Skip to main content
Log in

Dunaliella salina exopolysaccharides: a promising biostimulant for salt stress tolerance in tomato (Solanum lycopersicum)

  • 6th Congress of the International Society for Applied Phycology
  • Published:
Journal of Applied Phycology Aims and scope Submit manuscript

Abstract

Microalgal exopolysaccharides represent a potential sustainable alternative for the enhancement and protection of agricultural crops including management of both biotic and abiotic stress. In the present study, we investigated the potential of Dunaliella salina exopolysaccharides (PS) to attenuate the effect of salt stress on growth of Solanum lycopersicum, which was grown under different salinity levels (3 and 6 g L−1 NaCl). The effects of PS treatment on plant growth, osmoprotectant molecules, protein content, and antioxidant enzymes activities of tomato plants under salt stress were analyzed. A metabolomics study showed that the exopolysaccharides released by D. salina contained sulfated moiety along with carbohydrates and uronic acids. The application of sulfated exopolysaccharides on tomato plants alleviated the salt stress and mitigated the decrease in length and dry weight of the plant’s shoot and root systems, as well as that of potassium (K+), and K+/Na+ ratio. Furthermore, the increase in proline, phenolic compounds, Na+, and antioxidant enzymes (CAT, POD, SOD) activities caused by salt stress were attenuated after the exopolysaccharide treatment. GC-MS metabolomics analysis showed that PS treatment allowed the activation and/or inhibition of various metabolic pathways involved in the plant’s tolerance to stress such as jasmonic acid-dependent pathways. This study shows the potential of microalgal exopolysaccharides for enhancing tomato tolerance to salt stress and highlights the possibility of their use as plant growth biostimulants under harsh environmental conditions.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8

Similar content being viewed by others

References

  • Aebi H (1984) Catalase in vitro. Methods Enzymol 105:121–126

    Article  CAS  PubMed  Google Scholar 

  • Amjad M, Akhtar J, Anwar-ul-Haq M, Yang A, Akhtar S, Jacobsen E (2014) Integrating role of ethylene and ABA in tomato plants adaptation to salt stress. Sci Hortic 172:109–116

    Article  CAS  Google Scholar 

  • Ashraf M (2004) Some important physiological selection criteria for salt tolerance in plants. Flora Rev 199:361–376

    Article  Google Scholar 

  • Ashraf MY, & Wu L (1994) Breeding for salinity tolerance in plants. Crit Rev Plant Sci 13(1):17-42

    Article  Google Scholar 

  • Ashraf M, Hasnain S, Berge O, Mahmood T (2004) Inoculating wheat seedlings with exopolysaccharide-producing bacteria restricts sodium uptake and stimulates plant growth under salt stress. Biol Fertil Soils 40:157–162

    CAS  Google Scholar 

  • Ashraf M, Hasnain S, Berge O (2006) Effect of exo-polysaccharides producing bacterial inoculation on growth of roots of wheat (Triticum aestivum L.) plants grown in a salt-affected soil. Int J Environ Sci Technol 3:43–51

    Article  CAS  Google Scholar 

  • Assunção MFG, Amaral R, Martins CB, Ferreira JD, Ressurreição S, Santos SD, Varejão JMTB, Santos LMA (2017) Screening microalgae as potential sources of antioxidants. J Appl Phycol 29:865–877

    Article  Google Scholar 

  • Atkinson NJ, Lilley CJ, Urwin PE (2013) Identification of genes involved in the response of Arabidopsis to simultaneous biotic and abiotic stresses. Plant Physiol 162:2028–2041

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bacha H, Tekaya M, Drine S, Guasmi F, Touil L, Enneb H, Triki T, Cheour F, Ferchichi A (2017) Impact of salt stress on morpho-physiological and biochemical parameters of Solanum lycopersicum cv. microtom leaves. S Afr J Bot 108:364–369

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Blumenkrantz N, Asboe-Hansen G (1973) New method for quantitative determination of uronic acids. Anal Biochem 54:484–489

