, Volume 55, Issue 3, pp 510–521 | Cite as

Effectiveness of cyanobacteria and green algae in enhancing the photosynthetic performance and growth of willow (Salix viminalis L.) plants under limited synthetic fertilizers application

  • M. Grzesik
  • Z. Romanowska-DudaEmail author
  • H. M. KalajiEmail author
Open Access
Original Paper


The physiological response of plants to triple foliar biofertilization with cyanobacteria and green algae under the conditions of limited use of chemical fertilizers was investigated. Triple foliar biofertilization with intact cells of Microcystis aeruginosa MKR 0105, Anabaena sp. PCC 7120, and Chlorella sp. significantly enhanced physiological performance and growth of plants fertilized with a synthetic fertilizer YaraMila Complex (1.0, 0.5, and 0.0 g per plant). This biofertilization increased the stability of cytomembranes, chlorophyll content, intensity of net photosynthesis, transpiration, stomatal conductance, and decreased intercellular CO2 concentration. Applied monocultures augmented the quantity of N, P, K in plants, the activity of enzymes, such as dehydrogenases, RNase, acid or alkaline phosphatase and nitrate reductase. They also improved the growth of willow plants. This study revealed that the applied nontoxic cyanobacteria and green algae monocultures have a very useful potential to increase production of willow, and needed doses of chemical fertilizers can be reduced.

Additional key words

energy plant gas exchange mineral fertilization 



Anabaena sp. PCC 7120


Bio-Algeen S90


Chlorella sp.


the environmental sample


gibberellic acid


indole-3-butyric acid


not sonicated monocultures of Microcystis aeruginosa MKR 0105



Research was supported by National Science Center in Poland under Grant No. N N304 102940 and National Centre for Research and Development Grant No. BIOSTRATEG 2/296369/5/NCBR/2016.


