Hostname: page-component-848d4c4894-4hhp2 Total loading time: 0 Render date: 2024-05-14T06:09:31.474Z Has data issue: false hasContentIssue false

Stress responses of the green microalga, Dunaliella salina to PEG-induced drought

Published online by Cambridge University Press:  29 October 2020

Fatemeh Tafvizi
Affiliation:
Biotechnology Division, Department of Cell and Molecular Biology, Faculty of Chemistry, University of Kashan, Kashan, Iran
Seyed Ali Hosseini Tafreshi*
Affiliation:
Biotechnology Division, Department of Cell and Molecular Biology, Faculty of Chemistry, University of Kashan, Kashan, Iran
Zeinab Toluei
Affiliation:
Biotechnology Division, Department of Cell and Molecular Biology, Faculty of Chemistry, University of Kashan, Kashan, Iran
Mohammad Amin Toghyani
Affiliation:
Biotechnology Division, Department of Cell and Molecular Biology, Faculty of Chemistry, University of Kashan, Kashan, Iran
*
Author for correspondence: Seyed Ali Hosseini Tafreshi, E-mail: sahosseini@kashanu.ac.ir

Abstract

Drought stress was evaluated with polyethylene glycol 6000 (PEG 6000) treatment in Dunaliella salina, a microalga known for its great ability to withstand salinities of more than 30%. The aim was to explore the acclimation mechanisms used by the microalga to regulate its growth and physiology during coping with drought stress. The microalga was subjected to culture mediums containing 2 and 5% PEG for 25 days and was compared with a control culture medium. Significant decrease in growth parameters such as specific growth rate, biomass and number of divisions per day was demonstrated in PEG-treated algae. During PEG treatment, chlorophylls slightly increased, while β-carotene and total protein were not affected. Osmolytes, as well as carbohydrates, were found to be significantly higher in PEG-treated algae than in control. Increased catalase and ascorbate peroxidase activities were proportionally related to PEG concentrations in the cultures. The PEG-treated cells accumulated a considerable amount of hydrogen peroxide and malondialdehyde, especially at higher PEG concentrations. Electrolyte leakage increased, regardless of the PEG concentrations applied, while DNA fragmentation was not observed after 25 days of treating with PEG. It was concluded that Dunaliella cells could respond to the drought stress, probably by using a higher accumulation of a range of osmolytes and also more stimulation of the antioxidant enzymatic system.

Type
Research Article
Copyright
Copyright © Marine Biological Association of the United Kingdom 2020

