Skip to main content
SpringerLink
Log in

Involvement of Ethylene in Reversal of Salt Stress by Salicylic Acid in the Presence of Sulfur in Mustard (Brassica juncea L.)

  • Published:
Journal of Plant Growth Regulation Aims and scope Submit manuscript

Abstract

The involvement of ethylene in reversal of salt (NaCl; 50 mM) stress on photosynthetic activity and growth by salicylic acid (SA; 0.5 mM) together with sulfur (S; 2.0 mM) was studied in mustard (Brassica juncea L. cv. Pusa Vijay). Application of SA plus SO42− improved photosynthetic activity through markedly increased S-assimilation, strengthening antioxidant defense system and limiting NaCl-accrued oxidative consequences more conspicuously than their individual effect in B. juncea under 50 mM NaCl stress. Since SA acts as an inhibitor of ethylene and S-assimilation is associated with ethylene synthesis, we tried to figure out the interaction of ethylene in SA and SO42−-mediated salt tolerance. The involvement of ethylene was studied by supplementing salt-treated plants with 200 µL L−1 ethephon (an ethylene-releasing compound) or 100 µM norbornadiene (NBD, ethylene action inhibitor) to SA and SO42− treatments. Ethephon supplemented to NaCl-treated plants showed optimal ethylene formation, increasing ethylene sensitivity to enhance photosynthesis by affecting antioxidative capacity of plants. SA plus SO42− treatment decreased stress ethylene production and optimized ethylene formation under NaCl stress that contributed in the maintenance of high photosynthetic rate, which was reversed with NBD. NaCl-treated plants receiving SA plus SO42− and supplemented with NBD showed inhibited photosynthetic characteristics and growth, with minimal S-assimilation capacity, activity of antioxidant enzymes and GSH content. This showed that the reversal of salt stress by SA plus SO42− was through ethylene involvement. Overall, ethylene intervened the effect of SA in the presence of SO42− to induce S-assimilation, upregulated the enzymatic and non-enzymatic antioxidants, and imparted NaCl tolerance in plants.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

References

  • Ahmed W, Imran M, Yaseen M, Ul Haq T, Jamshaid MU, Rukh S, Khan MA (2020) Role of salicylic acid in regulating ethylene and physiological characteristics for alleviating salinity stress on germination, growth and yield of sweet pepper. Peer J 8:e8475

    Article  PubMed  PubMed Central  Google Scholar 

  • Anjum NA, Umar S, Chan MT (2010) Ascorbate-Glutathione Pathway and Stress Tolerance in Plants. Springer, Dordrecht

    Book  Google Scholar 

  • Anjum NA, Aref IM, Duarte AC, Pereira E, Ahmad I, Iqbal M (2014) Glutathione and proline can coordinately make plants withstand the joint attack of metal(loid) and salinity stresses. Front Plant Sci 5:662

    Article  PubMed  PubMed Central  Google Scholar 

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

    Article  PubMed  PubMed Central  Google Scholar 

  • Asgher M, Khan NA, Khan MIR, Fatma M, Masood A (2014) Ethylene production is associated with alleviation of cadmium-induced oxidative stress by sulfur in mustard types differing in ethylene sensitivity. Ecotoxicol Environ Saf 106:54–61

    Article  CAS  PubMed  Google Scholar 

  • Ashraf M (2009) Biotechnological approach of improving plant salt tolerance using antioxidants as markers. Biotechnol Adv 27:84–93

    Article  CAS  PubMed  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

    Article  CAS  PubMed  Google Scholar 

  • Cao WH, Liu J, He XJ, Mu RL, Zhou HL, Chen SY, Zhang JS (2007) Modulation of ethylene responses affects plant salt-stress responses. Plant Physiol 143:707–719

    Article  CAS  PubMed  PubMed Central  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

    Article  CAS  PubMed  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

    Article  CAS  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. Ann Res Rev Biol 10:267–295

    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

    Article  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

    Article  PubMed  PubMed Central  Google Scholar 

  • Fatma M, Iqbal N, Gautam H, Sehar Z, Sofo A, D’Ippolito I, Khan NA (2021) Ethylene and sulfur coordinately modulate the antioxidant system and ABA accumulation in mustard plants under salt stress. Plants 10:180