  1. Abd El-Moniem E, Abd-Allah A.S.E.: Effect of green alga cells extract as foliar spray on vegetative growth, yield and berries quality of superior grapevines.–Am.-Eurasian J. Agric. Environ. Sci. 4: 427–433, 2008.Google Scholar
  2. Adam M.S.: The promotive effect of cyanobacterium Nostoc muscorum on the growth of some crop plants.–Acta Microbiol. Pol. 48: 163–171, 1999.Google Scholar
  3. Al-Khiat S.H.A.: Effect of Cyanobacteria as a Soil Conditioner and Biofertilizer on Growth and some Biochemical Characteristics of Tomato (Lycopersicon esculentum L.) Seedlings. Pp. 190. Faculty of Science, King Saud University, Riyadh 2006.Google Scholar
  4. Bergman B., Johansson C., Söderbäck E.: The Nostoc-Gunnera symbiosis.–New Phytol. 122: 379–400, 1992.CrossRefGoogle Scholar
  5. Booker F.L.: Influence of ozone on ribonuclease activity in wheat (Triticum aestivum) leaves.–Physiol. Plantarum 120: 249–255, 2004.CrossRefGoogle Scholar
  6. Burja A.M., Banaigs B., Abou-Mansour E. et al.: Marine cyanobacteria–a profilic source of natural products.–Tetrahedron 57: 9347–9377, 2001.CrossRefGoogle Scholar
  7. Cheng K.J., Ingram J.M., Costerton J.W.: Interactions of alkaline phosphatase and the cell wall of Pseudomonas aeruginosa.–J. Bacteriol. 107: 325–336, 1971.PubMedPubMedCentralGoogle Scholar
  8. Chojnacka A., Romanowska-Duda Z.B., Grzesik M. et al.: Cyanobacteria as a source of bioactive compounds for crop cultivation.–In: Wolowski K., Kwandrans J., Wojtal A.Z. (ed): Taxonomy the Queen of Science -the Beauty of Algae. Book of Abstracts of the 29th International Phycological Conference Krakow. Pp. 81–82. Inst. Bot. Polish Acad. Sci., Krakow 2010.Google Scholar
  9. de Caire G.Z., de Cano M.S., Palma R.M. et al.: Changes in soi enzymes activity by cyanobacterial biomass and exopolysaccharides.–Soil Biol. Biochem. 32: 1985–1987, 2000.CrossRefGoogle Scholar
  10. de Mulé M.C.Z., de Caire G.Z., de Cano M.S. et al.: Effect of cyanobacterial inoculation and fertilizers on rice seedlings and post harvest soil structure.–Commun. Soil Sci. Plan. 30: 97–107, 1999.CrossRefGoogle Scholar
  11. Dick W.A., Tabatabai M.A.: Significance and potential uses of soil enzymes.–In: Metting F.B. (ed): Soil Microbial Ecology: Application in Agricultural and Environmental Management. Pp. 95–125. Marcel Dekker, New York 1993 Ecochem: Foliar Applied Fertilizer., 2017.Google Scholar
  12. El-Fouly M.M., Abdalla F.E., Shaaban M.M.: Multipurpose large scale production of microalgae biomass in Egypt. Proceedings on 1st Egyptian Etalian Symptoms on Biotechnology. Assiut, Egypt (Nov 21–23). Pp. 305–314, 1992.Google Scholar
  13. El Modafar C., Elgadda M., El Boutachfaiti R. et al.: Induction of natural defence accompanied by salicylic acid-dependant systemic acquired resistance in tomato seedlings in response to bioelicitors isolated from green algae.–Sci. Hortic.-Amsterdam 138: 55–63, 2012.CrossRefGoogle Scholar
  14. Falch B.S., König G.M., Wright A.D. et al.: Biological activities of cyanobacteria: evaluation of extracts and pure compounds.–Planta Med. 61: 321–328, 1995.CrossRefPubMedGoogle Scholar
  15. Glick B.R., Patten C.L., Holguin G. et al.: Biochemical and Genetic Mechanisms Used by Plant Growth Promoting Bacteria. Pp. 267. ICP, Ontario 1999.CrossRefGoogle Scholar
  16. Gorelova O. A.: Communication of cyanobacteria with plant partners during association formation.–Microbiology 75: 465–469, 2006.CrossRefGoogle Scholar
  17. Górnik K., Grzesik M.: Effect of Asahi SL on China aster ‘Aleksandra’ seed yield, germination and some metabolic events.–Acta Physiol. Plant. 24: 379–383, 2002.CrossRefGoogle Scholar
  18. Grzesik M., Romanowska-Duda Z.B., Piotrowski K.: The effect of potential climatic changes, Cyanobacteria, Biojodis and Asahi SL on development of the Virginia fanpetals (Sida hermaphrodita) plants.–Pamietnik Pulawski 151: 483–491, 2009.Google Scholar
  19. Grzesik M., Romanowska-Duda Z.: Improvements in germination, growth, and metabolic activity of corn seedlings by grain conditioning and root application with cyanobacteria and microalgae.–Pol. J. Environ. Stud. 23: 1147–1153, 2014.Google Scholar
