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Mechanistic Elucidation of Salicylic Acid and Sulphur-Induced Defence Systems, Nitrogen Metabolism, Photosynthetic, and Growth Potential of Mungbean (Vigna radiata) Under Salt Stress

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Abstract

The potential of plant nutrients (such as sulphur, S) and phytohormones (such as salicylic acid, SA) has been explored in isolated studies by researchers in controlling the impact of abiotic stresses such as salinity in plants. However, information is scanty on the major mechanisms underlying the role of S and/or SA in modulation of enzymes involved in nitrogen (N) assimilation, GOGAT cycle, and antioxidant defence system; the cellular status of N-containing osmolyte proline, glucose, S-containing compounds; and their cumulative role in photosynthesis functions and growth in crop plants. The present study aimed to assess the role of cumulative effect of SA and S (SO42−) mediated induction of N assimilatory enzymes, GOGAT cycle, N-osmolyte proline and its metabolizing enzymes, glyoxylase enzymes, and antioxidant capacity in mungbean (Vigna radiata L.) exposed to NaCl with or without SO42− and SA. Salt-exposed V. radiate showed differential elevations in damage (O.2, H2O2, lipid peroxidation; glucose) and defence (ascorbate peroxidase, APX; glutathione reductase, GR; superoxide dismutase, SOD; reduced GSH; proline) and inhibitions in the activities of NR and NiR; N content, photosynthesis, photosynthetic N-use-efficiency (NUE), and growth. The separate supplementation of SA and SO42− to 50 mM NaCl almost equally strengthened the antioxidant machinery and diminished NaCl-accrued damages. However, combined supply of SA and SO42− to NaCl-exposed cultivars led to significant improvements in NR and NiR activities, the accumulation of N, GSH, proline, enhanced activity of APX, GR, and reduced activity of SOD, and also decreases in O.2, H2O2, lipid peroxidation and glucose. These observations were corroborated with SA, SO42− and NaCl-mediated changes in the traits of photosynthesis and growth, stomatal behaviour, and the polypeptide patterns of Rubisco in V. radiata. Overall, in V. radiata, SA-mediated higher enhancements in the activity of N assimilatory enzymes (NR, NiR, and GS), increase in the N and proline, and GSH; and decreases in the contents of Na+ and Cl ions, and glucose (a photosynthesis repressor); maintenance of a fine tuning among SOD, APX, and GR enzymes; and higher minimization of ROS (O.2, H2O2) and lipid peroxidation finally led to a higher promotion in photosynthesis and growth.

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References

  • Anjum NA, Gill R, Kaushik M, Hasanuzzaman M, Pereira E, Ahmad I, Gill SS (2015a) ATP sulfurylase, sulfur-compounds, and plant stress tolerance. Front in Plant Sci 6:210

    Google Scholar 

  • Anjum NA, Sofo A, Scopa A, Roychoudhury A, Gill SS, Iqbal M (2015b) Lipids and proteins - major targets of oxidative modifications in abiotic stressed plants. Environ Sci Pollut Res 22:4099–4121

    CAS  Google Scholar 

  • Arfan M, Athar HR, Ashraf M (2007) Does exogenous application of salicylic acid through the rooting medium modulate growth and photosynthetic capacity in two differently adapted spring wheat cultivars under salt stress. J Plant Physiol 164:685–694

    CAS  PubMed  Google Scholar 

  • Badar-uz-Zaman AA, Salim M, Niazi BH (2002) Role of sulphur for potassium/sodium ratio in sunflower under saline conditions. Helia 25:69–78

    Google Scholar 

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

    CAS  Google Scholar 

  • Beyer WF Jr, Fridovich I (1987) Assaying for superoxide dismutase activity: some large consequences of minor changes in conditions. Anal Biochem 161:559–566

    CAS  PubMed  Google Scholar 

  • Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254

    CAS  PubMed  Google Scholar 

  • Carvalho LC, Esquível MG, Martins I, Ricardo CP, Amâncio S (2005) Monitoring the stability of Rubisco in micropropagated grapevine (Vitis vinifera L.) by two-dimensional electrophoresis. J Plant Physiol 162:365–374

    CAS  PubMed  Google Scholar 

  • Chao YY, Chen CY, Huang WD, Kao CH (2010) Salicylic acid-mediated hydrogen peroxide accumulation and protection against Cd toxicity in rice leaves. Plant Soil 329:327–337

