Skip to main content

Advertisement

SpringerLink
Log in

Exogenous Glutathione Modulates Salinity Tolerance of Soybean [Glycine max (L.) Merrill] at Reproductive Stage

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

Abstract

In this study, we evaluated salt stress responses of 11 soybean genotypes and explored the protective roles of exogenous glutathione (GSH) against salt toxicity by assessing various biochemical and yield-attributing parameters. Exposure of the soybean genotypes to salt stress at the reproductive (R1) stage significantly decreased their yields by down-regulating the yield-contributing parameters as compared with unstressed controls. The highest decrease was found in number of seeds plant−1, yield plant−1, and number of pods plant−1, whereas the lowest decrease was recorded in number of seeds pod−1. Exogenous GSH was found to be effective in improving salinity tolerance, and the highest positive effects of GSH were recorded in terms of yield plant−1, number of seeds plant−1 and number of pods plant−1, whereas its lowest effect was observed with respect to the 100-seed weight. Cluster analysis of the genotypes based on yield-contributing and yield data revealed different levels of salt tolerance. Notably, BINA-01 and -02, and BINA-04 were recognized as the highest and lowest salt-tolerant genotypes, respectively. Furthermore, exogenous GSH alleviated oxidative stress in the representative contrasting genotypes at the vegetative (V3) stage by decreasing salt-induced accumulation of malondialdehyde and hydrogen peroxide. Taken together, our findings revealed that exogenous GSH application can minimize oxidative stress and contribute to the improvement of yield-contributing parameters, leading to improved yield in soybean genotypes under salt stress. Further investigations on molecular aspects will enable us to gain an in-depth understanding of how exogenous GSH can improve salinity tolerance in soybean, particularly at reproductive stage, to discover relevant pathways for biotechnological manipulation.

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

Similar content being viewed by others

References

  • Adem GD, Roy SJ, Zhou M, Bowman JP, Shabala S (2014) Evaluating contribution of ionic, osmotic and oxidative stress components towards salinity tolerance in barley. BMC Plant Biol 14:113

    Article  PubMed  PubMed Central  Google Scholar 

  • Agarwal N, Singh A, Ashok K (2015) Salinity effects on growth and productivity of two soybean genotypes (Glycine max L.). Indian J Sci Res 6:59–69

    CAS  Google Scholar 

  • Ahmad M, Sandhu GR (1988) Response of legumes to salt stress and effect on growth and nitrogen status of soybean. Pak J Agric Res 9:44–50

    Google Scholar 

  • Ali MA, Yeasmin L, Gantait S, Goswami R, Chakraborty S (2014) Screening of rice landraces for salinity tolerance at seedling stage through morphological and molecular markers. Physiol Mol Biol Plants 20:411–423

  • Allu AD, Soja AM, Wu A, Szymanski J, Balazadeh S (2014) Salt stress and senescence: identification of cross-talk regulatory components. J Exp Bot 65:3993–4008

    Article  PubMed  PubMed Central  Google Scholar 

  • Ammar WB, Mediouni C, Tray B, Ghorbel MH, Jemal F (2008) Glutathione and phytochelatin contents in tomato plants exposed to cadmium. Biol Plant 52:314–320

    Article  Google Scholar 

  • Asim M, Aslam M, Asghari B, Munir M, Majeed A, Haider SA (2013) Role of phytohormones in root nodulation and yield of soybean under salt stress. Am J Res Comm 1:191–208

    Google Scholar 

  • Cao F, Cai Y, Liu L, Zhang M, He X, Zhang G, Wu F (2015) Differences in photosynthesis, yield and grain cadmium accumulation as affected by exogenous cadmium and glutathione in the two rice genotypes. Plant Growth Regul 75:715–723

    Article  CAS  Google Scholar 

  • Chaudhary J, Patil GB, Sonah H, Deshmukh RK, Vuong TD, Valliyodan B, Nguyen HT (2015) Expanding omics resources for improvement of soybean seed composition traits. Front Plant Sci 6:1021

