Skip to main content
Log in

Effect of Microalgae Polysaccharides on Biochemical and Metabolomics Pathways Related to Plant Defense in Solanum lycopersicum

  • Published:
Applied Biochemistry and Biotechnology Aims and scope Submit manuscript

Abstract

Microalgae are photosynthetic microorganisms that produce several bioactive molecules that have received considerable attention in scientific and industrial communities. Today, many plant biostimulants including seaweed extracts and polysaccharides are used in agriculture. However, microalgae have not been largely exploited in this field as a potential source of plant bio stimulants. This study investigated the biostimulatory effects of microalgae polysaccharides on different metabolomic and biochemical pathways related to plant defense. 0.2 mg mL−1 of crude polysaccharides extracted from four green microalgae strains was injected into tomato plants (Solanum lycopersicum). β-1,3-glucanase activity, lipid remodeling, phenylalanine ammonia lyase (PAL), Lipoxygenase (LOX), and antioxidant enzyme (APX, POD and CAT) activities were evaluated 48 h after treatment. Plants treated with crude polysaccharides extracted from. C. vulgaris and C. sorokiniana exhibited a significant increase in β-1,3-glucanase activity. Accordingly, C. sorokiniana crude polysaccharides had a significant stimulatory effect on PAL activity with a percentage increase of 188.73% compared to the control. GC/MS quantitative lipidomics analysis revealed that treatment with D. salina, C. sorokiniana, and C. reinhardtii crude polysaccharides increased PUFA content by 50.37%, 34.46%, and 33.37% respectively. Microalgae polysaccharides also enhanced stearic acid, palmitic acid, and VLCFA content, the optimal value of which increased by 45.50%, 32.83%, and 60.60% respectively under treatment with C. reinhardtii crude polysaccharides compared with the control. C. vulgaris and C. reinhardtii crude polysaccharides also exhibited higher APX and POD activity respectively. The present results therefore indicate the potentiality of microalgae crude polysaccharides as a promising renewable bio resource in the development plant bio stimulants.

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.

Institutional subscriptions

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

Similar content being viewed by others

References

  1. Kissoudis, C., van de Wiel, C., Visser, R. G., & van der Linden, G. (2014). Enhancing crop resilience to combined abiotic and biotic stress through the dissection of physiological and molecular crosstalk. Frontiers in Plant Science, 5, 207.

    Article  Google Scholar 

  2. Mittler, R. (2006). Abiotic stress, the field environment and stress combination. Trends in Plant Science, 11(1), 15–19.

    Article  CAS  Google Scholar 

  3. Calvo, P., Nelson, L., & Kloepper, J. W. (2014). Agricultural uses of plant biostimulants. Plant and Soil, 383(1–2), 3–41.

    Article  CAS  Google Scholar 

  4. Du Jardin, P. (2015). Plant biostimulants: definition, concept, main categories and regulation. Scientia Horticulturae, 196, 3–14.

    Article  Google Scholar 

  5. Sharma, H. S., Fleming, C., Selby, C., Rao, J. R., & Martin, T. (2014). Plant biostimulants: a review on the processing of macroalgae and use of extracts for crop management to reduce abiotic and biotic stresses. Journal of Applied Phycology, 26(1), 465–490.

    Article  CAS  Google Scholar 

  6. Priyadarshani, I., & Rath, B. (2012). Commercial and industrial applications of micro algae–a review. Journal of Algal Biomass Utilization, 3(4), 89–100.

    Google Scholar 

  7. Chen, B., You, W., Huang, J., Yu, Y., & Chen, W. (2010). Isolation and antioxidant property of the extracellular polysaccharide from Rhodella reticulata. World Journal of Microbiology and Biotechnology, 26(5), 833–840.

    Article  CAS  Google Scholar 

  8. De Souza, M. C. R., Marques, C. T., Dore, C. M. G., da Silva, F. R. F., Rocha, H. A. O., & Leite, E. L. (2007). Antioxidant activities of sulfated polysaccharides from brown and red seaweeds. Journal of Applied Phycology, 19(2), 153–160.

