salt stress on germination percentage and seedling growth in sweet sorghum cultivars. J Biol Sci 7(8):1492–1495.  https://doi.org/10.3923/jbs.2007.1492.1495 CrossRefGoogle Scholar
  13. Amirjani MR (2011) Effect of salinity stress on growth, sugar content, pigments and enzyme activity of rice. Int J Bot 7(1):73–81CrossRefGoogle Scholar
  14. Amtmann A, Sanders D (1998) Mechanisms of Na+ uptake by plant cells. In: Callow JA (ed) Advances in botanical research, vol 29. Academic Press, New York, pp 75–112.  https://doi.org/10.1016/S0065-2296(08)60310-9 CrossRefGoogle Scholar
  15. Asada K, Nakano Y (1981) Hydrogen peroxide is scavenged by ascorbate-specific peroxidase in spinach chloroplasts. Plant Cell Physiol 22(5):867–880.  https://doi.org/10.1093/oxfordjournals.pcp.a076232 CrossRefGoogle Scholar
  16. Ashraf M (2009) Biotechnological approach of improving plant salt tolerance using antioxidants as markers. Biotechnol Adv 27(1):84–93.  https://doi.org/10.1016/j.biotechadv.2008.09.003 CrossRefPubMedGoogle Scholar
  17. Ashraf M, Ali Q (2008) Relative membrane permeability and activities of some antioxidant enzymes as the key determinants of salt tolerance in canola (Brassica napus L). Environ Exp Bot 63(1):266–273.  https://doi.org/10.1016/j.envexpbot.2007.11.008 CrossRefGoogle Scholar
  18. Bahrani A (2013) Effect of salinity on growth, ions distribution, accumulation and chlorophyll concentrations in two canola (Brassica napus L.) cultivars. Am-Eurasian J Agric Environ Sci 13(5):683–689.  https://doi.org/10.5829/idosi.wasj.2013.27.08.642 CrossRefGoogle Scholar
  19. Bai X, Yang L, Yang Y, Ahmad P, Yang Y, Hu X (2011) Deciphering the protective role of nitric oxide against salt stress at the physiological and proteomic levels in maize. J Proteome Res 10(10):4349–4364.  https://doi.org/10.1021/pr200333f CrossRefPubMedGoogle Scholar
  20. Biddulph TB, Plummer JA, Setter TL, Mares DJ (2007) Influence of high temperature and terminal moisture stress on dormancy in wheat (Triticum aestivum L.). Field Crops Res 103(2):139–153.  https://doi.org/10.1016/j.fcr.2007.05.005 CrossRefGoogle Scholar
  21. Borek V, Elberson LR, McCaffrey JP, Morra MJ (1998) Toxicity of isothiocyanates produced by glucosinolates in Brassicaceae species to black vine weevil eggs. J Agric Food Chem 46(12):5318–5323.  https://doi.org/10.1021/jf9805754 CrossRefGoogle Scholar
  22. Bose J, Shabala S, Rodrigo-Moreno A (2013) ROS homeostasis in halophytes in the context of salinity stress tolerance. J Exp Bot 65(5):1241–1257.  https://doi.org/10.1093/jxb/ert430 CrossRefPubMedGoogle Scholar
  23. Bouchabke O, Tardieu F, Simonneau T (2006) Leaf growth and turgor in growing cells of maize (Zea mays L.) respond to evaporative demand under moderate irrigation but not in water-saturated soil. Plant Cell Environ 29(6):1138–1148.  https://doi.org/10.1111/j.1365-3040.2005.01494.x CrossRefPubMedGoogle Scholar
  24. Buer CS, Imin N, Djordjevic MA (2010) Flavonoids: new roles for old molecules. J Integr Plant Biol 52(1):98–111.  https://doi.org/10.1111/j.1744-7909.2010.00905.x CrossRefPubMedGoogle Scholar
  25. Cavalcanti FR, Oliveira JTA, Martins-Miranda AS, Viégas RA, Silveira JAG (2004) Superoxide dismutase, catalase and peroxidase activities do not confer protection against oxidative damage in salt-stressed cowpea leaves. New Phytol 163(3):563–571.  https://doi.org/10.1111/j.1469-8137.2004.01139.x CrossRefGoogle Scholar
  26. Chen S, Petersen BL, Olsen CE, Schulz A, Halkier BA (2001) Long-distance phloem transport of glucosinolates in Arabidopsis. Plant Physiol 127(1):194–201.  https://doi.org/10.1104/pp.127.1.194 CrossRefPubMedPubMedCentralGoogle Scholar
  27. Chen KM, Gong HJ, Chen GC, Wang SM, Zhang CL (2003a) Up-regulation of glutathione metabolism and changes in redox status involved in adaptation of reed (Phragmites communis) ecotypes to drought-prone and saline habitats. J Plant Physiol 160(3):293–301.  https://doi.org/10.1078/0176-1617-00927 CrossRefPubMedGoogle Scholar