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Aasen, AJ, Eimhjellen, KE and Liaaen-Jensen, S (1969) An extreme source of β-carotene. Acta Chemica Scandinavica 23, 25442545.CrossRefGoogle ScholarPubMed
Aebi, HE (1983) Catalase in vitro. In Keating, C (ed.), Methods in Enzymology. Amsterdam: Elsevier, pp. 121126.Google Scholar
Anaraki, ZE, Hosseini Tafreshi, SA and Shariati, M (2018) Transient silencing of heat shock proteins showed remarkable roles for HSP70 during adaptation to stress in plants. Environmental and Experimental Botany 155, 142157.CrossRefGoogle Scholar
Arora, A, Sairam, RK and Srivastava, GC (2002) Oxidative stress and antioxidative system in plants. Current Science 82, 12271238.Google Scholar
Arun, N and Singh, DP (2013) Differential response of Dunaliella salina and Dunaliella tertiolecta isolated from brines of Sambhar Salt Lake of Rajasthan (India) to salinities: a study on growth, pigment and glycerol synthesis. Journal of the Marine Biological Association of India 55, 6570.CrossRefGoogle Scholar
Bates, L, Waldren, RP and Teare, ID (1973) Rapid determination of free proline for water-stress studies. Plant and Soil 39, 205207.CrossRefGoogle Scholar
Belghith, T, Feki, AE, Athmouni, K, Ayadi, H and Bellassoued, K (2016) Physiological and biochemical response of Dunaliella salina to cadmium pollution. Journal of Applied Phycology 28, 991999.Google Scholar
Bewley, JD (1979) Physiological aspects of desiccation tolerance. Annual Review of Plant Physiology 30, 195238.CrossRefGoogle Scholar
Bradford, MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Analytical Biochemistry 72, 248254.CrossRefGoogle ScholarPubMed
Bremer, E and Krämer, R (2019) Responses of microorganisms to osmotic stress. Annual Review of Microbiology 73, 313–34.CrossRefGoogle ScholarPubMed
Chan, K, Wong, KH and Ng, SL (1981) Effects of polyethylene glycol on growth and cadmium accumulation of Chlorella salina CU-I. Chemosphere 10, 985991.CrossRefGoogle Scholar
Chen, H, Lao, YM and Jiang, JG (2011) Effects of salinities on the gene expression of a (NAD+)-dependent glycerol-3-phosphate dehydrogenase in Dunaliella salina. Science of the Total Environment 409, 12911297.CrossRefGoogle ScholarPubMed
Chitlaru, E and Pick, U (1991) Regulation of glycerol synthesis in response to osmotic changes in Dunaliella. Plant Physiology 96, 5060.CrossRefGoogle ScholarPubMed
Cowan, AK, Rose, PD and Horne, LG (1992) Dunaliella salina: a model system for studying the response of plant cells to stress. Journal of Experimental Botany 43, 15351547.CrossRefGoogle Scholar
Das, K and Roychoudhury, A (2014) Reactive oxygen species (ROS) and response of antioxidants as ROS-scavengers during environmental stress in plants. Frontiers of Environmental Science & Engineering 2, 113.Google Scholar
Davis, JS (1972) Survival records in the algae, and the survival role of certain algal pigments, fats and mucilaginous substances. Biologist (Columbus, Ohio) 54, 5293.Google Scholar
Delauney, AJ, Hu, CAA, Kavi Kishor, PB and Verma, DPS (1993) Cloning of ornithine d-aminotransferase cDNA from Vigna aconitifolia by trans-complementation in Escherichia coli and regulation of proline biosynthesis. Journal of Biological Chemistry 268, 1867318678.CrossRefGoogle Scholar
Dionisio-Sese, ML and Tobita, S (1998) Antioxidant responses of rice seedlings to salinity stress. Plant Science Journal 135, 19.CrossRefGoogle Scholar
Eijckelhoff, C and Dekker, JP (1997) A routine method to determine the chlorophyll a, pheophytin a and carotene contents of isolated Photosystem II reaction center complexes. Photosynthesis Research 52, 6973.CrossRefGoogle Scholar
Gechev, TS, Dinakar, C, Benina, M, Toneva, V and Bartels, D (2013) Molecular mechanisms of desiccation tolerance in resurrection plants. Cellular and Molecular Life Sciences 70, 689709.CrossRefGoogle Scholar
Hare, PD and Cress, WA (1997) Metabolic implications of stress induced proline accumulation in plants. Plant Growth Regulation 21, 79102.CrossRefGoogle Scholar
Havaux, M (1998) Carotenoids as membrane stabilizers in chloroplasts. Trends in Plant Science 3, 147151.Google Scholar
Heath, RL and Packer, L (1968) Photoperoxidation in isolated chloroplasts: I. Kinetics and stoichiometry of fatty acid peroxidation. Archives of Biochemistry and Biophysics 125, 189198.CrossRefGoogle ScholarPubMed
Holzinger, A and Karsten, U (2013) Desiccation stress and tolerance in green algae: consequences for ultrastructure, physiological, and molecular mechanisms. Frontiers of Plant Science 4, 118.CrossRefGoogle ScholarPubMed
Hosseini Tafreshi, SA and Shariati, M (2008) Dunaliella biotechnology: methods and applications. Journal of Applied Microbiology 107, 1435.CrossRefGoogle Scholar
Johnson, MK, Johnson, EJ, McElrory, RD, Speer, HL and Bruff, BS (1968) Effects of salt on the halophilic alga Dunaliella viridis. Journal of Bacteriology Research 95, 14611468.CrossRefGoogle ScholarPubMed
Kirst, GO (1990) Salinity tolerance of eukaryotic marine algae. Annual Review of Plant Physiology and Plant Molecular Biology 41, 2153.CrossRefGoogle Scholar