    Article  PubMed  PubMed Central  Google Scholar 

  • Chaves MM, Flexas J, Pinheiro C (2009) Photosynthesis under drought and salt stress, regulation mechanisms from whole plant to cell. Ann Bot 103:551–560

    Article  CAS  PubMed  Google Scholar 

  • Cheng MC, Ko K, Chang WL, Kuo WC, Chen GH, Lin TP (2015) Increased glutathione contributes to stress tolerance and global translational changes in Arabidopsis. Plant J 83:926–939

    Article  CAS  PubMed  Google Scholar 

  • Diaz-Vivancos P, Dong Y, Ziegler K, Markovic J, Pallardo FV, Pellny TK (2010) Recruitment of glutathione into the nucleus during cell proliferation adjusts whole-cell redox homeostasis in Arabidopsis thaliana and lowers the oxidative defense shield. Plant J 64:825–838

    Article  Google Scholar 

  • Ding X, Jiang Y, He L, Zhou Q, Yu J, Hui D, Huang D (2016) Exogenous glutathione improves high root-zone temperature tolerance by modulating photosynthesis, antioxidant and osmolytes systems in cucumber seedlings. Sci Rep 6:35424

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Do TD, Chen H, Hien VTT, Hamwieh A, Yamada T, Sato T, Yan Y, Cong H, Shono M, Suenaga K, Xu D (2016) Ncl synchronously regulates Na+, K+, and Cl– in soybean and greatly increases the grain yield in saline field conditions. Sci Rep 6:19147

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dong Z, Shi L, Wang Y, Chen L, Cai Z, Wang Y, Jin J, Li X (2013) Identification and dynamic regulation of microRNAs involved in salt stress responses in functional soybean nodules by high-throughput sequencing. Int J MolSci 14:2717–2738

    Article  CAS  Google Scholar 

  • El-Sabagh A, Sobhy S, Akihiro U, Hirofumi S, Celaleddin B (2015) Evaluation of salinity stress effects on seed yield and quality of three soybean cultivars. Azarian J Agric 2:138–141

    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 

  • Fotopoulos V, Ziogas V, Tanou G, Molassiotis A (2010) Involvement of AsA/DHA and GSH/GSSG ratios in gene and protein expression and in the activation of defence mechanisms under abiotic stress conditions. In: Anjum NA, Chan M-T, Umar S (eds) Ascorbate-glutathione pathway and stress tolerance in plants. Springer, Dordrecht, pp 265–302

    Chapter  Google Scholar 

  • Foyer CH, Pellny TK, Locato V, De Gara L (2008) Analysis of redox relationships in the plant cell cycle: determinations of ascorbate, glutathione and poly (ADPribose) polymerase (PARP) in plant cell cultures. Method Mol Biol 476:193–209

    Article  Google Scholar 

  • Hamayun M, Sumera AK, Latif KA, Shinwari ZK, Hussain J, Sohn EY, Kang SM, Kim YH, Khan MA, Lee IJ (2010) Effect of salt stress on growth attributes and endogenous growth hormones of soybean cultivar Hwangkeumkong. Pak J Bot 42:3103–3112

    CAS  Google Scholar 

  • Heath RL, Packer L (1968) Photoperoxidation in isolated chloroplast. I. Kinetics and stoichiometry of fatty acid peroxidation. Arch Biochem Biophys 25:189–198

    Article  Google Scholar 

  • Hossain MA, Fujita M (2013) Hydrogen peroxide priming stimulates drought tolerance in mustard (Brassica juncea L.). Plant Gene Trait 4:109–123

    Google Scholar 

  • Hossain MA, Hasanuzzaman M, Fujita M (2010) Up-regulation of antioxidant and glyoxalase systems by exogenous glycinebetaine and proline in mung bean confer tolerance to cadmium stress. Physiol Mol Biol Plants 16:259–272

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hossain MA, Mostofa MG, Fujita M (2013a) Cross protection by cold-shock to salinity and drought stress-induced oxidative stress in mustard (Brassica campestris L.) seedlings. Mol Plant Breed 4:50–70

