Skip to main content

EsHO 1 mediated mitigation of NaCl induced oxidative stress and correlation between ROS, antioxidants and HO 1 in seedlings of Eruca sativa: underutilized oil yielding crop of arid region

Abstract

Study have focused on NaCl induced HO 1 production and its co-relation to ROS and antioxidant regulation in Eruca sativa. Seedlings were subjected to NaCl stress ranges from 10 to 150 mM. After 96 h of treatment, plants samples were harvested to evaluate the cellular equilibrium and salt tolerance mechanisms through morphological, stress parameters, non enzymatic and antioxidant enzymes. The HO 1 activity was found to be highest at 75 mM NaCl in leaves and roots which were 2.49 and 2.02 folds respectively. The expression of EsHO 1 was also observed and the higher expression was recorded in roots than leaves. The overall activity of other antioxidants (APX and proline) was also found to be higher at 75 mM concentration. The highest HO 1 activity with other antioxidants indicates the decline in LPX and ROS at 75 mM NaCl. The present study concluded that HO 1 helps in amelioration of NaCl stress by working within a group of antioxidants that create the defense machinery in seedlings of E. sativa by manipulating various physiological processes of plants. These findings for the first time suggest the protective role of HO 1 in scavenging ROS in E. sativa under salinity stress.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Abbreviations

HO 1:

Heme oxygenase 1

CAT:

Catalase

APX:

Ascorbate peroxidase

GPX:

Guaiacol peroxidase

SOD:

Superoxide dismutase

EtBr:

Ethidium bromide

ROS:

Reactive oxygen species

TBA:

2-Thiobarbituric acid

TCA:

Trichloroacetic acid

References

  1. Abogadallah GM (2010) Insights into the significance of antioxidative defense under salt stress. Plant Signal Behav 5:369–374

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  2. Aebi H (1974) Catalases. In: Bergmeyer HU (ed) Methods of enzymatic analysis. Academic Press Inc, New York, pp 673–680

    Chapter  Google Scholar 

  3. 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 

  4. Balestrasse KB, Noriega GO, Batlle A, Tomaro ML (2005) Involvement of heme oxygenase as antioxidant defense in soybean nodules. Free Radic Res 39:145–151

    Article  CAS  PubMed  Google Scholar 

  5. Barbieri G, Bottino A, Di Stasio E, Vallone S, Maggio A (2011) Proline and light as quality enhancers of rocket (Eruca sativa Miller) grown under saline conditions. Sci Hortic 128:393–400

    Article  CAS  Google Scholar 

  6. Bates LS, Waldren RP, Tear ID (1973) Rapid determination of free proline for water stress studies. Plant Soil 39:205–207

    Article  CAS  Google Scholar 

  7. Cao Z, Geng B, Xu S, Xuan W, Nie L, Shen W, Liang Y, Guan R (2011) BnHO 1, a haem oxygenase-1 gene from Brassica napus, is required for salinity and osmotic stress-induced lateral root formation. J Exp Bot 62:4675–4689

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. Chen GX, Asada K (1989) Ascorbate peroxidase in tea leaves: occurrence of two isozymes and the differences in their enzymatic and molecular properties. Plant Cell Physiol 30:987–998

    Article  CAS  Google Scholar 

  9. De Vos CHR, Schat H, Vooijs R, Ernst WHO (1989) Copper-induced damage to the permeability barrier in roots of Silene cuiubalus. J Plant Physiol 135:164–179

    Article  Google Scholar 

  10. Demiral T, Turkan I (2005) Comparative lipid peroxidation, antioxidant defense systems and proline content in roots of two rice cultivars differing in salt tolerance. Environ Exp Bot 53:247–257

    Article  CAS  Google Scholar 

  11. Dixit S, Verma K, Shekhawat GS (2014) In vitro evaluation of mitochondrial–chloroplast subcellular localization of heme oxygenase 1 [HO 1] in Glycine max. Protoplasma 251:671–675