    Article  Google Scholar 

  9. Jha, D., Jain, V., Sharma, B., Kant, A., & Garlapati, V. K. (2017). Microalgae-based pharmaceuticals and nutraceuticals: an emerging field with immense market potential. ChemBioEng Reviews, 4(4), 257–272. https://doi.org/10.1002/cben.201600023.

    Article  CAS  Google Scholar 

  10. Wijesekara, I., Pangestuti, R., & Kim, S. K. (2011). Biological activities and potential health benefits of sulfated polysaccharides derived from marine algae. Carbohydrate Polymers, 84(1), 14–21.

    Article  CAS  Google Scholar 

  11. Qi, H., Zhang, Q., Zhao, T., Chen, R., Zhang, H., Niu, X., & Li, Z. (2005). Antioxidant activity of different sulfate content derivatives of polysaccharide extracted from Ulva pertusa (Chlorophyta) in vitro. International Journal of Biological Macromolecules, 37(4), 195–199.

    Article  CAS  Google Scholar 

  12. Vera, J., Castro, J., Gonzalez, A., & Moenne, A. (2011). Seaweed polysaccharides and derived oligosaccharides stimulate defense responses and protection against pathogens in plants. Marine Drugs, 9(12), 2514–2525.

    Article  CAS  Google Scholar 

  13. El Arroussi, H., El Mernissi, N., Benhima, R., El Kadmiri, I. M., Bendaou, N., Smouni, A., & Wahby, I. (2016). Microalgae polysaccharides a promising plant growth biostimulant. Journal of Algal Biomass Utilization, 7(4), 55–63.

    Google Scholar 

  14. Mercier, L., Lafitte, C., Borderies, G., Briand, X., Esquerré-Tugayé, M. T., & Fournier, J. (2001). The algal polysaccharide carrageenans can act as an elicitor of plant defence. New Phytologist, 149(1), 43–51.

    Article  CAS  Google Scholar 

  15. Paulert, R., Talamini, V., Cassolato, J. E. F., Duarte, M. E. R., Noseda, M. D., Smania, A., & Stadnik, M. J. (2009). Effects of sulfated polysaccharide and alcoholic extracts from green seaweed Ulva fasciata on anthracnose severity and growth of common bean (Phaseolus vulgaris L). Journal of Plant Diseases and Protection, 116(6), 263–270.

    Article  CAS  Google Scholar 

  16. Kauffman, G. L., Kneivel, D. P., & Watschke, T. L. (2007). Effects of a biostimulant on the heat tolerance associated with photosynthetic capacity, membrane thermostability, and polyphenol production of perennial ryegrass. Crop Science, 47(1), 261–267.

    Article  CAS  Google Scholar 

  17. Des Marais, D. L., Hernandez, K. M., & Juenger, T. E. (2013). Genotype-by-environment interaction and plasticity exploring genomic responses of plants to the abiotic environment. Annual Review of Ecology, Evolution, and Systematics, 44(1), 5–29.

    Article  Google Scholar 

  18. Pereira, A. (2016). Plant abiotic stress challenges from the changing environment. Frontiers in Plant Science, 7, 1123.

    PubMed  PubMed Central  Google Scholar 

  19. Yoshida, T., Mogami, J., & Yamaguchi-Shinozaki, K. (2014). ABA-dependent and ABA-independent signaling in response to osmotic stress in plants. Current Opinion in Plant Biology, 21, 133–139.

    Article  CAS  Google Scholar 

  20. Fujita, M., Fujita, Y., Noutoshi, Y., Takahashi, F., Narusaka, Y., Yamaguchi-Shinozaki, K., & Shinozaki, K. (2006). Crosstalk between abiotic and biotic stress responses: a current view from the points of convergence in the stress signaling networks. Current Opinion in Plant Biology, 9(4), 436–442.

