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NaCl induced oxidative stress in legume crops of Indian Thar Desert: an insight in the cytoprotective role of HO1, NO and antioxidants

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Abstract

The manuscript highlights the role of antioxidants in alleviation of salinity stress in two principal legume crops Cyamopsis tetragonoloba and Vigna radiata of Indian Thar Desert. The study evaluates correlation between the antioxidants of two cultivars in terms of morphological and physiological alterations. Hydroponically acclimatized seedlings of both the crops were subjected to NaCl stress at different concentrations ranges from 10 to 100 mM. After 96 h, the treated legumes were harvested to analyze the cellular homeostasis and salt tolerance mechanism via examining growth, stress parameters, osmoprotectants and enzymatic antioxidants. Differential response in the antioxidants activity was observed in crops. Equal contribution of antioxidants in mitigation of salinity stress was recorded in C. tetragonoloba while V. radiata shows greater tolerance by accumulating greater amount of proline which is approximately 2.72 folds higher than C. tetragonoloba. Moreover, the NR and HO1 activities in V. radiata were recorded to be 2.76 and 1.55 folds respectively which is 1.2 times higher in comparison to C. tetragonoloba. The detrimental effect of NaCl in terms of MDA content was also higher in V. radiata which concluded that V. radiata is more reactive towards salinity stress than C. tetragonoloba. The study is significant as this is the first report illustrating the sensitivity and tolerance level of NaCl in legumes of Thar Desert.

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References

  • Abdel Latef AA, Miransari M (2014) The role of arbuscular mycorrhizal fungi in alleviation of salt stress. In: Miransari M (ed) Use of microbes for the alleviation of soil stresses. Springer, NewYork, pp 23–38

    Google Scholar 

  • Aebi H (1974) Catalase. In: Bergmeyer HU (ed) Methods of enzymatic analysis. Verlag Chemie/Academic Press Inc, Weinheim/NewYork, pp 673–680. https://doi.org/10.1016/b978-0-12-091302-2.50032-3

    Chapter  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

    CAS  Google Scholar 

  • Alscher RG, Erturk N, Heath LS (2002) Role of superoxide dismutases [SODs] in controlling oxidative stress in plants. J Exp Bot 53:1331–1341

    PubMed  CAS  Google Scholar 

  • Ashraf MY, Akhtarw K, Sarwar G, Ashraf M (2002) Evaluation of arid and semi-arid ecotypes of guar (Cyamopsis tetragonoloba L.) for salinity (NaCl) tolerance. J Arid Environ 52:473–482

    Google Scholar 

  • Balestrasse KB, Noriega GO, Batlle A, Tomaro ML (2005) Involvement of Heme oxygenase as antioxidant defense in soybean Nodules. Free Radical Res 39:145–151

    CAS  Google Scholar 

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

    CAS  Google Scholar 

  • Baxter CJ, Redestig H, Schauer N, Repsilber D, Patil KR, Nielsen J (2007) The metabolic response of heterotrophic Arabidopsis cells to oxidative stress. Plant Physiol 143:312–325

    PubMed  PubMed Central  CAS  Google Scholar 

  • Beauchamp C, Fridovich I (1971) Superoxide dismutase: improved assays and an assay applicable to acrylamide gels. Anal Biochem 44:276–287

    PubMed  CAS  Google Scholar 

  • 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

    CAS  Google Scholar 

  • Datta R, Sharma R (1999) Temporal and spatial regulation of nitrate reductase and nitrite reductase in greening maize leaves. Plant Sci 144:77–83

    CAS  Google Scholar 

  • 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

    Google Scholar 

  • Demirevska-Kepova K, Simova-Stoilova L, Stoyanova Z, Holzer R, Feller U (2004) Biochemical changes in barley plants after excessive supply of copper and manganese. Environ Exp Bot 52:253–266

    CAS  Google Scholar 

  • Dixit S, Verma K, Shekhawat GS (2014) In vitro evaluation of mitochondrial-chloroplast subcellular localization of heme oxygenase1 [HO1] in Glycine max. Protoplasma 251:671–675

    PubMed  CAS  Google Scholar 

  • Hayat S, Yadav S, Wani AS, Irfan M, Alyemini MN, Ahmad A (2012) Impact of sodium nitroprusside on nitrate reductase, proline and antioxidant system in Solanum lycopersicum under salinity stress. Hortic Environ Biotechnol 53:362–367