  28. Chen S, Glawischnig E, Jørgensen K, Naur P, Jørgensen B, Olsen CE, Hansen CH, Rasmussen H, Pickett JA, Halkier BA (2003b) CYP79F1 and CYP79F2 have distinct functions in the biosynthesis of aliphatic glucosinolates in Arabidopsis. Plant J 33(5):923–937.  https://doi.org/10.1046/j.1365-313X.2003.01679.x CrossRefPubMedGoogle Scholar
  29. Chun OK, Kim DO, Lee CY (2003) Superoxide radical scavenging activity of the major polyphenols in fresh plums. J Agric Food Chem 51(27):8067–8072.  https://doi.org/10.1021/jf034740d CrossRefPubMedGoogle Scholar
  30. Clarke JD, Dashwood RH, Ho E (2008) Multi-targeted prevention of cancer by sulforaphane. Cancer Lett 269(2):291–304.  https://doi.org/10.1016/j.canlet.2008.04.018 CrossRefPubMedPubMedCentralGoogle Scholar
  31. Cusido RM, Palazon J, Altabella T, Morales C (1987) Effect of salinity on soluble protein, free amino acids and nicotine contents in Nicotiana rustica L. Plant Soil 102(1):55–60.  https://doi.org/10.1007/BF02370900 CrossRefGoogle Scholar
  32. Czegeny G, Wu M, Der A, Eriksson LA, Strid A, Hideg E (2014) Hydrogen peroxide contributes to the ultraviolet-B (280–315 nm) induced oxidative stress of plant leaves through multiple pathways. FEBS Lett 588(14):2255–2261.  https://doi.org/10.1016/j.febslet.2014.05.005 CrossRefPubMedGoogle Scholar
  33. Davies KJ (1987) Protein damage and degradation by oxygen radicals I. General aspects. J Biol Chem 262(20):9895–9901PubMedGoogle Scholar
  34. de Azevedo Neto AD, Prisco JT, Enéas-Filho J, Abreu CEBd, Gomes-Filho E (2006) Effect of salt stress on antioxidative enzymes and lipid peroxidation in leaves and roots of salt-tolerant and salt-sensitive maize genotypes. Environ Exp Bot 56(1):87–94.  https://doi.org/10.1016/j.envexpbot.2005.01.008 CrossRefGoogle Scholar
  35. Devi JR, Thangam EB (2012) Mechanisms of anticancer activity of sulforaphane from Brassica oleracea in HEp-2 human epithelial carcinoma cell line. Asian Pac J Cancer Prev 13(5):2095–2100.  https://doi.org/10.7314/APJCP.2012.13.5.2095 CrossRefPubMedGoogle Scholar
  36. Donohue K, Heschel MS, Butler CM, Barua D, Sharrock RA, Whitelam GC, Chiang GC (2008) Diversification of phytochrome contributions to germination as a function of seed-maturation environment. New Phytol 177(2):367–379.  https://doi.org/10.1111/j.1469-8137.2007.02281.x CrossRefPubMedGoogle Scholar
  37. Duan J, Li J, Guo S, Kang Y (2008) Exogenous spermidine affects polyamine metabolism in salinity-stressed Cucumis sativus roots and enhances short-term salinity tolerance. J Plant Physiol 165(15):1620–1635.  https://doi.org/10.1016/j.jplph.2007.11.006 CrossRefPubMedGoogle Scholar
  38. Dubey RS, Singh AK (1999) Salinity induces accumulation of soluble sugars and alters the activity of sugar metabolising enzymes in rice plants. Biol Plant 42(2):233–239.  https://doi.org/10.1023/A:1002160618700 CrossRefGoogle Scholar
  39. Eraslan F, Inal A, Pilbeam DJ, Gunes A (2008) Interactive effects of salicylic acid and silicon on oxidative damage and antioxidant activity in spinach (Spinacia oleracea L. cv. Matador) grown under boron toxicity and salinity. Plant Growth Regul 55(3):207.  https://doi.org/10.1007/s10725-008-9277-4 CrossRefGoogle Scholar
  40. Fahey JW, Zalcmann AT, Talalay P (2001) The chemical diversity and distribution of glucosinolates and isothiocyanates among plants. Phytochemistry 56(1):5–51.  https://doi.org/10.1016/S0031-9422(00)00316-2 CrossRefPubMedGoogle Scholar
  41. Fahey JW, Haristoy X, Dolan PM, Kensler TW, Scholtus I, Stephenson KK, Talalay P, Lozniewski A (2002) Sulforaphane inhibits extracellular, intracellular, and antibiotic-resistant strains of Helicobacter pylori and prevents benzo [a] pyrene-induced stomach tumors. Proc Natl Acad Sci 99(11):7610–7615.  https://doi.org/10.1073/pnas.112203099 CrossRefPubMedGoogle Scholar
  42. Fattahi S, Ardekani AM, Zabihi E, Abedian Z, Mostafazadeh A, Pourbagher R, Akhavan-Niaki H (2013) Antioxidant and apoptotic effects of an aqueous extract of Urtica dioica on the MCF-7 human breast cancer cell line. Asian Pac J Cancer Prev 14(9):5317–5323.  https://doi.org/10.7314/APJCP.2013.14.9.5317 CrossRefPubMedGoogle Scholar