    Article  CAS  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

    Article  CAS  PubMed  Google Scholar 

  • Gaitonde MK (1967) A spectrophotometric method for the direct determination of cysteine in the presence of other naturally occurring amino acids. Biochem J 104:627

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Giannopolitis CN, Ries SK (1977) Superoxide dismutases, occurrence in higher plants. Plant Physiol 59:309–314

    Article  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

    Article  CAS  PubMed  Google Scholar 

  • Gururani MA, Mohanta TK, Bae H (2015) Current understanding of the interplay between phytohormones and photosynthesis under environmental stress. Inter J Mol Sci 16:19055–19085

    Article  CAS  Google Scholar 

  • Herrera-Vásquez A, Salinas P, Holuigue L (2015) Salicylic acid and reactive oxygen species interplay in the transcriptional control of defense genes expression. Front Plant Sci 6:171

    Article  PubMed  PubMed Central  Google Scholar 

  • Hewitt EJ (1966) Sand and Water Culture Methods Used in the Study of Plant Nutrition Technical Communication No 22, Commonw Bur Hortic Plant Crops, East Malling, UK: CAB Rev 2nd ed., pp.547

  • 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 41:129

    Article  Google Scholar 

  • Hussain SJ, Khan NA, Anjum NA, Masood A, Khan MIR (2021) 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

    Article  CAS  Google Scholar 

  • Iqbal N, Khan NA, Nazar R, Silva JA (2012) Ethylene-stimulated photosynthesis results from increased nitrogen and sulfur assimilation in mustard types that differ in photosynthetic capacity. Environ Exp Bot 78:84–90

    Article  CAS  Google Scholar 

  • Iqbal N, Umar S, Khan NA (2015) Nitrogen availability regulates proline and ethylene production and alleviates salinity stress in mustard (Brassica juncea). J Plant Physiol 178:84–91

    Article  CAS  PubMed  Google Scholar 

  • Iqbal N, Khan NA, Ferrante A, Trivellini A, Francini A, Khan MIR (2017) Ethylene role in plant growth, development and senescence: interaction with other phytohormones. Front Plant Sci 8:475

    Article  PubMed  PubMed Central  Google Scholar 

  • Isayenkov SV, Maathuis FJM (2019) Plant salinity stress, many unanswered question remain. Front Plant Sci 10:80

    Article  PubMed  PubMed Central  Google Scholar 

  • Jahan B, Iqbal N, Fatma M, Sehar Z, Sofo A, D’Ippolito I, Khan NA (2021a) Ethylene supplementation combined with split application of nitrogen and sulfur protects salt-inhibited photosynthesis through optimization of proline metabolism and antioxidant system in mustard (Brassica juncea L.). Plants 10:1303

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jahan B, Rasheed F, Sehar Z, Fatma M, Iqbal N, Masood A, Anjum NA, Khan NA (2021b) Coordinated role of nitric oxide, ethylene, nitrogen, and sulfur in plant salt stress tolerance. Stresses 1:181–199

    Article  Google Scholar 

  • Jahan B, Sehar Z, Masood A, Anjum NA, Khan MIR, Khan NA (2019) Sulfur availability potentiates phytohormones-mediated action in plants. In: Plant Signaling Molecules - Role and Regulation Under Stressful Environments, Woodhead Publishing pp. 287–301

  • Jamil A, Riaz S, Ashraf M, Foolad MR (2011) Gene expression profiling of plants under salt stress. Critic Rev Plant Sci 30:435–458

    Article  Google Scholar 

  • Jia H, Chen S, Liu D, Liesche J, Shi C, Wang J, Ren M, Wang X, Yang J, Shi W, Li J (2018) Ethylene-induced hydrogen sulfide negatively regulates ethylene biosynthesis by persulfidation of ACO in tomato under osmotic stress. Front Plant Sci 9:1517

    Article  PubMed  PubMed Central  Google Scholar 

  • Kazan K (2015) Diverse roles of jasmonates and ethylene in abiotic stress tolerance. Trends Plant Sci 20(4):219–229

    Article  CAS  PubMed  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

    Article  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

    Article  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 30:462

    Google Scholar 

  • Khan NA, Asgher M, Per TS, Masood A, Fatma M, Khan MIR (2016) Ethylene potentiates sulfur-mediated reversal of cadmium inhibited photosynthetic responses in mustard. Front Plant Sci 7:1628