  20. Grzesik M., Romanowska-Duda Z.: Ability of cyanobacteria and green algae to improve metabolic activity and development of willow plants.–Pol. J. Environ. Stud. 24: 1003–1012, 2015.CrossRefGoogle Scholar
  21. Haroun S.A., Hussein M.H.: The promotive effect of algal biofertilizers on growth, protein pattern and some metabolic activities of Lupinus termis plants grown in siliceous soil.–Asian J. Plant Sci. 2: 944–951, 2003.CrossRefGoogle Scholar
  22. Hegazi A.Z., Mostafa M.S.S., Ahmed H.M.I.: Influence of different cyanobacterial application methods on growth and seed production of common bean under various levels of mineral nitrogen fertilization.–Nat. Sci. 8: 183–194, 2010.Google Scholar
  23. Hussain A., Hasnain, S.: Comparative assessment of the efficacy of bacterial and cyanobacterial phytohormones in plant tissue culture.–World J. Microb. Biot. 28: 1459–1466, 2012.CrossRefGoogle Scholar
  24. Kalaji M.H, Schansker G., Ladle R. J. et al.: Frequently Asked Questions about chlorophyll fluorescence: practical issues.–Photosynth. Res. 122: 121–158, 2014.CrossRefPubMedPubMedCentralGoogle Scholar
  25. Karthikeyan N., Prasanna R., Nain L. et al.: Evaluating the potential of plant growth promoting cyanobacteria as inoculants for wheat.–Eur. J. Soil Biol. 43: 23–30, 2007.CrossRefGoogle Scholar
  26. Khan A.S., Ahmad B., Jaskani M.J. et al.: Foliar application of mixture of amino acids and seaweed (Ascophylum nodosum) extract improve growth and physico-chemical properties of grapes.–Int. J. Agric. Biol., 14: 383–388, 2012.Google Scholar
  27. Knypl J.S., Kabzinska E.: Growth, phosphatase and ribonuclease activity in phosphate deficient Spirodela oligorrhiza cultures. Biochem. Physiol. Pfl. 171: 279–287, 1977.Google Scholar
  28. Kreitlow S., Mundt S., Lindequist, U.: Cyanobacteria–a potential source of new biologically active substances.–J. Biotechnol. 70: 61–63, 1999.CrossRefPubMedGoogle Scholar
  29. Kulk M.M.: The potential for using cyanobacteria (blue-green algae) and algae in the biological control of plant pathogenic bacteria and fungi.–Eur. J. Plant Pathol. 101: 85–599, 1995.Google Scholar
  30. Lehmann K., Hause B., Altmann D. et al.: Tomato ribonuclease LX with the functional endoplasmic reticulum retention motif HDEF is expressed during programmed cell death processes, including xylem differentiation, germination, and senescence.–Plant Physiol. 127: 436–449, 2001.CrossRefPubMedPubMedCentralGoogle Scholar
  31. Mahmoud M.S.: Nutritional status and growth of maize plants as affected by green microalgae as soil additives.–J. Biol. Sci. 1: 475–479, 2001.CrossRefGoogle Scholar
  32. Malliga P., Uma L, Subramanian G.: Lignolytic activity of the cyanobacterium Anabena azollae ML2 and the value of coir waste as a carrier for biofertilizer.–Microbios 86: 175–183, 1996.Google Scholar
  33. Markou G., Nerantzis E.: Microalgae for high-value compounds and biofuels production: A review with focus on cultivation under stress conditions.–Biotechnol. Adv. 31: 1532–1542, 2013.CrossRefPubMedGoogle Scholar
  34. Masojídek J., Prášil O.: The development of microalgal biotechnology in the Czech Republic.–J. Ind. Microbiol. Biot. 37: 1307–1317, 2010.CrossRefGoogle Scholar
  35. Mohammadi K., Ghalavand A., Aghaalikhani M.: Study the efficacies of green manure application as chickpea per plant.–World Acad. Sci. Eng. Technol. 46: 233–236, 2010.Google Scholar
  36. Nain L., Rana A., Joshi M. et al.: Evaluation of synergistic effects of bacterial and cyanobacterial strains as biofertilizers for wheat.–Plant Soil 331: 217–230, 2010.CrossRefGoogle Scholar
  37. Nilsson M., Rasmussen U., Bergman B.: Competition among symbiotic cyanobacterial Nostoc strains forming artificial associations with rice (Oryza sativa).–FEMS Microbiol. Lett. 245: 139–144, 2005.CrossRefPubMedGoogle Scholar
  38. Nunnery J.K., Mevers E., Gerwick W.H.: Biologically active secondary metabolites from marine cyanobacteria.–Curr. Opin Biotech. 21: 787–793, 2010.CrossRefPubMedPubMedCentralGoogle Scholar