  43. Fattahi S, Zabihi E, Abedian Z, Pourbagher R, Motevalizadeh Ardekani A, Mostafazadeh A, Akhavan-Niaki H (2014) Total phenolic and flavonoid contents of aqueous extract of stinging nettle and in vitro antiproliferative effect on hela and BT-474 cell lines. Int J Mol Cell Med 3(2):102–107PubMedPubMedCentralGoogle Scholar
  44. Feyereisen R (1999) Insect P450 enzymes. Annu Rev Entomol 44:507–533.  https://doi.org/10.1146/annurev.ento.44.1.507 CrossRefPubMedGoogle Scholar
  45. Foyer CH, Noctor G (2005) Oxidant and antioxidant signalling in plants: a re-evaluation of the concept of oxidative stress in a physiological context. Plant Cell Environ 28(8):1056–1071.  https://doi.org/10.1111/j.1365-3040.2005.01327.x CrossRefGoogle Scholar
  46. Fridovich I (1986) Biological effects of the superoxide radical. Arch Biochem Biophys 247(1):1–11.  https://doi.org/10.1016/0003-9861(86)90526-6 CrossRefPubMedGoogle Scholar
  47. Gautam M, Ge X-H, Li Z-Y (2014) Brassica. In: Pratap A, Kumar J (eds) Alien gene transfer in crop plants: achievements and impacts, vol 2. Springer, New York, pp 207–229.  https://doi.org/10.1007/978-1-4614-9572-7_10 CrossRefGoogle Scholar
  48. Gengmao Z, Yu H, Xing S, Shihui L, Quanmei S, Changhai W (2015) Salinity stress increases secondary metabolites and enzyme activity in safflower. Ind Crops Prod 64:175–181.  https://doi.org/10.1016/j.indcrop.2014.10.058 CrossRefGoogle Scholar
  49. Gil R, Boscaiu M, Lull C, Bautista I, Lidón A, Vicente O (2013) Are soluble carbohydrates ecologically relevant for salt tolerance in halophytes? Funct Plant Biol 40(9):805–818.  https://doi.org/10.1071/FP12359 CrossRefGoogle Scholar
  50. Gitelson AA, Merzlyak MN (2004) Non-destructive assessment of chlorophyll carotenoid and anthocyanin content in higher plant leaves: principles and algorithms.Google Scholar
  51. Goharrizi KJ, Wilde HD, Amirmahani F, Moemeni MM, Zaboli M, Nazari M, Moosavi SS, Jamalvandi M (2018) Selection and validation of reference genes for normalization of qRT-PCR gene expression in wheat (Triticum durum L.) under drought and salt stresses. J Genet 97(5):1433–1444.  https://doi.org/10.1007/s12041-018-1042-5 CrossRefGoogle Scholar
  52. Goharrizi KJ, Baghizadeh A, Kalantar M, Fatehi F (2019) Assessment of changes in some biochemical traits and proteomic profile of UCB-1 pistachio rootstock leaf under salinity stress. J Plant Growth Regul.  https://doi.org/10.1007/s00344-019-10004-3 CrossRefGoogle Scholar
  53. Gould KS, Markham KR, Smith RH, Goris JJ (2000) Functional role of anthocyanins in the leaves of Quintinia serrata A Cunn. J Exp Bot 51(347):1107–1115.  https://doi.org/10.1093/jexbot/51.347.1107 CrossRefPubMedGoogle Scholar
  54. Granier C, Inze D, Tardieu F (2000) Spatial distribution of cell division rate can be deduced from that of p34(cdc2) kinase activity in maize leaves grown at contrasting temperatures and soil water conditions. Plant Physiol 124(3):1393–1402CrossRefGoogle Scholar
  55. Gu X-Y, Kianian SF, Foley ME (2006) Dormancy genes from weedy rice respond divergently to seed development environments. Genetics 172(2):1199–1211.  https://doi.org/10.1534/genetics.105.049155 CrossRefPubMedPubMedCentralGoogle Scholar
  56. Gu Z-X, Guo Q-H , Gu Y-J (2012) Factors influencing glucoraphanin and sulforaphane formation in Brassica plants: a review. J Integr Agric 11(11):1804–1816.  https://doi.org/10.1016/S2095-3119(12)60185-3 CrossRefGoogle Scholar
  57. Guo R-f, Yuan G-f, Wang Q-m (2013) Effect of NaCl treatments on glucosinolate metabolism in broccoli sprouts. J Zhejiang Univ Sci B 14(2):124.  https://doi.org/10.1631/jzus.B1200096 CrossRefPubMedPubMedCentralGoogle Scholar
  58. Halkier BA, Gershenzon J (2006) Biology and biochemistry of glucosinolates. Annu Rev Plant Biol 57:303–333.  https://doi.org/10.1146/annurev.arplant.57.032905.105228 CrossRefPubMedGoogle Scholar
  59. Hamed KB, Castagna A, Salem E, Ranieri A, Abdelly C (2007) Sea fennel (Crithmum maritimum L.) under salinity conditions: a comparison of leaf and root antioxidant responses. Plant Growth Regul 53(3):185–194.  https://doi.org/10.1007/s10725-007-9217-8 CrossRefGoogle Scholar