    Article  Google Scholar 

  21. Rejeb, I. B., Pastor, V., & Mauch-Mani, B. (2014). Plant responses to simultaneous biotic and abiotic stress: molecular mechanisms. Plants, 3(4), 458–475.

    Article  Google Scholar 

  22. Okazaki, Y., & Saito, K. (2016). Integrated metabolomics and phytochemical genomics approaches for studies on rice. GigaScience, 5(1), 11.

    Article  Google Scholar 

  23. Başkan, K. S., Tütem, E., Akyüz, E., Özen, S., & Apak, R. (2016). Spectrophotometric total reducing sugars assay based on cupric reduction. Talanta, 147, 162–168.

    Article  Google Scholar 

  24. Melton, L. D., & Smith, B. G. (2001). Determination of the uronic acid content of plant cell walls using a colorimetric assay. Current Protocols in Food Analytical Chemistry, 00(1), E3.3.1–E3.3.4.

    Article  Google Scholar 

  25. Campo, V. L., Kawano, D. F., da Silva Jr., D. B., & Carvalho, I. (2009). Carrageenans: biological properties, chemical modifications and structural analysis–a review. Carbohydrate Polymers, 77(2), 167–180.

    Article  CAS  Google Scholar 

  26. Hu, T., Qv, X., Hu, Z., Chen, G., & Chen, Z. (2011). Expression, molecular characterization and detection of lipoxygenase activity of tomloxD from tomato. African Journal of Biotechnology, 10(4), 491.

    Google Scholar 

  27. Chandrasekaran, M., Belachew, S. T., Yoon, E., & Chun, S. C. (2017). Expression of β-1, 3-glucanase (GLU) and phenylalanine ammonia-lyase (PAL) genes and their enzymes in tomato plants induced after treatment with Bacillus subtilis CBR05 against Xanthomonas campestris pv. vesicatoria. Journal of General Plant Pathology, 83(1), 7–13.

    Article  CAS  Google Scholar 

  28. Bradford, M. M. (1976). A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Analytical Biochemistry, 72(1–2), 248–254.

    Article  CAS  Google Scholar 

  29. Stadnik, M. J., & Freitas, M. B. D. (2014). Algal polysaccharides as source of plant resistance inducers. Tropical Plant Pathology, 39(2), 111–118.

    Article  Google Scholar 

  30. Shukla, P. S., Borza, T., Critchley, A. T., & Prithiviraj, B. (2016). Carrageenans from red seaweeds as promoters of growth and elicitors of defense response in plants. Frontiers in Marine Science, 3, 81.

    Article  Google Scholar 

  31. Raposo, M. F. D. J., de Morais, R. M. S. C., & de Morais, B. A. M. (2013). Bioactivity and applications of sulphated polysaccharides from marine microalgae. Marine Drugs, 11(1), 233–252.

    Article  Google Scholar 

  32. Ho, S. H., Huang, S. W., Chen, C. Y., Hasunuma, T., Kondo, A., & Chang, J. S. (2013). Bioethanol production using carbohydrate-rich microalgae biomass as feedstock. Bioresource Technology, 135, 191–198.

    Article  CAS  Google Scholar 

  33. Singh, S. P., & Singh, P. (2015). Effect of temperature and light on the growth of algae species: a review. Renewable and Sustainable Energy Reviews, 50, 431–444.

    Article  CAS  Google Scholar 

  34. Kim, K. H., Choi, I. S., Kim, H. M., Wi, S. G., & Bae, H. J. (2014). Bioethanol production from the nutrient stress-induced microalga Chlorella vulgaris by enzymatic hydrolysis and immobilized yeast fermentation. Bioresource Technology, 153, 47–54.

    Article  CAS  Google Scholar 

  35. Gupta, P., Ravi, I., & Sharma, V. (2013). Induction of β-1, 3-glucanase and chitinase activity in the defense response of Eruca sativa plants against the fungal pathogen Alternaria brassicicola. Journal of Plant Interactions, 8(2), 155–161.