    Article  CAS  PubMed  Google Scholar 

  • Boland W, Hopke J, Donath J, Nüske J, Bublitz F (1995) Jasmonic acid and coronatin induce odor production in plants. Angew Chem Int Ed 34:1600–1602

    Article  CAS  Google Scholar 

  • Borghesi E, González-Miret ML, Escudero-Gilete ML, Malorgio F, Heredia FJ, Meléndez-Martínez AJ (2011) Effects of salinity stress on carotenoids, anthocyanins, and color of diverse tomato genotypes. J Agric Food Chem 59:11676–11682

    Article  CAS  PubMed  Google Scholar 

  • Borowitzka MA (2013) Dunaliella: biology, production, and markets. In: Richmond A, Hu Q (eds) Handbook of microalgal culture. John Wiley & Sons, Ltd, pp 359–368

    Chapter  Google Scholar 

  • Borowitzka LJ, Brown AD (1974) The salt relations of marine and halophilic species of the uni cellular green alga Dunaliella. The role of glycerol as a compatible solute. Arch Microbiol 96:37–52

    Article  CAS  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

    Article  CAS  PubMed  Google Scholar 

  • Cai W, Gu X, Tang J (2008) Extraction, purification, and characterization of the polysaccharides from Opuntia milpa alta. Carbohydr Polym 71:403–410

    Article  CAS  Google Scholar 

  • Cameron KD, Teece MA, Smart LB (2006) Increased accumulation of cuticular wax and expression of lipid transfer protein in response to periodic drying events in leaves of tree tobacco. Plant Physiol 140:176–183

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chaiklahan R, Chirasuwan N, Triratana P, Loha V, Tia S, Bunnag B (2013) Polysaccharide extraction from Spirulina sp. and its antioxidant capacity. Int J Biol Macromol 58:73–78

    Article  CAS  PubMed  Google Scholar 

  • Choi SJ, Kim JK, Kim HK, Harris K, Kim CJ, Park GG, Shin DH (2013) 2,4-Di-tert-butylphenol from sweet potato protects against oxidative stress in PC12 cells and in mice. J Med Food 16:977–983

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Claussen W (2005) Proline as a measure of stress in tomato plants. Plant Sci 168:241–248

    Article  CAS  Google Scholar 

  • Cortés-Jiménez D, Gómez-Guzmán A, Iturriaga G, Suárez R, Alpírez GM, Escalante F (2014) Microorganisms associated to tomato seedlings growing in saline culture act as osmoprotectant. Braz J Microbiol 45:613–620

    Article  PubMed  PubMed Central  Google Scholar 

  • Costa LS, Fidelis GP, Cordeiro SL, Oliveira RM, Sabry DA, Câmara RBG, Leite EL (2010) Biological activities of sulfated polysaccharides from tropical seaweeds. Biomed Pharmacother 64:21–28

    Article  CAS  PubMed  Google Scholar 

  • De Abreu CE, Prisco JT, Nogueira AR, Bezerra MA, Lacerda CFD, Gomes-Filho E (2008) Physiological and biochemical changes occurring in dwarf-cashew seedlings subjected to salt stress. Braz J Plant Physiol 20:105–118

    Article  Google Scholar 

  • Di T, Chen G, Sun Y, Ou S, Zeng X, Ye H (2017) Antioxidant and immunostimulating activities in vitro of sulfated polysaccharides isolated from Gracilaria rubra. J Funct Foods 28:64–75

    Article  CAS  Google Scholar 

  • Dubois M, Gilles KA, Hamilton JK, Rebers P, Smith F (1956) Colorimetric method for determination of sugars and related substances. Anal Chem 28:350–356

    Article  CAS  Google Scholar 

  • Dumville JC, Fry SC (2000) Uronic acid-containing oligosaccharins: their biosynthesis, degradation and signalling roles in non-diseased plant tissues. Plant Physiol Biochem 38:125–140

    Article  CAS  Google Scholar 

  • El-Sharkawy M, El-Beshsbeshy T, Al-Shal R, Missaoui A (2017) Effect of plant growth stimulants on alfalfa response to salt stress. Agric Sci 8:267–291