  60. Hansen CH, Wittstock U, Olsen CE, Hick AJ, Pickett JA, Halkier BA (2001) Cytochrome P450 CYP79F1 from Arabidopsis catalyzes the conversion of dihomomethionine and trihomomethionine to the corresponding aldoximes in the biosynthesis of aliphatic glucosinolates. J Biol Chem 276(14):11078–11085.  https://doi.org/10.1074/jbc.M010123200 CrossRefPubMedGoogle Scholar
  61. Heath RL, Packer L (1968) Photoperoxidation in isolated chloroplasts. I. Kinetics and stoichiometry of fatty acid peroxidation. Arch Biochem Biophys 125 (1):189–198.  https://doi.org/10.1016/0003-9861(68)90654-1 CrossRefGoogle Scholar
  62. Hniličková H, Hnilička F, Orsák M, Hejnák V (2019) Effect of salt stress on growth, electrolyte leakage, Na+ and K+ content in selected plant species. Plant Soil Environ 65(2):90–96.  https://doi.org/10.17221/620/2018-PSE CrossRefGoogle Scholar
  63. Hoagland DR, Arnon DI (1950) The water-culture method for growing plants without soil. Circ Calif Agric Exp Stn 347 (2nd edit)Google Scholar
  64. Hughes NM, Reinhardt K, Feild TS, Gerardi AR, Smith WK (2010) Association between winter anthocyanin production and drought stress in angiosperm evergreen species. J Exp Bot 61(6):1699–1709.  https://doi.org/10.1093/jxb/erq042 CrossRefPubMedPubMedCentralGoogle Scholar
  65. Hull AK, Vij R, Celenza JL (2000) Arabidopsis cytochrome P450s that catalyze the first step of tryptophan-dependent indole-3-acetic acid biosynthesis. Proc Natl Acad Sci 97(5):2379–2384.  https://doi.org/10.1073/pnas.040569997 CrossRefPubMedGoogle Scholar
  66. Hurry VM, Strand A, Tobiaeson M, Gardestrom P, Oquist G (1995) Cold hardening of spring and winter wheat and rape results in differential effects on growth, carbon metabolism, and carbohydrate content. Plant Physiol 109(2):697–706CrossRefGoogle Scholar
  67. Hussain S, Khan F, Cao W, Wu L, Geng M (2016) Seed priming alters the production and detoxification of reactive oxygen intermediates in rice seedlings grown under sub-optimal temperature and nutrient supply. Front Plant Sci 7:439.  https://doi.org/10.3389/fpls.2016.00439 CrossRefPubMedPubMedCentralGoogle Scholar
  68. Imlay JA, Linn S (1988) DNA damage and oxygen radical toxicity. Science (New York, NY) 240(4857):1302–1309CrossRefGoogle Scholar
  69. Kabiri R, Nasibi F, Farahbakhsh H (2014) Effect of exogenous salicylic acid on some physiological parameters and alleviation of drought stress in Nigella sativa plant under hydroponic culture. Plant Prot Sci 50(1):43–51.  https://doi.org/10.17221/56/2012-pps CrossRefGoogle Scholar
  70. Kamiab F, Talaie A, Khezri M, Javanshah A (2014) Exogenous application of free polyamines enhance salt tolerance of pistachio (Pistacia vera L.) seedlings. Plant Growth Regul 72(3):257–268.  https://doi.org/10.1007/s10725-013-9857-9 CrossRefGoogle Scholar
  71. Kaur H, Sirhindi G, Bhardwaj R, Alyemeni MN, Siddique KHM, Ahmad P (2018) 28-homobrassinolide regulates antioxidant enzyme activities and gene expression in response to salt- and temperature-induced oxidative stress in Brassica juncea. Sci Rep 8(1):8735.  https://doi.org/10.1038/s41598-018-27032-w CrossRefPubMedPubMedCentralGoogle Scholar
  72. Kaya MD, Okçu G, Atak M, Çıkılı Y, Kolsarıcı Ö (2006) Seed treatments to overcome salt and drought stress during germination in sunflower (Helianthus annuus L.). Eur J Agron 24(4):291–295.  https://doi.org/10.1016/j.eja.2005.08.001 CrossRefGoogle Scholar
  73. Keutgen AJ, Pawelzik E (2007) Modifications of strawberry fruit antioxidant pools and fruit quality under NaCl stress. J Agric Food Chem 55(10):4066–4072.  https://doi.org/10.1021/jf070010k CrossRefPubMedGoogle Scholar
  74. Khoo HE, Azlan A, Tang ST, Lim SM (2017) Anthocyanidins and anthocyanins: colored pigments as food, pharmaceutical ingredients, and the potential health benefits. Food Nutr Res 61(1):1361779.  https://doi.org/10.1080/16546628.2017.1361779 CrossRefPubMedPubMedCentralGoogle Scholar
  75. Kordrostami M, Rabiei B, Hassani Kumleh H (2017) Biochemical, physiological and molecular evaluation of rice cultivars differing in salt tolerance at the seedling stage. Physiol Mol Biol Plants 23(3):529–544.  https://doi.org/10.1007/s12298-017-0440-0 CrossRefPubMedPubMedCentralGoogle Scholar