    CAS  Google Scholar 

  • 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

    Google Scholar 

  • Kausar F, Shahbaz M, Ashraf M (2013) Protective role of foliar-applied nitric oxide in Triticum aestivum under saline stress. Turk J Bot 37:1155–1165

    CAS  Google Scholar 

  • Liu Y, Xiong Y, Bassham DC (2009) Autophagy is required for tolerance of drought and salt stress in plants. Autophagy 5:954–963

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • Lowry OH, Rosenberg NJ, Farr AL, Randall RJ (1951) Protein measurement with folin phenol reagent. J Biol Chem 193:265–275

    PubMed  CAS  Google Scholar 

  • Lu Y, Lei JQ, Zeng FJ, Zhang B, Liu GJ, Liu B, Li XY (2017) Effect of NaCl-induced changes in growth, photosynthetic characteristics, water status and enzymatic antioxidant system of Calligonum caput-medusae seedlings. Photosynthetica 55:96–106

    CAS  Google Scholar 

  • 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

    Google Scholar 

  • 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 4:483–500

    Google Scholar 

  • Mahawar L, Shekhawat GS (2019) EsHO1 mediated mitigation of NaCl induced oxidative stress and correlation between ROS, antioxidants and HO1 in seedlings of Eruca sativa: underutilized oil yielding crop of arid region. Physiol Mol Biol Plants. https://doi.org/10.1007/s12298-019-00663-7

    Article  PubMed  Google Scholar 

  • Mahawar L, Khator K, Shekhawat GS (2018a) 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 Biotech 3:55–63

    Google Scholar 

  • Mahawar L, Kumar R, Shekhawat GS (2018b) Evaluation of hemeoxygenase1 (HO1) in Cd and Ni induced cytotoxicity and crosstalk with ROS quenching enzyme in two to four leaf stage seedling of Vigna radiata. Protoplasma 255:527–545

    PubMed  CAS  Google Scholar 

  • Maksymiec W, Krupa Z (2006) The effects of short-term exposure to Cd, excess Cu ions and jasmonate on oxidative stress appearing in Arabidopsis thaliana. Environ Exp Bot 57:187–194

    CAS  Google Scholar 

  • Manai J, Kalai T, Gouia H, Corpas FJ (2014) Exogenous nitric oxide (NO) ameliorates salinity-induced oxidative stress in tomato (Solanum lycopersicum) plants. J Soil Sci Plant Nutr 14:433–446

    CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Noriega G, Cruz DS, Batlle A, Tomaro M, Balestrasse K (2012) Heme Oxygenase is involved in the protection exerted by jasmonic acid against Cadmium stress in soybean roots. J Plant Growth Regul 31:79–89

    CAS  Google Scholar 

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

    Google Scholar 

  • Rai V, Vajpayee P, Singh SN, Mehrotra S (2004) Effect of chromium accumulation on photosynthetic pigments, oxidative stress defense system, nitrate reduction, proline level and eugenol content of Ocimum tenuiflorum L. Plant Sci 167:1159–1169

    CAS  Google Scholar 

  • Ramani B, Reeck T, Debez A, Stelzer R, Huchzermeyer B, Schmidt A, Papenbrock J (2006) Aster tripolium L. and Sesuvium portulacastrum L.: two halophytes, two strategies to survive in saline habitats. Plant Physiol Biochem 44:395–408

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Sangwan P, Kumar V, Joshi UN (2014) Effect of chromium (VI) toxicity on enzymes of nitrogen metabolism in clusterbean (Cyamopsis tetragonoloba L.). Enzyme Res. https://doi.org/10.1155/2014/784036

    Article  PubMed  PubMed Central  Google Scholar 

  • Sanita di Toppi L, Gabbrielli R (1999) Responses to cadmium in higher plants. Environ Exp Bot 41:105–130

    Google Scholar 

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

    CAS  Google Scholar 

  • 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. Appl Biochem Biotechnol 178:267–284

    PubMed  CAS  Google Scholar 

  • Sharma SS, Dietz KJ (2009) The relationship between metal toxicity and cellular redox imbalance. Trends Plant Sci 14:43–50