Kochert, G (1978) Carbohydrate determination by the phenol-sulfuric acid method. In Helebust, JA and Craigie, JS (eds), Handbook of Physiological Methods – Physiological and Biochemical Methods. Cambridge: Cambridge University Press, pp. 9697.Google Scholar
Kohl, KI and Losch, R (2004) Experimental characterisation of metal tolerance. In Prasad, MNV (ed.), Heavy Metal Stress in Plants: From Biomolecules to Ecosystem, 2nd Edn. Berlin: Springer-Verlag, pp. 434454.CrossRefGoogle Scholar
Kranner, I, Beckett, R, Hochman, A and Nash, TH (2008) Desiccation-tolerance in lichens: a review. Bryologist 111, 576593.CrossRefGoogle Scholar
Kumar, PS and Dharmaraj, S (2003) Studies on the growth of the marine microalga Dunaliella salina (Teodoresco). Indian Journal of Fisheries 50, 259262.Google Scholar
Kuznetsov, VI and Shevykova, NI (1999) Proline under stress: biological role, metabolism, and regulation. Russian Journal of Plant Physiology 46, 274287.Google Scholar
Lee, YH and Yeh, YL (2014) Using polyethylene glycol as nonionic osmoticum to promote growth and lipid production of marine microalgae Nannochloropsis oculata. Bioprocess and Biosystems Engineering 37, 16691677.CrossRefGoogle ScholarPubMed
Levasseur, M, Thompson, PA and Harrison, PJ (1993) Physiological acclimation of marine-phytoplankton to different nitrogen-sources. Journal of Phycology 29, 587595.CrossRefGoogle Scholar
Li, JF, Li, L and Sheen, J (2010) Protocol: a rapid and economical procedure for purification of plasmid or plant DNA with diverse applications in plant biology. Plant Methods 6, 18.CrossRefGoogle ScholarPubMed
Lin, CS and Wu, JT (2014) Tolerance of soil algae and cyanobacteria to drought stress. Journal of Phycology 50, 131139.CrossRefGoogle ScholarPubMed
Matysik, J, Alia, A, Bhalu, B and Mohanty, P (2002) Molecular mechanisms of quenching of reactive oxygen species by proline under stress in plants. Current Science 82, 525532.Google Scholar
Michel, B and Kaufmann, M (1973) The osmotic potential of polyethylene glycol 6000. Plant Physiology 51, 914916.CrossRefGoogle ScholarPubMed
Mishra, A, Mandoli, A and Jha, B (2008) Physiological characterization and stress-induced metabolic responses of Dunaliella salina isolated from salt pan. Journal of Industrial Microbiology & Biotechnology 35, 10931101.CrossRefGoogle ScholarPubMed
Molinari, HBC, Marur, CJ, Daros, E, De Campos, MKF, Carvalho, JFRP, Filho, JCB, Pereira, LFP and Vieira, LGE (2007) Evaluation of the stress-inducible production of proline in transgenic sugarcane (Saccharum spp.): osmotic adjustment, chlorophyll fluorescence and oxidative stress. Physiologia Plantarum 130, 218229.CrossRefGoogle Scholar
Nakano, Y and Asada, K (1981) Hydrogen-peroxide is scavenged by ascorbate-specific peroxidase in spinach chloroplasts. Plant and Cell Physiology 22, 867880.Google Scholar
Oliver, M, Farrant, JM, Hilhorst, HWM, Mundree, S, Williams, B and Bewley, JD (2020) Desiccation tolerance: avoiding cellular damage during drying and rehydration. Annual Review of Plant Biology 71, 435460.CrossRefGoogle ScholarPubMed
Phadwal, K and Singh, PK (2003) Effect of nutrient depletion on β carotene and glycerol accumulation in two strains of Dunaliella sp. Bioresource Technology 90, 5558.CrossRefGoogle ScholarPubMed
Rogers, ME, Colmer, TD, Frost, K, Henry, D, Cornwall, D, Hulm, E, Hughers, SR, Nichols, PGH and Craig, AD (2009) The influence of NaCl salinity and hypoxia on aspects of growth in Trifolium species. Crop and Pasture Science 60, 7182.CrossRefGoogle Scholar
Sairam, RK and Srivastava, GC (2002) Changes in antioxidant activity in subcellular fractions of tolerant and susceptible wheat genotypes in response to long term salt stress. Plant Science 162, 897904.CrossRefGoogle Scholar
Scheibe, R and Beck, E (2011) Drought, desiccation, and oxidative stress. In Lüttge, U (ed.), Plant Desiccation Tolerance. Heidelberg: Springer, pp. 209232.CrossRefGoogle Scholar
Sergiev, I, Alxieva, V and Karanov, E (1997) Effect of spermone, atrazine and combination between them on some endogenous protective systems and stress markers in plants. Comptes Rendus de l'Academie Bulgare des Sciences 51, 121124.Google Scholar
Tardieu, T, Simonneau, T and Muller, B (2018) The physiological basis of drought tolerance in crop plants: a scenario-dependent probabilistic approach. Annual Review of Plant Biology 69, 733759.CrossRefGoogle ScholarPubMed
Tattini, M, Traversi, ML, Castelli, S, Biricolti, S, Guidi, L and Massai, R (2009) Contrasting response mechanisms to root-zone salinity in three co-occurring Mediterranean woody evergreens: a physiological and biochemical study. Functional Plant Biology 36, 551563.CrossRefGoogle ScholarPubMed
Toghyani, MA, Karimi, F, Hosseini Tafreshi, SA and Talei, D (2020) Two distinct time dependent strategic mechanisms used by Chlorella vulgaris in response to gamma radiation. Journal of Applied Phycology 32, 16771695.CrossRefGoogle Scholar
Venekemp, JH (1989) Regulation of cytosol acidity in plants under conditions of drought. Physiologia Plantarum 76, 112–7.CrossRefGoogle Scholar
Yilancioglu, K, Cokol, M, Pastirmaci, I, Erman, B and Cetiner, S (2014) Oxidative stress is a mediator for increased lipid accumulation in a newly isolated Dunaliella salina strain. PLoS ONE 9, e91957.Google Scholar