  76. Kumar V, Shriram V, Jawali N, Shitole MG (2007) Differential response of indica rice genotypes to NaCl stress in relation to physiological and biochemical parameters. Arch Agron Soil Sci 53(5):581–592.  https://doi.org/10.1080/03650340701576800 CrossRefGoogle Scholar
  77. Kumar S, Stecher G, Tamura K (2016) MEGA7: molecular evolutionary genetics analysis version 70 for bigger datasets. Mol Biol Evol 33(7):1870–1874.  https://doi.org/10.1093/molbev/msw054 CrossRefPubMedGoogle Scholar
  78. Labdelli A, Adda A, Halis Y, Soualem S (2014) Effects of water regime on the structure of roots and stems of durum wheat (Triticum durum Desf.). J Bot.  https://doi.org/10.1155/2014/703874.CrossRefGoogle Scholar
  79. Laleh G, Frydoonfar H, Heidary R, Jameei R, Zare S (2006) The effect of light, temperature, pH and species on stability of anthocyanin pigments in four Berberis species. Pak J Nutr 5(1):90–92.  https://doi.org/10.3923/pjn.2006.90.92 CrossRefGoogle Scholar
  80. Landi M, Tattini M, Gould KS (2015) Multiple functional roles of anthocyanins in plant-environment interactions. Environ Exp Bot 119:4–17.  https://doi.org/10.1016/j.envexpbot.2015.05.012 CrossRefGoogle Scholar
  81. Lee MH, Cho EJ, Wi SG, Bae H, Kim JE, Cho JY, Lee S, Kim JH, Chung BY (2013) Divergences in morphological changes and antioxidant responses in salt-tolerant and salt-sensitive rice seedlings after salt stress. Plant Physiol Biochem 70:325–335.  https://doi.org/10.1016/j.plaphy.2013.05.047 CrossRefPubMedGoogle Scholar
  82. Li J, Jia H, Wang J, Cao Q, Wen Z (2014) Hydrogen sulfide is involved in maintaining ion homeostasis via regulating plasma membrane Na+/H+ antiporter system in the hydrogen peroxide-dependent manner in salt-stress Arabidopsis thaliana root. Protoplasma 251(4):899–912.  https://doi.org/10.1007/s00709-013-0592-x CrossRefPubMedGoogle Scholar
  83. Liang H, Yuan QP, Dong HR, Liu YM (2006) Determination of sulforaphane in broccoli and cabbage by high-performance liquid chromatography. J Food Compos Anal 19(5):473–476.  https://doi.org/10.1016/j.jfca.2005.11.005 CrossRefGoogle Scholar
  84. Lim JH, Park KJ, Kim BK, Jeong JW, Kim HJ (2012) Effect of salinity stress on phenolic compounds and carotenoids in buckwheat (Fagopyrum esculentum M.) sprout. Food Chem 135(3):1065–1070.  https://doi.org/10.1016/j.foodchem.2012.05.068 CrossRefPubMedGoogle Scholar
  85. Lin CC, Kao CH (1999) NaCl induced changes in ionically bound peroxidase activity in roots of rice seedlings. Plant Soil 216(1):147.  https://doi.org/10.1023/A:1004714506156 CrossRefGoogle Scholar
  86. López-Berenguer C, Martínez-Ballesta MC, García-Viguera C, Carvajal M (2008) Leaf water balance mediated by aquaporins under salt stress and associated glucosinolate synthesis in broccoli. Plant Sci 174(3):321–328.  https://doi.org/10.1016/j.plantsci.2007.11.012 CrossRefGoogle Scholar
  87. Lopez-Berenguer C, Martinez-Ballesta Mdel C, Moreno DA, Carvajal M, Garcia-Viguera C (2009) Growing hardier crops for better health: salinity tolerance and the nutritional value of broccoli. J Agric Food Chem 57(2):572–578.  https://doi.org/10.1021/jf802994p CrossRefPubMedGoogle Scholar
  88. Mahmoudi H, Kaddour R, Huang J, Nasri N, Olfa B, M’Rah S, Hannoufa A, Lachaâl M, Ouerghi Z (2011) Varied tolerance to NaCl salinity is related to biochemical changes in two contrasting lettuce genotypes. Acta Physiol Plant 33(5):1613–1622.  https://doi.org/10.1007/s11738-010-0696-2 CrossRefGoogle Scholar
  89. Mansour MMF, Salama KHA (2004) Cellular basis of salinity tolerance in plants. Environ Exp Bot 52(2):113–122.  https://doi.org/10.1016/j.envexpbot.2004.01.009 CrossRefGoogle Scholar
  90. Mao Y-B, Tao X-Y, Xue X-Y, Wang L-J, Chen X-Y (2011) Cotton plants expressing CYP6AE14 double-stranded RNA show enhanced resistance to bollworms. Transgenic Res 20(3):665–673.  https://doi.org/10.1007/s11248-010-9450-1 CrossRefPubMedGoogle Scholar
  91. McCord JM, Fridovich I (1969) Superoxide dismutase: an enzymic function for erythrocuprein (hemocuprein). J Biol Chem 244(22):6049–6055Google Scholar
  92. Meir S, Philosoph-Hadas S, Aharoni N (1992) Ethylene-increased accumulation of fluorescent lipid-peroxidation products detected during senescence of parsley by a newly developed method. J Am Soc Hortic Sci 117(1):128–132.  https://doi.org/10.21273/JASHS.117.1.128 CrossRefGoogle Scholar