    CAS  Google Scholar 

  • Chen J, Zhang Y, Wang C, Lü W (2011) Proline induces calcium-mediated oxidative burst and salicylic acid signaling. Amino Acids 40:1473–1484

    CAS  PubMed  Google Scholar 

  • Daud MK, Sun Y, Dawood M, Hayat Y, Variath MT, Wu YX, Mishkat U, Najeeb U, Zhu S (2009) Cadmium-induced functional and ultrastructural alterations in roots of two transgenic cotton cultivars. J Hazard Mater 161:463–473

    CAS  PubMed  Google Scholar 

  • Deinlein U, Stephan AB, Horie T, Luo W, Xu G, Schroeder JI (2014) Plant salt-tolerance mechanisms. Trend Plant Sci 19:371–379

    CAS  Google Scholar 

  • Dhindsa RH, Plumb-Dhindsa P, Thorpe TA (1981) Leaf senescence correlated with increased level of membrane permeability, lipid peroxidation and decreased level of SOD and CAT. J Exp Bot 32:93–101

    CAS  Google Scholar 

  • Doderer A, Kokkelink I, van der Veen S, Valk BE, Schram A, Douma AC (1992) Purification and characterization of two lipoxygenase isoenzymes from germinating barley. Biochem Biophys Acta 1120:97–104

    CAS  PubMed  Google Scholar 

  • Fatma M, Khan MI, Masood A, Khan NA (2013) Coordinate changes in assimilatory sulfate reduction are correlated to salt tolerance: involvement of phytohormones. Annu Rev Res Biol 3:267–295

    Google Scholar 

  • Fatma M, Asgher M, Masood A, Khan NA (2014) Excess sulfur supplementation improves photosynthesis and growth in mustard under salt stress through increased production of glutathione. Environ Exp Bot 107:55–63

    CAS  Google Scholar 

  • Fatma M, Masood A, Per TS, Khan NA (2016) Nitric oxide alleviates salt stress inhibited photosynthetic performance by interacting with sulfur assimilation in mustard. Front Plant Sci 7:521

    PubMed  PubMed Central  Google Scholar 

  • Foyer CH, Halliwell B (1976) The presence of glutathione and glutathione reductase in chloroplasts: a proposed role in ascorbic acid metabolism. Planta 133:21–25

    CAS  PubMed  Google Scholar 

  • Gharbi E, Martínez J, Benahmed H, Dailly H, Quinet M, Lutts S (2017) The salicylic acid analog 2,6-dichloroisonicotinic acid has specific impact on the response of the halophyte plant species Solanum chilense to salinity. Plant Growth Regul 82:17–525

    Google Scholar 

  • Giannopolitis CN, Ries SK (1977) Superoxide dismutases:II. Purification and quantitative relationship with water-soluble protein in seedlings. Plant Physiol 59:315–318

    CAS  PubMed  PubMed Central  Google Scholar 

  • Griffith OW (1980) Determination of glutathione and glutathione disulfide using glutathione reductase and 2-vinylpyridine. Anal Biochem 106:207–212

    CAS  PubMed  Google Scholar 

  • Gunes A, Inal A, Alpaslan M, Cicek N, Guneri E, Eraslan F, Guzelordu T (2005) Effects of exogenously applied salicylic acid on the induction of multiple stress tolerance and mineral nutrition in maize (Zea mays L.). Arch Agron Soil Sci 51:687–695

    CAS  Google Scholar 

  • Gunes A, Inal A, Alpaslan M, Eraslan F, Bagci EG, Cicek N (2007) Salicylic acid induced changes on some physiological parameters symptomatic for oxidative stress and mineral nutrition in maize (Zea mays L.) grown under salinity. J Plant Physiol 164:728–736

    CAS  PubMed  Google Scholar 

  • Hasanuzzaman M, Nahar K, Anee TI, Khan MIR, Fujita M (2018) Silicon-mediated regulation of antioxidant defense and glyoxalase systems confers drought stress tolerance in Brassica napus L. South Africa J Bot 115:50–57

    CAS  Google Scholar 

  • Hayzer DJ, Leisinger TH (1980) The gene-enzyme relationships of proline biosynthesis in Escherichia coli. Microbiology 118:287–293

    CAS  Google Scholar 

  • Hewitt EJ (1966) Sand and water culture methods used in study of plant nutrition, 2nd edn. Common wealth Agricultural Bureaux Farnham Royal, Bucks