    Google Scholar 

  • Hossain MA, Mostofa MG, Fujita M (2013b) Heat-shock positively modulates oxidative protection of salt and drought-stressed mustard (Brassica campestris L.) seedlings. J Plant Sci Mol Breed 2:1–14

    Article  Google Scholar 

  • Hossain MA, Ismail MR, Uddin MK, Islam MZ, Ashrafuzzaman M (2013c) Efficacy of ascorbate-glutathione cycle for scavenging H2O2 in two contrasting rice genotypes during salinity stress. Aust J Crop Sci 7:1801–1808

    CAS  Google Scholar 

  • Hossain MM, Liu X, Qi X, Lam HM, Zhang J (2014) Differences between soybean genotypes in physiological response to sequential soil drying and rewetting. Crop J 2:366–380

    Article  Google Scholar 

  • Hossain H, Rahman MA, Alam MS, Singh RK (2015) Mapping of quantitative trait loci associated with reproductive stage salt tolerance in rice. J Agron Crop Sci 201:17–31

    Article  CAS  Google Scholar 

  • Islam MT, Jahan NA, Sen AK, Pramanik MHR (2012) Effects of salinity on morpho-physiological attributes and yield of lentil genotypes. Int J Sust Crop Prod 1:12–18

    Google Scholar 

  • Jacob OO, Francis NI (2015) Effect of different levels of NaCl and Na2SO4 salinity on dry matter and ionic content of cowpea (Vigna unguiculata L.). Afr J Agric Res 10:1239–1243

    Google Scholar 

  • Jagadish S, Septiningsih E, Kohli A, Thomson M, Ye C, Redona E, Kumar A, Greorio G, Wassmann R, Ismail A (2012) Genetic advances in adapting rice to a rapidly changing climate. J Agron Crop Sci 198:360–373

    Article  Google Scholar 

  • Kan G, Zhang W, Yang W, Ma D, Zhang D, Hao D, Hu Z, Yu D (2015) Association mapping of soybean seed germination under salt stress. Mol Genet Genomics 290:2147–2162

    Article  CAS  PubMed  Google Scholar 

  • Kocsy G, Tari I, Vankova R, Zechmann B, Gulyas Z, Poor P, Galiba G (2013) Redox control of plant growth and development. Plant Sci 211:77–91

    Article  CAS  PubMed  Google Scholar 

  • Krasensky J, Jonak C (2012) Drought, salt, and temperature stress-induced metabolic rearrangements and regulatory networks. J Exp Bot 63:1593–1608

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Labudda M, Azam FMS (2014) Glutathione-dependent responses of plants to drought: a review. Acta Soc Bot Pol 83:3–12

    Article  CAS  Google Scholar 

  • Lu Y, Lam H, Pi E, Zhan Q, Tsai S, Wang C, Kwan Y, Ngai S (2013) Comparative metabolomics in Glycine max and Glycine soja under salt stress to reveal the phenotypes of their offspring. J Agric Food Chem 61:8711–8721

    Article  CAS  PubMed  Google Scholar 

  • Maheswari J, Bose J, Babourina O, Rengel Z, Shabala S (2015) Salicylic acid in plant salinity stress signaling and tolerance. Plant Growth Regul 76:25–40

    Article  Google Scholar 

  • Malek MA, Rafii MY, Afroz MSS, Nath UK, Mondal MMA (2014) Morphological characterization and assessment of genetic variability, character association, and divergence in soybean mutants. Sci World J 2014:968796

    Article  CAS  Google Scholar 

  • Mathur S (2004) Soybean the Wonder Legume. Beverage Food World 31: 61–62

    Google Scholar 

  • Meher HC, Gajbhiye VT, Singh G (2011) Salicylic acid-induced glutathione status in tomato crop and resistance to root-knot nematode, Meloidogyne incognita (Kofoid& White) Chitwood. J Xeno 1:e5

    Article  Google Scholar 

  • Mostofa MG, Seraj ZI, Fujita M (2014) Exogenous sodium nitroprusside and glutathione alleviate copper toxicity by reducing copper uptake and oxidative damage in rice (Oryza sativa L.) seedlings. Protoplasma 251:1373–1386