  93. Meloni DA, Oliva MA, Martinez CA, Cambraia J (2003) Photosynthesis and activity of superoxide dismutase, peroxidase and glutathione reductase in cotton under salt stress. Environ Exp Bot 49(1):69–76.  https://doi.org/10.1016/S0098-8472(02)00058-8 CrossRefGoogle Scholar
  94. Mikkelsen MD, Hansen CH, Wittstock U, Halkier BA (2000) Cytochrome P450 CYP79B2 from Arabidopsis catalyzes the conversion of tryptophan to indole-3-acetaldoxime, a precursor of indole glucosinolates and indole-3-acetic acid. J Biol Chem 275(43):33712–33717.  https://doi.org/10.1074/jbc.M001667200 CrossRefPubMedGoogle Scholar
  95. Mikkelsen MD, Petersen BL, Glawischnig E, Jensen AB, Andreasson E, Halkier BA (2003) Modulation of CYP79 genes and glucosinolate profiles in arabidopsis by defense signaling pathways. Plant Physiol 131(1):298–308.  https://doi.org/10.1104/pp.011015 CrossRefPubMedPubMedCentralGoogle Scholar
  96. Mittler R (2002) Oxidative stress, antioxidants and stress tolerance. Trends Plant Sci 7(9):405–410.  https://doi.org/10.1016/S1360-1385(02)02312-9 CrossRefPubMedGoogle Scholar
  97. Mulligan GA, Frankton C (1962) Taxonomy of the genus cardaria with particular reference to the species introduced into North America. Can J Bot 40(11):1411–1425.  https://doi.org/10.1139/b62-136 CrossRefGoogle Scholar
  98. Munns R, Tester M (2008) Mechanisms of salinity tolerance. Annu Rev Plant Biol 59:651–681.  https://doi.org/10.1146/annurev.arplant.59.032607.092911 CrossRefPubMedGoogle Scholar
  99. Nafisi M, Sønderby IE, Hansen BG, Geu-Flores F, Nour-Eldin HH, Nørholm MH, Jensen NB, Li J, Halkier BA (2006) Cytochromes P450 in the biosynthesis of glucosinolates and indole alkaloids. Phytochem Rev 5(2–3):331–346.  https://doi.org/10.1007/s11101-006-9004-6 CrossRefGoogle Scholar
  100. Noreen Z, Ashraf M, Akram NA (2010) Salt-induced regulation of some key antioxidant enzymes and physio-biochemical phenomena in five diverse cultivars of turnip (Brassica rapa L.). J Agron Crop Sci 196(4):273–285.  https://doi.org/10.1111/j.1439-037X.2010.00420.x CrossRefGoogle Scholar
  101. Núñez M, Mazzafera P, Mazorra LM, Siqueira WJ, Zullo MAT (2003) Influence of a brassinosteroid analogue on antioxidant enzymes in rice grown in culture medium with NaCl. Biol Plant 47(1):67–70.  https://doi.org/10.1023/A:1027380831429 CrossRefGoogle Scholar
  102. Parida AK, Das AB (2005) Salt tolerance and salinity effects on plants: a review. Ecotoxicol Environ Saf 60(3):324–349.  https://doi.org/10.1016/j.ecoenv.2004.06.010 CrossRefPubMedGoogle Scholar
  103. Pattanagul W, Thitisaksakul M (2008) Effect of salinity stress on growth and carbohydrate metabolism in three rice (Oryza sativa L.) cultivars differing in salinity tolerance. Indian J Exp Biol 46(10):736–742PubMedGoogle Scholar
  104. Pedras MSC, Okinyo-Owiti DP, Thoms K, Adio AM (2009) The biosynthetic pathway of crucifer phytoalexins and phytoanticipins: de novo incorporation of deuterated tryptophans and quasi-natural compounds. Phytochemistry 70(9):1129–1138.  https://doi.org/10.1016/j.phytochem.2009.05.015 CrossRefPubMedGoogle Scholar
  105. Piao HL, Lim JH, Kim SJ, Cheong GW, Hwang I (2001) Constitutive over-expression of AtGSK1 induces NaCl stress responses in the absence of NaCl stress and results in enhanced NaCl tolerance in Arabidopsis. Plant J 27(4):305–314.  https://doi.org/10.1046/j.1365-313x.2001.01099.x CrossRefPubMedGoogle Scholar
  106. Qasim M, Ashraf M, Ashraf M, Rehman S-U, Rha E (2003) Salt-induced changes in two canola cultivars differing in salt tolerance. Biol Plant 46(4):629–632.  https://doi.org/10.1023/A:1024844402000 CrossRefGoogle Scholar
  107. Radonic A, Blazevic I, Mastelic J, Zekic M, Skocibusic M, Maravic A (2011) Phytochemical analysis and antimicrobial activity of Cardaria draba (L.) Desv volatiles. Chem Biodivers 8(6):1170–1181.  https://doi.org/10.1002/cbdv.201000370 CrossRefPubMedGoogle Scholar
  108. Rask L, Andréasson E, Ekbom B, Eriksson S, Pontoppidan B, Meijer J (2000) Myrosinase: gene family evolution and herbivore defense in Brassicaceae. Plant Mol Biol.  https://doi.org/10.1023/A:1006380021658 CrossRefPubMedGoogle Scholar