    Article  PubMed  PubMed Central  Google Scholar 

  • Kopriva S, Talukdar D, Takahashi H, Hell R, Sirko A, D’Souza SF, Talukdar T (2016) Editorial: Frontiers of sulfur metabolism in plant growth, development, and stress response. Front Plant Sci 6:1220

    Article  PubMed  PubMed Central  Google Scholar 

  • Kuo TM, Warner RL, Kleinhofs A (1982) In vitro stability of nitrate reductase from barley leaves. Phytochem 21(3):531–533

    Article  CAS  Google Scholar 

  • Lappartient AG, Touraine B (1996) Demand-driven control of root ATP sulfurylase activity and SO42- uptake in intact canola (the role of phloem-translocated glutathione). Plant Physiol 111:147–157

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Leslie CA, Romani RJ (1986) Salicylic acid, a new inhibitor of ethylene biosynthesis. Plant Cell Rep 5:144–146

    Article  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

    Article  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

    Article  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(1):76

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Masood A, Khan MI, Fatma M, Asgher M, Per TS, Khan NA (2016) Involvement of ethylene in gibberellic acid-induced sulfur assimilation, photosynthetic responses, and alleviation of cadmium stress in mustard plant. Plant Physiol Biochem 104:1–10

    Article  CAS  PubMed  Google Scholar 

  • Mateo A, Funck D, Mühlenbock P, Kular B (2006) Mullineaux PM, Karpinski S. Controlled levels of salicylic acid are required for optimal photosynthesis and redox homeostasis. J Exp Bot 57:1795–1807

    Article  CAS  PubMed  Google Scholar 

  • Mittal S, Kumari N, Sharma V (2012) Differential response of salt stress on Brassica juncea, photosynthetic performance, pigment, proline, D1 and antioxidant enzymes. Plant Physiol Biochem 54:17–26

    Article  CAS  PubMed  Google Scholar 

  • Miura K, Tada Y (2014) Regulation of water, salinity, and cold stress responses by salicylic acid. Front Plant Sci 5:4

    Article  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  Google Scholar 

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

    Article  CAS  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, Syeed S, Khan NA (2011) Salicylic acid alleviates decreases in photosynthesis under salt stress by enhancing nitrogen and sulfur assimilation and antioxidant metabolism differentially in two mungbean cultivars. J Plant Physiol 168:807–815

    Article  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

    Article  PubMed  PubMed Central  Google Scholar 

  • Novozamsky I, Houba VJ, Van Eck R, Van Vark W (1983) A novel digestion technique for multi-element plant analysis. Commun Soil Sci Plant Anal 14:239–248

    Article  CAS  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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rasheed F, Sehar Z, Masood A, Khan NA (2018) Sulfur-use-efficiency evaluation in Brassica juncea genotypes under salinity stress. J Funct Environ Bot 8:12–22

    Article  Google Scholar 

  • Rasheed F, Anjum NA, Masood A, Sofo A, Khan NA (2020) The key roles of salicylic acid and sulfur in plant salinity stress tolerance. J Plant Growth Regul 30:1–4

    Google Scholar 

  • Rivas-San Vicente M, Plasencia J (2011) Salicylic acid beyond defence, its role in plant growth and development. J Exp Bot 62:3321–3338

    Article  CAS  PubMed  Google Scholar 

  • Riyazuddin R, Verma R, Singh K, Nisha N, Keisham M, Bhati KK, Kim ST, Gupta R (2020) Ethylene: A master regulator of salinity stress tolerance in plants. Biomolecules 10:959

    Article  CAS  PubMed Central  Google Scholar 

  • 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 

  • Sehar Z, Iqbal N, Khan MIR, Masood A, Rehman MT, Hussain A, Khan NA (2021) Ethylene reduces glucose sensitivity and reverses photosynthetic repression through optimization of glutathione production in salt-stressed wheat (Triticum aestivum L.). Sci Rep 11:1–12

    Article  Google Scholar 

  • Shahbaz M, Ashraf M (2013) Improving salinity tolerance in cereals. Critic Rev Plant Sci 32:237–249