    Article  CAS  PubMed  Google Scholar 

  12. Eyidogan F, Oz MT (2007) Effect of salinity on antioxidant responses of chickpea seedlings. Acta Physiol Plant 29:485–493

    Article  CAS  Google Scholar 

  13. Fagbenro OA (2004) Soybean meal replacement by roquette (Eruca sativa Miller) seed meal as protein feedstuff in diets for African catfish, Clarias gariepinus (Burchell 1822), fingerlings. Aqua Res 35:917–923

    Article  Google Scholar 

  14. Foyer C, Lopez-Delgado H, Dat J, Scott I (1997) Hydrogen peroxide and glutathione-associated mechanisms of acclimatory stress tolerance and signalling. Physiol Plant 100:241–254

    Article  CAS  Google Scholar 

  15. Grattana SR, Grieveb CM (1999) Salinity-mineral nutrient relations in horticultural crops. Sci Hortic 78:127–157

    Article  Google Scholar 

  16. Huang Y, Zu L, Zhou M, Shi C, Shen G, Shi F (2018) Accumulation and tolerance characteristics of lead in Althaea rosea Cav. and Malva crispa L. Biologia. https://doi.org/10.2478/s11756-018-0042-5

    Article  Google Scholar 

  17. Jakhar SS, Duhan JC, Chauhan MS (2002) Effect of soil amendment with some oil cakes on root rot of cotton caused by rhizoctonia spp. Plant Dis Res 17:16–20

    Google Scholar 

  18. Katerji N, Van Hoorn JW, Hamdy A, Mastrorilli M, Moukarzel E (1997) Osmotic adjustment of sugar beets in response to soil salinity and its influence on stomatal conductance, growth and yield. Agric Water Manag 34:57–69

    Article  Google Scholar 

  19. Katsuhara M, Otsuka T, Ezaki B (2005) Salt stress-induced lipid peroxidation is reduced by glutathione S-transferase, but this reduction of lipid peroxides is not enough for a recovery of root growth in Arabidopsis. Plant Sci 169:369–373

    Article  CAS  Google Scholar 

  20. Khan MH, Panda SK (2008) Alterations in root lipid peroxidation and antioxidative responses in two rice cultivars under NaCl salinity stress. Acta Physiol Plant 30:81–89

    Article  CAS  Google Scholar 

  21. Lin YT, Zhang W, Qi F, Cui WT, Xie YJ, Shen WB (2014) Hydrogen-rich water regulates cucumber adventitious root development in a heme oxygenase-1/carbon monoxide-dependent manner. J Plant Physiol 171:1–8

    Article  CAS  PubMed  Google Scholar 

  22. Ling B, Cui WT, Wu MZ, Lin JS, Zhou WT, Huang JJ, Shen WB (2009) Carbon monoxide mitigates salt induced inhibition of root growth and suppresses programmed cell death in wheat primary roots by inhibiting superoxide anion overproduction. Plant Sci 177:331–340

    Article  CAS  Google Scholar 

  23. Liu H, Song J, Dong L, Wang D, Zhang S, Liu J (2017) Physiological responses of three soybean species (Glycine soja, G. gracilis, and G. max cv. Melrose) to salinity stress. J Plant Res 130:723–733

    Article  CAS  PubMed  Google Scholar 

  24. Luna CM, Gonzalez CA, Trippi US (1994) Oxidative damage caused by an excess copper in oat leaves. Plant Cell Physiol 35:11–15

    CAS  Google Scholar 

  25. Mahawar L, Shekhawat GS (2016) Salt induce oxidative stress and its tolerance mechanism in plant: morphological, biochemical and molecular perspective. Biotech Today 6:80–87

    Article  Google Scholar 

  26. Mahawar L, Shekhawat GS (2018) Haem oxygenase: a functionally diverse enzyme of photosynthetic organisms and its role in phytochrome chromophore biosynthesis, cellular signalling and defence mechanisms. Plant Cell Environ 41:483–500