  109. Rebey IB, Bourgou S, Rahali FZ, Msaada K, Ksouri R, Marzouk B (2017) Relation between salt tolerance and biochemical changes in cumin (Cuminum cyminum L.) seeds. J Food Drug Anal 25(2):391–402.  https://doi.org/10.1016/j.jfda.2016.10.001 CrossRefGoogle Scholar
  110. Reintanz B, Lehnen M, Reichelt M, Gershenzon J, Kowalczyk M, Sandberg G, Godde M, Uhl R, Palme K (2001) Bus, a bushy Arabidopsis CYP79F1 knockout mutant with abolished synthesis of short-chain aliphatic glucosinolates. Plant Cell 13(2):351–367.  https://doi.org/10.1105/tpc.13.2.351 CrossRefPubMedPubMedCentralGoogle Scholar
  111. Riahi-Madvar A, Mohammadi M, Pourseyedi S (2014) Elicitors induced sulforaphane production in Lepidium draba. Asian J Biomed Pharm Sci 4(35):64.  https://doi.org/10.15272/ajbps.v4i35.561 CrossRefGoogle Scholar
  112. Sharma A, Kumar V, Singh R, Thukral AK, Bhardwaj R (2015) 24-Epibrassinolide induces the synthesis of phytochemicals effected by imidacloprid pesticide stress in Brassica juncea L. J Pharmacognosy Phytochem 4(3):60–64.Google Scholar
  113. Sharma A, Thakur S, Kumar V, Kanwar MK, Kesavan AK, Thukral AK, Bhardwaj R, Alam P, Ahmad P (2016) Pre-sowing seed treatment with 24-epibrassinolide ameliorates pesticide stress in Brassica juncea L through the modulation of stress markers. Front Plant Sci 7:1569.  https://doi.org/10.3389/fpls.2016.01569 CrossRefPubMedPubMedCentralGoogle Scholar
  114. Sharma A, Shahzad B, Kumar V, Kohli SK, Sidhu GPS, Bali AS, Handa N, Kapoor D, Bhardwaj R, Zheng B (2019a) Phytohormones regulate accumulation of osmolytes under abiotic stress. Biomolecules 9(7):285.  https://doi.org/10.3390/biom9070285 CrossRefPubMedCentralGoogle Scholar
  115. Sharma A, Shahzad B, Rehman A, Bhardwaj R, Landi M, Zheng B (2019b) Response of phenylpropanoid pathway and the role of polyphenols in plants under abiotic stress. Molecules 24(13):2452.  https://doi.org/10.3390/molecules24132452 CrossRefPubMedCentralGoogle Scholar
  116. Shi H, Wang X, Ye T, Chen F, Deng J, Yang P, Zhang Y, Chan Z (2014) The cysteine2/histidine2-type transcription factor zinc finger of Arabidopsis thaliana6 modulates biotic and abiotic stress responses by activating salicylic acid-related genes and C-repeat-binding factor genes in Arabidopsis. Plant Physiol 165(3):1367–1379.  https://doi.org/10.1104/pp.114.242404 CrossRefPubMedPubMedCentralGoogle Scholar
  117. Shoeva OY, Mock H-P, Kukoeva TV, Börner A, Khlestkina EK (2016) Regulation of the flavonoid biosynthesis pathway genes in purple and black grains of Hordeum vulgare. PLoS ONE 11(10):e0163782.  https://doi.org/10.1371/journal.pone.0163782 CrossRefPubMedPubMedCentralGoogle Scholar
  118. Taïbi K, Taïbi F, Ait Abderrahim L, Ennajah A, Belkhodja M, Mulet JM (2016) Effect of salt stress on growth, chlorophyll content, lipid peroxidation and antioxidant defence systems in Phaseolus vulgaris L. South African Journal of Botany 105:306–312.  https://doi.org/10.1016/j.sajb.2016.03.011 CrossRefGoogle Scholar
  119. Tamura K, Nei M, Kumar S (2004) Prospects for inferring very large phylogenies by using the neighbor-joining method. Proc Natl Acad Sci USA 101(30):11030–11035.  https://doi.org/10.1073/pnas.0404206101 CrossRefPubMedPubMedCentralGoogle Scholar
  120. Tanveer M, Shahzad B, Sharma A, Biju S, Bhardwaj R (2018) 24-Epibrassinolide; an active brassinolide and its role in salt stress tolerance in plants: a review. Plant Physiol Biochem 130:69–79.  https://doi.org/10.1016/j.plaphy.2018.06.035 CrossRefPubMedGoogle Scholar
  121. Tavakkoli E, Rengasamy P, McDonald GK (2010) High concentrations of Na+ and Cl- ions in soil solution have simultaneous detrimental effects on growth of faba bean under salinity stress. J Exp Bot 61(15):4449–4459.  https://doi.org/10.1093/jxb/erq251 CrossRefPubMedPubMedCentralGoogle Scholar
  122. Tester M, Davenport R (2003) Na+ tolerance and Na+ transport in higher plants. Ann Bot 91(5):503–527CrossRefGoogle Scholar
  123. Traka M, Mithen R (2009) Glucosinolates, isothiocyanates and human health. Phytochem Rev 8(1):269–282.  https://doi.org/10.1007/s11101-008-9103-7 CrossRefGoogle Scholar