    Google Scholar 

  • Eryılmaz F (2006) The relationships between salt stress and anthocyanin content in higher plants. Biotech Biotechnol Equip 20:47–52

    Article  Google Scholar 

  • Ferreira IC, Heleno SA, Reis FS, Stojkovic D, Queiroz MJR, Vasconcelos MH, Sokovic M (2015) Chemical features of Ganoderma polysaccharides with antioxidant, antitumor and antimicrobial activities. Phytochemistry 114:38–55

    Article  CAS  PubMed  Google Scholar 

  • Fleita D, El-Sayed M, Rifaat D (2015) Evaluation of the antioxidant activity of enzymatically-hydrolyzed sulfated polysaccharides extracted from red algae; Pterocladia capillacea. LWT Food Sci Technol 63:1236–1244

    Article  CAS  Google Scholar 

  • Folch J, Lees M, Stanley GHS (1957) A simple method for the isolation and purification of total lipides from animal tissues. J Biol Chem 226:497–509

    CAS  PubMed  Google Scholar 

  • Ghanem ME, Han RM, Classen B, Quetin-Leclerq J, Mahy G, Ruan CJ, Lutts S (2010) Mucilage and polysaccharides in the halophyte plant species Kosteletzkya virginica: localization and composition in relation to salt stress. J Plant Physiol 167:382–392

    Article  CAS  Google Scholar 

  • Guajardo E, Correa JA, Contreras-Porcia L (2016) Role of abscisic acid (ABA) in activating antioxidant tolerance responses to desiccation stress in intertidal seaweed species. Planta 243:767–781

    Article  CAS  PubMed  Google Scholar 

  • Guzmán-Murillo MA, Ascencio F, Larrinaga-Mayoral JA (2013) Germination and ROS detoxification in bell pepper (Capsicum annuum L.) under NaCl stress and treatment with microalgae extracts. Protoplasma 250:33–42

    Article  PubMed  Google Scholar 

  • Hadi MR, Shariati M, Afsharzadeh A (2008) Microalgal biotechnology: carotenoid and glycerol production by the green algae Dunaliella isolated from the Gave-Khooni salt marsh, Iran. Biotechnol Bioprocess Eng 13:540–544

    Article  CAS  Google Scholar 

  • Jeschke WD, Wolf O (1988) Effect of NaCI salinity on growth, development, ion distribution, and ion translocation in castor bean (Ricinus communis L.). J Plant Physiol 132:45–53

    Article  CAS  Google Scholar 

  • Jiang M, Zhang J (2002) Water stress-induced abscisic acid accumulation triggers the increased gene ration of reactive oxygen species and up-regulates the activities of antioxidant enzymes in maize leaves. J Exp Bot 53:2401–2410

    Article  CAS  PubMed  Google Scholar 

  • Jiao G, Yu G, Zhang J, Ewart HS (2011) Chemical structures and bioactivities of sulfated polysaccharides from marine algae. Mar Drugs 9:196–223

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jin M, Zhao K, Huang Q, Xu C, Shang P (2012) Isolation, structure and bioactivities of the polysaccharides from Angelica sinensis (Oliv.) Diels: a review. Carbohydr Polym 89:713–722

    Article  CAS  PubMed  Google Scholar 

  • Koleška I, Hasanagić D, Maksimović I, Bosančić B, Kukavica B (2017) The role of antioxidative metabolism of tomato leaves in long-term salt- stress response. J Soil Sci Plant Nutr 180:105–112

    Article  Google Scholar 

  • Kumar MS, Ali K, Dahuja A, Tyagi A (2015) Role of phytosterols in drought stress tolerance in rice. Plant Physiol Biochem 96:83–89

    Article  CAS  PubMed  Google Scholar 

  • Lichtenthaler HK, Buschmann C (2001) Chlorophylls and carotenoids: measurement and characterization by UV-VIS spectroscopy. Curr Prot Food Analyt Chem. https://doi.org/10.1002/0471142913.faf0403s01