    Google Scholar 

  • Huang AH, Cavalieri AJ (1979) Proline oxidase and water stress-induced proline accumulation in spinach leaves. Plant Physiol 63:531–535

    CAS  PubMed  PubMed Central  Google Scholar 

  • Hussain SJ, Masood A, Anjum NA, Khan NA (2019) Sulfur-mediated control of salinity impact on photosynthesis and growth in mungbean cultivars screened for salt tolerance involves glutathione and proline metabolism, and glucose sensitivity. Acta Physiol Plant 41:1–13

    Google Scholar 

  • Jagendorf AT, Takabe T (2001) Inducers of glycinebetaine synthesis in barley. Plant Physiol 127:1827–1835

    CAS  PubMed  PubMed Central  Google Scholar 

  • Jain M, Nagar P, Sharma A, Batth R, Aggarwal S, Kumari S, Mustafiz A (2018) GLYI and D-LDH play key role in methylglyoxal detoxification and abiotic stress tolerance. Sci Rep 8(1):1–9

    Google Scholar 

  • Khan MIR, Iqbal N, Masood A, Per TS, Khan NA (2013) Salicylic acid alleviates adverse effects of heat stress on photosynthesis through changes in proline production and ethylene formation. Plant Signal Behav 8:e26374

    PubMed  PubMed Central  Google Scholar 

  • Khan MIR, Asgher M, Khan NA (2014) Alleviation of salt-induced photosynthesis and growth inhibition by salicylic acid involves glycinebetaine and ethylene in mungbean (Vigna radiata L.). Plant Physiol Biochem 80:67–74

    CAS  PubMed  Google Scholar 

  • Khan MIR, Fatma M, Per TS, Anjum NA, Khan NA (2015) Salicylic acid-induced abiotic stress tolerance and underlying mechanisms in plants. Front Plant Sci 6:462

    PubMed  PubMed Central  Google Scholar 

  • Khan MIR, Jahan B, Alajmi MF, Rehman MT, Khan NA (2019) Exogenously-sourced ethylene modulates defense mechanisms and promotes tolerance to zinc stress in mustard (Brassica juncea L). Plants 8:540

    CAS  PubMed Central  Google Scholar 

  • Kuo TM, Warner RL, Kleinhofs A (1982) In vitro stability of nitrate reductase from barley leaves. Phytochemistry 21:531–533

    CAS  Google Scholar 

  • Laemmli UK, Beguin F, Gujer-Kellenberger G (1970) A factor preventing the major head protein of bacteriophage T4 from random aggregation. J Mol Biol 47:69–85

    CAS  PubMed  Google Scholar 

  • Li G, Peng X, Wei L, Kang G (2013) Salicylic acid increases the contents of glutathione and ascorbate and temporally regulates the related gene expression in salt-stressed wheat seedlings. Gene 529:321–325

    CAS  PubMed  Google Scholar 

  • Li T, Hu Y, Du X, Tang H, Shen C, Wu J (2014) Salicylic acid alleviates the adverse effects of salt stress in Torreya grandis cv. Merrillii seedlings by activating photosynthesis and enhancing antioxidant systems. PLoS ONE 9:e109492

    PubMed  PubMed Central  Google Scholar 

  • Lindner RC (1944) Rapid analytical methods for some of the more common inorganic constituents of plant tissues. Plant Physiol 19:76

    CAS  PubMed  PubMed Central  Google Scholar 

  • Machado RMA, Serralheiro RP (2017) Soil salinity: effect on vegetable crop growth. Management practices to prevent and mitigate soil salinization. Horticulturae 3:30

    Google Scholar 

  • Masood A, Iqbal N, Khan NA (2012) Role of ethylene in alleviation of cadmium-induced photosynthetic capacity inhibition by sulphur in mustard. Plant Cell Environ 35:524–533

    CAS  PubMed  Google Scholar 

  • Moharekar ST, Lokhande SD, Hara T, Tanaka R, Tanaka A, Chavan PD (2003) Effects of salicylic acid on chlorophyll and carotenoid contents on wheat and moong seedlings. Photosynthetica 41:315–317

    CAS  Google Scholar 

  • Mostofa MG, Fujita M (2013) Salicylic acid alleviates copper toxicity in rice (Oryza sativa L.) seedlings by up-regulating antioxidative and glyoxalase systems. Ecotoxicology 22:959–973