    Article  CAS  PubMed  Google Scholar 

  27. Mahawar L, Kumar R, Shekhawat GS (2018a) Evaluation of heme oxygenase 1 (HO 1) in Cd and Ni induced cytotoxicity and crosstalk with ROS quenching enzymes in two to four leaf stage seedlings of Vigna radiata. Protoplasma 255:527–545

    Article  CAS  PubMed  Google Scholar 

  28. Mahawar L, Khator K, Shekhawat GS (2018b) Role of Proline in mitigating NaCl induced oxidative stress in Eruca sativa Miller: an important oil yielding crop of Indian Thar Desert. Vegetos Int J Plant Res Biotechnol. https://doi.org/10.5958/2229-4473.2018.00032.0

    Article  Google Scholar 

  29. Munns R (2002) Comparative physiology of salt and water stress. Plant Cell Environ 25:239–250

    Article  CAS  PubMed  Google Scholar 

  30. Munns R, Tester M (2008) Mechanisms of salinity tolerance. Annu Rev Plant Biol 59:651–681

    Article  CAS  PubMed  Google Scholar 

  31. Parida K, Das AB (2005) Salt tolerance and salinity effects on plants: a review. Ecotoxicol Environ Saf 60:324–349

    Article  CAS  PubMed  Google Scholar 

  32. Putter J (1974) Peroxidase. In: Bergemeyer HU (ed) Methods of enzymatic analysis. Academic Press, London, pp 685–690

    Chapter  Google Scholar 

  33. Sandalio LM, Dalurzo HC, Gomez M, Romero-Puertas MC, Del Rio LA (2001) Cadmium-induced changes in the growth and oxidative metabolism of pea plants. J Exp Bot 52:2115–2126

    Article  CAS  PubMed  Google Scholar 

  34. Santa-Cruz D, Pacienza N, Zilli C, Pagano E, Balestrasse K, Yannarelli G (2017) Heme oxygenase up-regulation under ultraviolet-B radiation is not epigenetically restricted and involves specific stress-related transcriptions factors. Redox Biol 12:549–557

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. Sehrawat N, Bhat KV, Sairam RK, Jaiwal PK (2013) Identification of salt resistant wild relatives of mungbean (Vigna radiata (L.) Wilczek). Asian J Plant Sci Res 5:41–49

    Google Scholar 

  36. Serrano R, Culianz-Macia F, Moreno V (1999) Genetic engineering of salt and drought tolerance with yeast regulatory genes. Sci Hortic 78:261–269

    Article  CAS  Google Scholar 

  37. Shan C, Liu R (2017) Exogenous hydrogen peroxide up-regulates the contents of ascorbate and glutathione in the leaves of Vigna radiata (Linn.) Wilczek. exposed to salt stress. Braz J Bot 40:583–589

    Article  Google Scholar 

  38. Shankar V, Kumar D, Agarwal V (2016) Assessment of antioxidant enzyme activity and mineral nutrients in response to NaCl stress and its amelioration through glutathione in chickpea. App Biochem Biotechnol 178:267–284

    Article  CAS  Google Scholar 

  39. Shanker A, Venkateswarlu B (2011) Abiotic stress response in plants physiological, biochemical and genetic perspectives. InTech, Croatia. https://doi.org/10.5772/1762

  40. Shekhawat GS, Verma K (2010) Heme oxygenase [HO]: an overlooked enzyme of plant metabolism and defence. J Exp Bot 61:2255–2270

    Article  CAS  PubMed  Google Scholar 

  41. Shekhawat GS, Dixit S, Verma K, Nasybullina EI, Kosmachevskaya OV, Topunov AF (2011) Haem oxygenase: enzyme with functional diversity. J Stress Physiol Biochem 7:88–94

    Google Scholar 

  42. Singh KN, Chatrath R (2001) Salinity tolerance: application of physiology in wheat breeding. In: Reynolds MP, Ortiz-Monasterio JJ, McNab A (eds) Application of physiology in wheat breeding. CIMMYT, Mexico, pp 101–110