    Article  CAS  PubMed  Google Scholar 

  • Mostofa MG, Saegusa D, Fujita M, Tran LSP (2015a) Hydrogen sulfide regulates salt tolerance in rice by maintaining Na+/K+ balance, mineral homeostasis and oxidative metabolism under excessive salt stress. Front Plant Sci 6:1055

    Article  PubMed  PubMed Central  Google Scholar 

  • Mostofa MG, Hossain MA, Fujita M (2015b) Trehalose pretreatment induces salt tolerance in rice seedlings: oxidative damage and co-induction of antioxidant defense and glyoxalase systems. Protoplsasma 252:461–475

    Article  CAS  Google Scholar 

  • Munns R, Gilliham M (2015) Salinity tolerance of crops–what is the cost? New Phytol 208:668–673

    Article  CAS  PubMed  Google Scholar 

  • Nahar K, Hasanuzzaman M, Alam MM, Fujita M (2015a) Roles of exogenous glutathione in antioxidant defense system and methylglyoxal detoxification during salt stress in mung bean. Biol Plant 59:745–756

    Article  CAS  Google Scholar 

  • Nahar K, Hasanuzzaman M, Alam MM, Fujita M (2015b) Exogenous glutathione confers high temperature stress tolerance in mung bean (Vigna radiata L.) by modulating antioxidant defense and methylglyoxal detoxification system. Environ Exp Bot 112:44–54

    Article  CAS  Google Scholar 

  • Nahar K, Hasanuzzaman M, Alam MM, Fujita M (2015c) Glutathione-induced drought stress tolerance in mung bean: coordinated roles of the antioxidant defence and methylglyoxal detoxification systems. AoB Plants 7:plv069

    Article  PubMed  PubMed Central  Google Scholar 

  • Phang TH, Shao GH, Lam HM (2008) Salt tolerance in soybean. J Integr Plant Biol 50:1196–1212

    Article  CAS  PubMed  Google Scholar 

  • Potters G, Horemans N, Bellone S, Caubergs J, Trost P, Guisez Y, Asard H (2004) Dehydroascorbate influences the plant cell cycle through a glutathione-independent reduction mechanism. Plant Physiol 134:1479–1487

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Purwaningrahayu DR, SebayangTH, Syekhfani, Aini N (2015) Resistance level of some soybean (Glycine max L. Merrill) genotypes towards salinity stress. J Biol Res 20:7–14

    Article  Google Scholar 

  • Qadir M, Tubeileh A, Akhtar J, Larbi A, Minhas PS, Khan MA (2008) Productivity enhancement of salt affected environments through crop diversification. Land Degrad Develop 19:429–453

    Article  Google Scholar 

  • Rawia EA, Taha LS, Ibrahiem SMM (2011) Alleviation of adverse effects of salinity on growth and chemical constituents of marigold plants by using glutathione and ascorbate. J Appl Sci Res 7:714–721

    Google Scholar 

  • Roy SJ, Negrao S, Tester M (2014) Salt resistant crop plants. Curr Opin Biotechnol 26:115–124

    Article  CAS  PubMed  Google Scholar 

  • SAS Institute Inc., 2010.SAS/STAT user’s guide, 3rd ed, SAS Institute Inc. Cary

    Google Scholar 

  • Schnaubelt D, Queval G, Dong Y, Diaz-Vivancos P, Makgopa ME, Howell G, Simone AD, Bai, J, Hannah MA, Foyer CH (2015) Low glutathione regulates gene expression and the redox potentials of the nucleus and cytosol in Arabidopsis thaliana. Plant Cell Environ 38:266–279

    Article  CAS  PubMed  Google Scholar 

  • Shabala S (2013) Learning from halophytes: physiological basis and strategies to improve abiotic stress tolerance in crops. Ann Bot 112(1209–1):221

    Google Scholar 

  • Szalai G, Kell 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 

  • Taffouo VD, Kouamou JK, Ngalangue LMT, Ndjeudji BAN, Akoa A (2009) Effects of salinity stress on growth, ions partitioning and yield of some cowpea (Vigna ungiuculata L.) cultivars. Int J Bot 5:135–143