    PubMed  CAS  Google Scholar 

  • Sharma KK, Mehra SP (2009) The Thar of Rajasthan (India): Ecology and conservation of a desert ecosystem. In: Sivaperuman C (ed) Faunal ecology and conservation of the great indian desert. Springer, Berlin, pp 1–5

    Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Shekhawat GS, Verma K, Jana S, Singh K, Teotia P, Prasad A (2010) In vitro biochemical evaluation of cadmium tolerance mechanism in callus and seedlings of Brassica juncea. Protoplasma 239:31–38

    PubMed  CAS  Google Scholar 

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

    Google Scholar 

  • Shekhawat GS, Parihar S, Mahawar L, Khator K, Bulchandani N (2019) Bilin metabolism in plants: Structure, function and Hemeoxygenase regulation of Bilin biosynthesis. eLS 2001:1–13

    Google Scholar 

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

    Google Scholar 

  • Thomas C, Robertson MJ, Fukaic S, Peoples MB (2004) The effect of timing and severity of water deficit on growth, development, yield accumulation and nitrogen fixation of mungbean. Field Crops Res 86:67–80

    Google Scholar 

  • Tripathi BN, Singh V, Ezaki B, Sharma V, Gaur JP (2013) Mechanism of Cu and Cd-Induced Proline Hyper accumulation in Triticum aestivum (Wheat). J Plant Growth Regul 32:799–808

    CAS  Google Scholar 

  • Verma K, Shekhawat GS, Sharma A, Mehta SK, Sharma V (2008) Cadmium induced oxidative stress and changes in soluble and ionically bound cell wall peroxidase activities in roots of seedling and 3–4 leaf stage plants of Brassica juncea (L.) Czern. Plant Cell Rep 27:1261–1269

    PubMed  CAS  Google Scholar 

  • Verma K, Mehta SK, Shekhawat GS (2013) Nitric oxide (NO) counteracts cadmium induced cytotoxic processes mediated by reactive oxygen species (ROS) in Brassica juncea: cross-talk between ROS, NO and antioxidant responses. Biometals 26:255–269

    PubMed  CAS  Google Scholar 

  • Verma K, Dixit S, Shekhawat GS, Alam A (2015) Antioxidant activity of heme oxygenase1 in Brassica juncea (L.) Czern (Indian mustard) under salt stress. Turk J Biol 39:540–549

    CAS  Google Scholar 

  • Wang Y, Gu W, Meng Y, Xie T, Li L, Li J, Shi W (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

    PubMed  PubMed Central  Google Scholar 

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

    CAS  Google Scholar 

  • Xie Y, Mao Y, Xu S, Zhou H, Duan X, Cui W, Zhang J, Xu G (2015) Heme-heme oxygenase1 system is involved in ammonium tolerance by regulating antioxidant defence in Oryza sativa. Plant Cell Environ 38:129–143

    PubMed  CAS  Google Scholar 

  • Arora J, Goyal S, Ramawat KG (2010) Biodiversity, biology and conservation of medicinal plants of the Thar Desert. In: Ramawat KG (ed) Desert plants. Springer, Berlin. https://doi.org/10.1007/978-3-642-02550-1

    Chapter  Google Scholar 

  • Yannarelli GG, Noriega GO, Batlle A, Tomaro ML (2006) Heme oxygenase up regulation in ultraviolet-B irradiated soybean plants involves reactive oxygen species. Planta 224:154–1162

    Google Scholar 

  • Yildiztugay E, Sekmen AH, Turkan I (2011) Elucidation of physiological and biochemical mechanisms of an endemic halophyte Centaurea tuzgoluensis under salt stress. Plant Physiol Biochem 49:816–824

    PubMed  CAS  Google Scholar 

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

    Google Scholar 

  • 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. Int J Cell Biol. https://doi.org/10.1155/2009/848516

    Article  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

The authors gratefully acknowledge University Grants Commission, New Delhi for providing financial assistance through centre for advanced study program.

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Correspondence to Gyan Singh Shekhawat.

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Khator, K., Mahawar, L. & Shekhawat, G.S. NaCl induced oxidative stress in legume crops of Indian Thar Desert: an insight in the cytoprotective role of HO1, NO and antioxidants. Physiol Mol Biol Plants 26, 51–62 (2020). https://doi.org/10.1007/s12298-019-00728-7

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