    CAS  PubMed  Google Scholar 

  • Mostofa MG, Fujita M, Tran LSP (2015) Nitric oxide mediates hydrogen peroxide-and salicylic acid-induced salt tolerance in rice (Oryza sativa L.) seedlings. Plant Growth Regul 77:265–277

    CAS  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Mustafiz A, Sahoo KK, Singla-Pareek SL, Sopory SK (2010) Metabolic engineering ofglyoxalase pathwayfor enhancing stress tolerance in plants. Methods Mol Biol 639:95–118

    CAS  PubMed  Google Scholar 

  • Nakagawa H, Poulle M, Oaks A (1984) Characterization of nitrate reductase from corn leaves (Zea mays cv W64A × W182E): two molecular forms of the enzyme. Plant Physiol 75:285–289

    CAS  PubMed  PubMed Central  Google Scholar 

  • Nakano Y, Asada K (1981) Hydrogen peroxide is scavenged by ascorbate-specific peroxidase in spinach chloroplasts. Plant Cell Physiol 22:867–880

    CAS  Google Scholar 

  • Nazar R, Iqbal N, Masood A, Syeed S, Khan NA (2011a) Understanding the significance of sulphur in improving salinity tolerance in plants. Environ Exp Bot 70:80–87

    CAS  Google Scholar 

  • Nazar R, Iqbal N, Syeed S, Khan NA (2011b) Salicylic acid alleviates decreases in photosynthesis under salt stress by enhancing nitrogen and sulphur assimilation and antioxidant metabolism differentially in two mungbean cultivars. J Plant Physiol 168:807–815

    CAS  PubMed  Google Scholar 

  • Nazar R, Umar S, Khan NA (2015) Exogenous salicylic acid improves photosynthesis and growth through increase in ascorbate-glutathione metabolism and S assimilation in mustard under salt stress. Plant Signal Behav 10:e1003751

    PubMed  PubMed Central  Google Scholar 

  • Nisarga KN, Vemanna RS, Kodekallu Chandrashekar B, Rao H, Vennapusa AR, Narasimaha A, Makarla U, Basavaiah MR (2017) Aldo-ketoreductase 1 (AKR1) improves seed longevity in tobacco and rice by detoxifying reactive cytotoxic compounds generated during ageing. Rice (NY) 10(1):11

    Google Scholar 

  • Okuda T, Matsuda Y, Yamanaka A, Sagisaka S (1991) Abrupt increase in the level of hydrogen peroxide in leaves of winter wheat is caused by cold treatment. Plant Physiol 97:1265–1267

    CAS  PubMed  PubMed Central  Google Scholar 

  • Palma F, López-Gómez M, Tejera NA, Lluch C (2013) Salicylic acid improves the salinity tolerance of Medicago sativa in symbiosis with Sinorhizobium meliloti by preventing nitrogen fixation inhibition. Plant Sci 208:75–82

    CAS  PubMed  Google Scholar 

  • Pancheva TV, Popova LP, Uzunova AN (1996) Effects of salicylic acid on growth and photosynthesis in barley plants. J Plant Physiol 149:57–63

    CAS  Google Scholar 

  • Parihar P, Singh S, Singh R, Singh VP, Prasad SM (2015) Effect of salinity stress on plants and its tolerancestrategies: a review. Environ Sci Pollut Res 22:4056–4075

    CAS  Google Scholar 

  • Per TS, Khan NA, Reddy PS, Masood A, Hasanuzzaman M, Khan MIR, Anjum NA (2017) Approaches in modulating proline metabolism in plants for salt and drought stress tolerance: phytohormones, mineral nutrients and transgenics. Plant Physiol Biochem 115:126–140

    CAS  PubMed  Google Scholar 

  • Principato GB, Rosi G, Talesa V, Giovanni E, Uotila L (1987) Purification and characterization of two forms of glyoxalase II from the liver and brain of Wistar rats. Biochim Biophys Acta 911:349–355

    CAS  PubMed  Google Scholar 

  • Sairam RK, Srivastava GC (2002) Changes in antioxidant activity in sub-cellular fractions of tolerant and susceptible wheat genotypes in response to long term salt stress. Plant Sci 162:897–904