    Article  CAS  Google Scholar 

  • Teh CY, Mahmood M, Shaharuddin NA, Ho CL (2014) In vitro rice shoot apices as simple model to study the effect of NaCl and the potential of exogenous proline and glutathione in mitigating salinity stress. Plant Growth Regul 75:771–781

    Article  Google Scholar 

  • Velikova V, Yordanov I, Edreva A (2000) Oxidative stress and some antioxidant systems in acid rain-treated bean plants. Plant Sci 151: 59–66

    Article  CAS  Google Scholar 

  • Wan C, Shao G, Chen Y, Yan S (2002) Relationship between salt tolerance and chemical quality of soybean under salt stress. Chin J Oil Crop Sci 24:67–72

    Google Scholar 

  • Wang R, Liu S, Zhou F, Ding C, Hua C (2014) Exogenous ascorbic acid and glutathione alleviate oxidative stress induced by salt stress in the chloroplasts of rice (Oryza sativa L.). J Biosci 69:226–236

    CAS  Google Scholar 

  • Wu G, Zhou Z, Chen P, Tang X, Shao H, Wang H (2014) Comparative ecophysiological study of salt stress for wild and cultivated soybean species from the yellow river delta, China. Sci World J 2014:651745

    Google Scholar 

  • Yasuta Y, Kokubun M (2014) Salinity tolerance of super-nodulating soybean genotype. Plant Prod Sci 17:32–40

    Article  Google Scholar 

  • You J, Chan Z (2015) ROS regulation during abiotic stress responses in crop plants. Front Plant Sci 6:1092

    Article  PubMed  PubMed Central  Google Scholar 

  • Zechmann B, Koffler BE, Russell S (2011) Glutathione synthesis is essential for pollen germination in vitro. BMC Plant Biol 11:54

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zeng L, Shannon MC (2000) Salinity effects on seedling growth and yield components of rice. Crop Sci 40:996–1003

    Article  Google Scholar 

Download references

Acknowledgements

Mohammad Anwar Hossain and Mohammad Golam Mostofa thankfully acknowledges the postdoc fellowship from the Japan Society for the Promotion of Science (JSPS).

Author information

Author notes

  1. Mohammad Golam Mostofa

    Present address: Signaling Pathway Research Unit, RIKEN Center for Sustainable Resource Science, Yokohama, Japan

Authors and Affiliations

  1. Department of Genetics and Plant Breeding, Bangladesh Agricultural University, Mymensingh, 2202, Bangladesh

    Soleh Akram, B. M. Nahid Hussain, Md. Abdullah Al Bari & Mohammad Anwar Hossain

  2. Department of Biochemistry and Molecular Biology, Bangabandhu Sheikh Mujibur Rahman Agricultural University, Gazipur, 1706, Bangladesh

    Md. Nurealam Siddiqui & Mohammad Golam Mostofa

  3. Plant Abiotic Stress Research Group & Faculty of Applied Sciences, Ton Duc Thang University, Ho Chi Minh City, Vietnam

    Lam-Son Phan Tran

  4. Signaling Pathway Research Unit, RIKEN Center for Sustainable Resource Science, Yokohama, Japan

    Lam-Son Phan Tran

Authors
  1. Soleh Akram
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Md. Nurealam Siddiqui
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. B. M. Nahid Hussain
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Md. Abdullah Al Bari
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Mohammad Golam Mostofa
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Mohammad Anwar Hossain
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Lam-Son Phan Tran
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Mohammad Anwar Hossain or Lam-Son Phan Tran.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (PDF 184 KB)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Akram, S., Siddiqui, M.N., Hussain, B.M.N. et al. Exogenous Glutathione Modulates Salinity Tolerance of Soybean [Glycine max (L.) Merrill] at Reproductive Stage. J Plant Growth Regul 36, 877–888 (2017). https://doi.org/10.1007/s00344-017-9691-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00344-017-9691-9

Keywords

Search

Navigation