  124. Vattem DA, Lin YT, Labbe RG, Shetty K (2004) Phenolic antioxidant mobilization in cranberry pomace by solid-state bioprocessing using food grade fungus Lentinus edodes and effect on antimicrobial activity against select food borne pathogens. Innov Food Sci Emerg Technol 5(1):81–91.  https://doi.org/10.1016/j.ifset.2003.09.002 CrossRefGoogle Scholar
  125. 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(1):59–66.  https://doi.org/10.1016/S0168-9452(99)00197-1 CrossRefGoogle Scholar
  126. Wagner GJ (1979) Content and vacuole/extravacuole distribution of neutral sugars, free amino acids, and anthocyanin in protoplasts. Plant Physiol 64(1):88–93.  https://doi.org/10.1104/pp.64.1.88 CrossRefPubMedPubMedCentralGoogle Scholar
  127. Wang Y, Li X, Li J, Bao Q, Zhang F, Tulaxi G, Wang Z (2016) Salt-induced hydrogen peroxide is involved in modulation of antioxidant enzymes in cotton. Crop J 4(6):490–498.  https://doi.org/10.1016/j.cj.2016.03.005 CrossRefGoogle Scholar
  128. Wardlaw IF, Willenbrink J (1994) Carbohydrate storage and mobilisation by the culm of wheat between heading and grain maturity: the relation to sucrose synthase and sucrose-phosphate synthase. Funct Plant Biol 21(3):255–271.  https://doi.org/10.1071/PP9940255 CrossRefGoogle Scholar
  129. Wei P, Yang Y, Wang F, Chen H (2015) Effects of drought stress on the antioxidant systems in three species of Diospyros L. Hortic Environ Biotechnol 56(5):597–605.  https://doi.org/10.1007/s13580-015-0074-5 CrossRefGoogle Scholar
  130. Wise RR, Naylor AW (1987) Chilling-enhanced photooxidation : evidence for the role of singlet oxygen and superoxide in the breakdown of pigments and endogenous antioxidants. Plant Physiol 83(2):278–282.  https://doi.org/10.1104/pp.83.2.278 CrossRefPubMedPubMedCentralGoogle Scholar
  131. Wittstock U, Halkier BA (2000) Cytochrome P450 CYP79A2 from Arabidopsis thaliana L catalyzes the conversion of L-phenylalanine to phenylacetaldoxime in the biosynthesis of benzylglucosinolate. J Biol Chem 275(19):14659–14666.  https://doi.org/10.1074/jbc.275.19.14659 CrossRefPubMedGoogle Scholar
  132. Yasar F, Ellialtioglu S, Yildiz K (2008) Effect of salt stress on antioxidant defense systems, lipid peroxidation, and chlorophyll content in green bean. Russ J Plant Physiol 55(6):782.  https://doi.org/10.1134/S1021443708060071 CrossRefGoogle Scholar
  133. Yemm E, Cocking E, Ricketts R (1955) The determination of amino-acids with ninhydrin. Analyst 80(948):209–214.  https://doi.org/10.1039/AN9558000209 CrossRefGoogle Scholar
  134. Yen WJ, Chyau CC, Lee CP, Chu HL, Chang LW, Duh PD (2013) Cytoprotective effect of white tea against H2O2-induced oxidative stress in vitro. Food Chem 141(4):4107–4114.  https://doi.org/10.1016/j.foodchem.2013.06.106 CrossRefPubMedGoogle Scholar
  135. Yuan G, Wang X, Guo R, Wang Q (2010) Effect of salt stress on phenolic compounds, glucosinolates, myrosinase and antioxidant activity in radish sprouts. Food Chem 121(4):1014–1019.  https://doi.org/10.1016/j.foodchem.2010.01.040 CrossRefGoogle Scholar
  136. Zhang Y, Talalay P, Cho CG, Posner GH (1992) A major inducer of anticarcinogenic protective enzymes from broccoli: isolation and elucidation of structure. Proc Natl Acad Sci USA 89(6):2399–2403.  https://doi.org/10.1073/pnas.89.6.2399 CrossRefPubMedGoogle Scholar
  137. Zhishen J, Mengcheng T, Jianming W (1999) The determination of flavonoid contents in mulberry and their scavenging effects on superoxide radicals. Food Chem 64(4):555–559.  https://doi.org/10.1016/S0308-8146(98)00102-2 CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Department of Plant Breeding, Yazd BranchIslamic Azad UniversityYazdIran
  2. 2.Department of Biotechnology, Institute of Science and High Technology and Environmental SciencesGraduate University of Advanced TechnologyKermanIran
  3. 3.Department of Biology, Faculty of ScienceFerdowsi University of MashhadMashhadIran
  4. 4.Department of Biotechnology, Institute of Science and High Technology and Environmental SciencesGraduate University of Advanced TechnologyKermanIran

Personalised recommendations