    CAS  Google Scholar 

  • Sehar Z, Masood A, Khan NA (2019) Nitric oxide reverses glucose-mediated photosynthetic repression in wheat (Triticum aestivum L.) under salt stress. Environ Exp Bot 161:277–289

    CAS  Google Scholar 

  • Takashima T, Hikosaka K, Hirose T (2004) Photosynthesis or persistence: nitrogen allocationin leaves of evergreen and deciduous Quercus species. Plant Cell Environ 27:1047–1054

    CAS  Google Scholar 

  • Teh CY, Shaharuddin NA, Ho CL, Mahmood M (2016) Exogenous proline significantly affects the plant growth and nitrogen assimilation enzymes activities in rice (Oryza sativa) under salt stress. Acta Physiol Plant 38:151

    Google Scholar 

  • Tholen D, Pons TL, Voesenek LA, Poorter H (2007) Ethylene insensitivity results in down-regulation of Rubisco expression and photosynthetic capacity in tobacco. Plant Physiol 144:1305–1315

    CAS  PubMed  PubMed Central  Google Scholar 

  • Usuda H (1985) The activation state of ribulose1, 5-bisphosphate carboxylase in maize leaves in dark and light. Plant Cell Physiol 26:1455–1463

    CAS  Google Scholar 

  • Valentine AJ, Kleinert A, Benedito VA (2017) Adaptive strategies for nitrogen metabolism in phosphatedeficient legume nodules. Plant Sci 256:46–52

    CAS  PubMed  Google Scholar 

  • Vernooij B, Friedrich L, Goy PA, Staub T, Kessmann H, Ryals J (1995) 2,6-dichloroisonicotinic acid-induced resistance to pathogens without the accumulation of salicylic acid. Mol Plant-Microbe Interact 8:228–234

    CAS  Google Scholar 

  • Wang JF, Jiang D, Yu ZW, Cao WX (2003) Effects of nitrogen rates on grain yield and protein content of wheat and its physiological basis. Sci Agric Sin 36:513–520

    Google Scholar 

  • Wang C, Zhang S, Wang P, Hou J, Qian J, Ao Y, Li L (2011) Salicylic acid involved in the regulation of nutrient elements uptake and oxidative stress in Vallisneria natans (Lour.) Hara under Pb stress. Chemosphere 84:136–142

    CAS  PubMed  Google Scholar 

  • Wasti S, Mimouni H, Smiti S, Zid E, Ben Ahmed H (2012) Enhanced salt tolerance of tomatoes by exogenous salicylic acid applied through rooting medium. Omics J Integ Biol 16:200–207

    CAS  Google Scholar 

  • Wild R, Ooi L, Srikanth V, Münch G (2012) A quick, convenient and economical method for the reliable determination of methylglyoxal in millimolar concentrations: the N-acetyl-L-cysteine assay. Anal Bioanal Chem 403:2577–2581

    CAS  PubMed  Google Scholar 

  • Wirtz M, Droux M (2005) Synthesis of the sulfur amino acids: cysteine and methionine. Photosynth Res 86:345–362

    CAS  PubMed  Google Scholar 

  • Yoshida S, Tamaoki M, Ioki M, Ogawa D, Sato Y, Aono M, Kubo A, Saji S, Saji H, Satoh S, Nakajima N (2009) Ethylene and salicylic acid control glutathione biosynthesis inozone-exposed Arabidopsis thaliana. Physiol Plant 136:284–298

    CAS  PubMed  Google Scholar 

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Acknowledgements

S.J.H. would like to acknowledge the UGC for financial support in the form of UGC non-NET fellowship. Authors are thankful to Dr. C. Viswanathan, Division of Plant Physiology, IARI, New Delhi (India) for HPLC-based analysis of glucose.

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NAK and MIRK conceived the idea of this study; SJH carried out experiments and analysed the data; SJH, NAK,and MIRK prepared the first draft; NAK, MIRK, NAA, and AM improved the manuscript.

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Correspondence to Nafees A. Khan or M. Iqbal R. Khan.

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Hussain, S.J., Khan, N.A., Anjum, N.A. et al. Mechanistic Elucidation of Salicylic Acid and Sulphur-Induced Defence Systems, Nitrogen Metabolism, Photosynthetic, and Growth Potential of Mungbean (Vigna radiata) Under Salt Stress. J Plant Growth Regul 40, 1000–1016 (2021). https://doi.org/10.1007/s00344-020-10159-4

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