    Google Scholar 

  43. Tenhunen R, Marver HS, Schmid R (1968) The enzymatic conversion of heme to bilirubin by microsomal heme oxygenase. Proc Natl Acad Sci 61:748–755

    Article  CAS  PubMed  Google Scholar 

  44. Tripathi BN, Singh V, Ezaki B, Sharma V, Gaur JP (2013) Mechanism of Cu and Cd induced proline hyperaccumulation in Triticum aestivum [Wheat]. J Plant Growth Regul 32:799–808

    Article  CAS  Google Scholar 

  45. Verma K, Shekhawat GS (2013) New development in chromophore research. In: Moliere A, Vigneron E (eds) Phytochrome chromophore biosynthesis and chloroplast development: possible role and regulation of HO (Haem oxygenase). Nova Science publishers, New York, pp 267–279

    Google Scholar 

  46. Verma K, Dixit S, Shekhawat GS, Alam A (2015) Antioxidant activity of heme oxygenase 1 in Brassica juncea (L.) Czern. (Indian mustard) under salt stress. Turk J Biol 39:540–549

    Article  CAS  Google Scholar 

  47. Wang Y, Gu W, Meng Y, Xie T, Li L, Li J, Wei S (2017) γ-Aminobutyric acid imparts partial protection from salt stress injury to maize seedlings by improving photosynthesis and upregulating osmoprotectants and antioxidants. Sci Rep 7:43609

    Article  PubMed  PubMed Central  Google Scholar 

  48. Wilkins DA (1978) The measurement of tolerance to edaphic factors by means of root growth. New Phytol 80:623–633

    Article  CAS  Google Scholar 

  49. Xie Y, Mao Y, Xu S, Zhou H, Duan X, Cui W, Zhang J, Xu G (2015) Heme-heme oxygenase 1 system is involved in ammonium tolerance by regulating antioxidant defence in Oryza sativa. Plant Cell Environ 38:129–143

    Article  CAS  PubMed  Google Scholar 

  50. Xu S, Zhang B, Cao ZY, Ling TF, Shen WB (2011) Heme oxygenase is involved in cobalt chloride-induced lateral root development in tomato. Biometals 24:181–191

    Article  CAS  PubMed  Google Scholar 

  51. Yannarelli GG, Noriega GO, Batlle A, Tomaro ML (2006) Heme oxygenase up regulation in ultraviolet-B irradiated soybean plants involves reactive oxygen species. Planta 224:1154–1162

    Article  CAS  PubMed  Google Scholar 

  52. Zhu JK (2007) Plant salt stress. Wiley, New York

    Book  Google Scholar 

  53. Zhu L, Yang Z, Zeng X, Gao J, Liu J, Yi B, Ma C, Shen J, Tu J, Fu T, We J (2017) Heme oxygenase 1 defects lead to reduced chlorophyll in Brassica napus. Plant Mol Biol 93:579–592

    Article  CAS  PubMed  Google Scholar 

  54. Zilli CG, Santa-Cruz DM, Yannarelli CG, Noriega GO, Tomaro ML, Balestrasse KB (2009) Heme oxygenase contributes to alleviate salinity damage in Glycine max L. leaves. Inter J Cell Biol. https://doi.org/10.1155/2009/848516

    Article  Google Scholar 

Download references

Author information

Affiliations

Authors

Corresponding author

Correspondence to Gyan Singh Shekhawat.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Mahawar, L., Shekhawat, G.S. EsHO 1 mediated mitigation of NaCl induced oxidative stress and correlation between ROS, antioxidants and HO 1 in seedlings of Eruca sativa: underutilized oil yielding crop of arid region. Physiol Mol Biol Plants 25, 895–904 (2019). https://doi.org/10.1007/s12298-019-00663-7

Download citation

Keywords

  • Heme oxygenase 1
  • Eruca sativa
  • Salinity stress
  • Antioxidants
  • Reactive oxygen species