    Article  CAS  Google Scholar 

  36. Fesel, P. H., & Zuccaro, A. (2016). β-glucan: crucial component of the fungal cell wall and elusive MAMP in plants. Fungal Genetics and Biology, 90, 53–60.

    Article  CAS  Google Scholar 

  37. Alon, M., Malka, O., Eakteiman, G., Elbaz, M., Zvi, M. M. B., Vainstein, A., & Morin, S. (2013). Activation of the Phenylpropanoid pathway in Nicotiana tabacum improves the performance of the whitefly Bemisia tabaci via reduced jasmonate signaling. PLoS One, 8(10), e76619.

    Article  CAS  Google Scholar 

  38. Cooper, L. L., Oliver, J. E., De Vilbiss, E. D., & Doss, R. P. (2000). Lipid composition of the extracellular matrix of Botrytis cinerea germlings. Phytochemistry, 53(2), 293–298.

    Article  CAS  Google Scholar 

  39. Wang, K., Senthil-Kumar, M., Ryu, C. M., Kang, L., & Mysore, K. S. (2012). Phytosterols play a key role in plant innate immunity against bacterial pathogens by regulating nutrient efflux into the apoplast. Plant Physiology, 158, 111.

    Google Scholar 

  40. Lim, G. H., Singhal, R., Kachroo, A., & Kachroo, P. (2017). Fatty acid–and lipid-mediated signaling in plant defense. Annual Review of Phytopathology, 55(1), 505–536.

    Article  CAS  Google Scholar 

  41. Walley, J. W., Kliebenstein, D. J., Bostock, R. M., & Dehesh, K. (2013). Fatty acids and early detection of pathogens. Current Opinion in Plant Biology, 16(4), 520–526.

    Article  CAS  Google Scholar 

  42. Yaeno, T., Matsuda, O., & Iba, K. (2004). Role of chloroplast trienoic fatty acids in plant disease defense responses. The Plant Journal, 40(6), 931–941.

    Article  CAS  Google Scholar 

  43. Stumpe, M., & Feussner, I. (2006). Formation of oxylipins by CYP74 enzymes. Phytochemistry Reviews, 5(2–3), 347–357.

    Article  CAS  Google Scholar 

  44. Dolch, L. J., Rak, C., Perin, G., Tourcier, G., Broughton, R., Leterrier, M., Morosinotto, T., Tellier, F., Faure, J. D., Falconet, D., Jouhet, J., Sayanova, O., Beaudoin, F., & Marechal, E. (2016). A palmitic acid elongase affects eicosapentaenoic acid and plastidal monogalactosyldiacylglcerol levels in Nannochloropsis. Plant Physiology, 173, 01420.

    Google Scholar 

  45. Serrano, M., Coluccia, F., Torres, M., L’Haridon, F., & Métraux, J. P. (2014). The cuticle and plant defense to pathogens. Frontiers in Plant Science, 5, 274.

    Article  Google Scholar 

  46. Senthil-Kumar, M., Wang, K., & Mysore, K. S. (2013). AtCYP710A1 gene-mediated stigmasterol production plays a role in imparting temperature stress tolerance in Arabidopsis thaliana. Plant Signaling & Behavior, 8(2), e23142.

    Article  Google Scholar 

  47. Gill, S. S., & Tuteja, N. (2010). Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiology and Biochemistry, 48(12), 909–930.

    Article  CAS  Google Scholar 

Download references

Funding

The authors would link to give special thanks for the financial support of MESRSFC and CNRST for the realization of this project under the best conditions (Grant number: PPR2).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to EL Arroussi Hicham.

Ethics declarations

Conflicts of Interest

The authors declare that they have no conflict of interest.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Farid, R., Mutale-joan, C., Redouane, B. et al. Effect of Microalgae Polysaccharides on Biochemical and Metabolomics Pathways Related to Plant Defense in Solanum lycopersicum. Appl Biochem Biotechnol 188, 225–240 (2019). https://doi.org/10.1007/s12010-018-2916-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12010-018-2916-y

Keywords

Navigation