    Google Scholar 

  • Lioyd AG, Dodgson KS, Price RG, Rose FAI (1961) Infrared studies on sulphate esters. I. Polysaccharide sulphates. Biochim Biophys Acta 46:108–115

    Article  Google Scholar 

  • Macková J, Vašková M, Macek P, Hronková M, Schreiber T, Šantrůček J (2013) Plant response to drought stress simulated by ABA application: changes in chemical composition of cuticular waxes. Environ Exp Bot 86:70–75

    Article  Google Scholar 

  • Maehly A, Chance B (1954) Catalases and peroxidases. Methods Biochem Anal 1:357–424

    CAS  PubMed  Google Scholar 

  • Manaf HH (2016) Beneficial effects of exogenous selenium, glycine betaine and seaweed extract on salt stressed cowpea plant. Ann Agric Sci 61:41–48

    Google Scholar 

  • Mansori M, Chernane H, Latique S, Benaliat A, Hsissou D, El Kaoua M (2016) Effect of seaweed extract (Ulva rigida) on the water deficit tolerance of Salvia officinalis L. J Appl Phycol 28:1363–1370

    Article  CAS  Google Scholar 

  • Meloni DA, Gulotta MR, Martínez CA, Oliva MA (2004) The effects of salt stress on growth, nitrate reduction and proline and glycinebetaine accumulation in Prosopisalba. Braz J Plant Physiol 16:39–46

    Article  CAS  Google Scholar 

  • Miller G, Suzuki N, Ciftci-Yilmaz S, Mittler R (2010) Reactive oxygen species homeostasis and signalling during drought and salinity stresses. Plant Cell Environ 33:453–467

    Article  CAS  PubMed  Google Scholar 

  • Mishra A, Jha B (2009) Isolation and characterization of extracellular polymeric substances from micro-algae Dunaliella salina under salt stress. Bioresour Technol 100:3382–3386

    Article  CAS  PubMed  Google Scholar 

  • Mishra A, Kavita K, Jha B (2011) Characterization of extracellular polymeric substances produced by micro-algae Dunaliella salina. Carbohydr Polym 83:852–857

    Article  CAS  Google Scholar 

  • Navarro L, Dunoyer P, Jay F, Arnold B, Dharmasiri N, Estelle M, Voinnet O, Jones JDA (2006) Plant miRNA contributes to antibacterial resistance by repressing auxin signaling. Science 312:436–439

    Article  CAS  PubMed  Google Scholar 

  • Opriş O, Copaciu F, Soran ML, Ristoiu D, Niinemets Ü, Copolovici L (2013) Influence of nine antibiotics on key secondary metabolites and physiological characteristics in Triticum aestivum: leaf volatiles as a promising new tool to assess toxicity. Ecotoxicol Environ Saf 87:70–79

    Article  PubMed  Google Scholar 

  • Pedranzani H, Racagni G, Alemano S, Miersch O, Ramírez I, Peña-Cortés H, Machado-Domenech E, Abdala G (2003) Salt tolerant tomato plants show increased levels of jasmonic acid. Plant Growth Regul 41:149–158

    Article  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

    Article  CAS  PubMed  Google Scholar 

  • Rossi F, De Philippis R (2016) Exocellular polysaccharides in microalgae and cyanobacteria: chemical features, role and enzymes and genes involved in their biosynthesis. In: Borowitzka MA, Beardall J, Raven JA (eds) The physiology of microalgae. Springer, Dordrecht, pp 565–590

    Chapter  Google Scholar 

  • Scodelaro Bilbao PG, Damiani C, Salvador GA, Leonardi P (2016) Haematococcus pluvialis as a source of fatty acids and phytosterols: potential nutritional and biological implications. J Appl Phycol 28:3283–3294

    Article  CAS  Google Scholar 

  • Shepherd T, Wynne Griffiths D (2006) The effects of stress on plant cuticular waxes. New Phytol 171:469–499

    Article  CAS  PubMed  Google Scholar 

  • Stadnik MJ, Freitas MBD (2014) Algal polysaccharides as source of plant resistance inducers. Trop Plant Pathol 39:111–118