    Article  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Syeed S, Sehar Z, Masood A, Anjum NA, Khan NA (2021) Control of elevated ion accumulation, oxidative stress, and lipid peroxidation with salicylic acid-induced accumulation of glycinebetaine in salinity-exposed Vigna radiata L. Appl Biochem Biotechnol. https://doi.org/10.1007/s12010-021-03595-9

    Article  PubMed  Google Scholar 

  • Szalai G, Kellős T, Galiba G, Kocsy G (2009) Glutathione as an antioxidant and regulatory molecule in plants under abiotic stress conditions. J Plant Growth Regul 28:66–80

    Article  CAS  Google Scholar 

  • Tao JJ, Chen HW, Ma B, Zhang WK, Chen SY, Zhang JS (2015) The role of ethylene in plants under salinity stress. Front Plant Sci 6:1059

    Article  PubMed  PubMed Central  Google Scholar 

  • Tari I, Csiszár J, Horváth E, Poór P, Takács Z, Szepesi Á (2015) The alleviation of the adverse effects of salt stress in the tomato plant by salicylic acid shows a time-and organ-specific antioxidant response. Acta Biol Crac Bot 57:21–30

    CAS  Google Scholar 

  • USDA-National Agricultural Statistics Service (NASS) (2018) Crops U.S. state and county databases. Washington DC

  • Wang F, Chen F, Cai Y, Zhang G, Wu F (2011) Modulation of exogenous glutathione in ultrastructure and photosynthetic performance against Cd stress in the two barley genotypes differing in Cd tolerance. Biol Trace Elem Res 144:1275–1288

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Yamaguchi T, Blumwald E (2005) Developing salt-tolerant crop plants: challenges and opportunities. Trends Plant Sci 10:615–620

    Article  CAS  PubMed  Google Scholar 

  • Yang Y, Guo Y (2018) Elucidating the molecular mechanisms mediating plant salt-stress responses. New Phytol 217:523–539

    Article  CAS  PubMed  Google Scholar 

  • Yoshida K, Noguchi K (2009) Differential gene expression profiles of the mitochondrial respiratory components in illuminated Arabidopsis leaves. Plant Cell Physiol 50:1449–1462

    Article  CAS  PubMed  Google Scholar 

  • Yousuf PY, Ahmad A, Aref IM, Ozturk M, Ganie AH, Iqbal M (2016) Salt-stress-responsive chloroplast proteins in Brassica juncea genotypes with contrasting salt tolerance and their quantitative PCR analysis. Protoplasma 253:1565–1575

    Article  CAS  PubMed  Google Scholar 

  • Zhang M, Smith JAC, Harberd NP, Jiang C (2016) The regulatory roles of ethylene and reactive oxygen species (ROS) in plant salt stress responses. Plant Mol Biol 91:651–659

    Article  CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Plant Physiology and Biochemistry Laboratory, Department of Botany, Aligarh Muslim University, Aligarh, 202002, India

    Faisal Rasheed, Zebus Sehar, Mehar Fatma, Asim Masood, Naser A. Anjum & Nafees A. Khan

  2. Department of Botany, Jamia Hamdard, New Delhi, 110062, India

    Noushina Iqbal

Authors
  1. Faisal Rasheed
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Zebus Sehar
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Mehar Fatma
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Noushina Iqbal
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Asim Masood
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Naser A. Anjum
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Nafees A. Khan
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

Conceptualization: N.I., N.A.K.; Investigation and data curation: F.R., M.F., Z.S; N.I., Cytological and histological analysis: Z.S., A.M., N.A.A.; Original draft preparation: F.R., Z.S., M.F. N.A.A.; Editing and content improvement: N.I., M.F., N.A.A.; Supervision: N.A.K. All authors have read and agreed to the published version of the manuscript.

Corresponding author

Correspondence to Nafees A. Khan.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Handling Author: Bram Van de Poel.

Publisher's Note

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

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (DOCX 19 KB)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Rasheed, F., Sehar, Z., Fatma, M. et al. Involvement of Ethylene in Reversal of Salt Stress by Salicylic Acid in the Presence of Sulfur in Mustard (Brassica juncea L.). J Plant Growth Regul 41, 3449–3466 (2022). https://doi.org/10.1007/s00344-021-10526-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00344-021-10526-9

Keywords

Search

Navigation