    Article  Google Scholar 

  • Szarka A, Tomasskovics B, Bánhegyi G (2012) Theascorbate-glutathione-α-tocopherol triad in abiotic stress response. Int J Mol Sci 13:4458–4483

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Taga MS, Miller EE, & Pratt D E (1984) Chia seeds as a source of natural lipid antioxidants. J Amer Oil Chem Soci 61(5):928-931

    Article  CAS  Google Scholar 

  • Tong CB, Labavitch JM, Yang SF (1986) The induction of ethylene production from pear cell-culture by cell-wall fragments. Plant Physiol 81:929–930

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Upadhyayet S, Singh J, Singh D (2011) Exopolysaccharide-producing plant growth-promoting Rhizobacteria under salinity condition. Pedosphere 21:214–222

    Article  Google Scholar 

  • Upchurch RG (2008) Fatty acid unsaturation, mobilization, and regulation in the response of plants to stress. Biotechnol Lett 30:967–977

    Article  CAS  PubMed  Google Scholar 

  • Varsha KK, Devendra L, Shilpa G, Priya S, Pandey A, Nampoothiri KM (2015) 2,4-Di-tert-butyl phenol as the antifungal, antioxidant bioactive purified from a newly isolated Lactococcus sp. Int J Food Microbiol 211:44–50

    Article  CAS  PubMed  Google Scholar 

  • Wahid A, Ghazanfar A (2006) Possible involvement of some secondary metabolites in salt tolerance of sugarcane. J Plant Physiol 163:723–730

    Article  CAS  PubMed  Google Scholar 

  • Walne PR (1970) Studies on the food value of nineteen genera of algae to juvenile bivalves of the genera Ostrea, Crassostrea, Mercenaria and Mytilus. H M Stationary Office, London

    Google Scholar 

  • Wang K, Senthil-Kumar M, Ryu CM, Kang L, Mysore KS (2012) Phytosterols play a key role in plant innate immunity against bacterial pathogens by regulating nutrient efflux into the apoplast. Plant Physiol 158:1789–1802

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang WJ, Liu XW, Gai XS, Ren JJ, Liu XF, Cai YL, Wang Q, Ren H (2015) Cucumissativus L. WAX2 plays a pivotal role in WAX biosynthesis, influencing pollen fertility and plant biotic and abiotic stress responses. Plant Cell Physiol 56:1339–1354

    Article  CAS  PubMed  Google Scholar 

  • Wells ML, Potin P, Craigie JS, Raven JA, Merchant SS, Helliwell KE, Smith AG, Camire ME, Brawley SH (2017) Algae as nutritional and functional food sources: revisiting our understanding. J Appl Phycol 29:949–982

    Article  CAS  PubMed  Google Scholar 

  • Yoshimura K, Yabuta Y, Ishikawa T, Shigeoka S (2004) Expression of spinach ascorbate peroxidase isoenzymes in response to oxidative stresses. Plant Physiol 123:223–233

    Article  Google Scholar 

  • Zaki HE, Yokoi S (2016) A comparative in vitro study of salt tolerance in cultivated tomato and related wild species. Plant Biotechnol 33:361–372

    Article  Google Scholar 

  • Zhang H, Zhang Q, Zhai H, Li Y, Wang X, Liu Q, He S (2017) Transcript profile analysis reveals important roles of jasmonic acid signalling pathway in the response of sweet potato to salt stress. Sci Rep 7:40819

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zepeda-Jazo I, Shabala S, Chen Z, Pottosin II (2008) Na+-K+ transport in roots under salt stress. Plant Signal Behav 3(6):401-403

Download references

Acknowledgements

The authors would like to acknowledgement Chanda Mutale Joan for the revision of the quality of the English language of this article.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to H. EL Arroussi.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

EL Arroussi, H., Benhima, R., Elbaouchi, A. et al. Dunaliella salina exopolysaccharides: a promising biostimulant for salt stress tolerance in tomato (Solanum lycopersicum). J Appl Phycol 30, 2929–2941 (2018). https://doi.org/10.1007/s10811-017-1382-1

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10811-017-1382-1

Keywords

Navigation