  39. Obreht Z., Kerby N.W., Gantar M. et al.: Effects of rootassociated N2-fixing cyanobacteria on the growth and nitrogen content of wheat (Triticum vulgare L.) seedlings.–Biol. Fert. Soils 15: 68–72, 1993.CrossRefGoogle Scholar
  40. Perez-Garcia O., Escalante F.M.E., de Bashan L.E. et al.: Heterotrophic cultures of microalgae: Metabolism and potential products.–Water Res. 45: 11–36, 2011.CrossRefPubMedGoogle Scholar
  41. Prakash S., Nikhil N.: Algae as a soil conditioner.–Int. J. Eng. Tech. Res. 2: 68–70, 2014.Google Scholar
  42. Prasad R.C., Prasad B.N.: Cyanobacteria as a source biofertilizer for sustainable agriculture in Nepal.–J. Plant Sci. Bot. Orientalis 1: 127–133, 2001.Google Scholar
  43. Pszczolkowski W., Romanowska-Duda Z., Owczarczyk A. et al.: Influence of Secondary Metabolites from Cyanobacteria on the Growth and Plant Development. Physiological Reports: Current Advances in Algal Taxonomy and its Applications: Phylogenetic, Ecological and Applied Perspective. Pp. 195–203. Institute of Botany, Polish Academy of Sciences, Krakow 2012.Google Scholar
  44. Rana A., Joshi M., Prasanna R. et al.: Biofortification of wheat through inoculation of plant growth promoting rhizobacteria and cyanobacteria.–Eur. J. Soil Biol. 50: 118–126, 2012.CrossRefGoogle Scholar
  45. Rastogi R.P., Sinha R.P.: Biotechnological and industrial significance of cyanobacterial secondary metabolites.–Biotechnol. Adv. 27: 521–539, 2009.CrossRefPubMedGoogle Scholar
  46. Rodríguez A.A., Stella A.A., Storni M.M. et al.: Effects of cyanobacterial extracelular products and gibberellic acid on salinity tolerance in Oryza sativa L.–Saline Syst. 2: 7, 2006.CrossRefPubMedPubMedCentralGoogle Scholar
  47. Roger P.A., Reynaud P.A.: Free-living Blue-green Algae in Tropical Soils. Pp. 147–168. Martinus Nijh Publ., The Hague 1982.Google Scholar
  48. Romanowska-Duda Z., Wolska A., Malecka, A.: Influence of blue-green algae as nitrogen fertilizer supplier in regulation of water status in grapevines under stress conditions.–In: Medrano H. (ed.): Book of Abstracts: COST 858: Water Transport and Aquaporins in Grapevines, October 20–23, Alcudia, Spain. Pp. 10. University of the Balearic Islands, Palma 2004Google Scholar
  49. Romanowska-Duda Z.B., Grzesik M., Owczarczyk A. et al.: Impact of intra and extracellular substances from Cyanobacteria on the growth and physiological parameters of grapevine (Vitis vinifera).–In: Arola L., Carbonell J. (ed.): 20th International Conference on Plant Growth Substance (IPGSA), Book of Abstracts 28.07–02.08. 2010 Pp. 118. Universitat Rovira i Virgili, Tarragona 2010.Google Scholar
  50. Saadatnia H., Riahi H.: Cyanobacteria from paddy fields in Iran as a biofertilizer in rice plants.–Plant Soil Environ. 55: 207–212, 2009.Google Scholar
  51. Sahu D., Priyadarshani I., Rath, B.: Cyanobacteria–as potential biofertilizer.–CIBTech J. Microbiol. 1: 20–26, 2012.Google Scholar
  52. Sergeeva E., Liaimer A., Bergman B.: Evidence for production of the phytohormone indole-3-acetic acid by cyanobacteria.–Planta 215: 229–238, 2002.CrossRefPubMedGoogle Scholar
  53. Shanan N.T., Higazy A.M.: Integrated biofertilization management and cyanobacteria application to improve growth and flower quality of Matthiola incana.–J. Agr. Biol. Sci 5: 1162–1168, 2009.Google Scholar
  54. Shariatmadari Z., Riahi H., Hashtroudi M.S. et al.: Plant growth promoting cyanobacteria and their distribution in terrestrial habitats of Iran.–Soil Sci. Plant Nutr. 59: 535–547, 2013.CrossRefGoogle Scholar
  55. Šindelárová M., Šindelár L., Wilhelmová N. et al.: Changes in key enzymes of viral-RNA biosynthesis in chloroplasts from PVY and TMV infected tobacco plants.–Biol. Plantarum 49: 471–474, 2005.CrossRefGoogle Scholar
  56. Spinelli F., Fiori G., Noferini M. et al.: Perspectives on the use of a seaweed extract to moderate the negative effects of alternate bearing in apple trees.–J. Hortic. Sci. Biotech. 84: 131–137, 2009.CrossRefGoogle Scholar
  57. Spiller H., Gunasekaran M.: Ammonia-excreting mutant strain of the cyanobacterium Anabaena variabilis supports growth of wheat.–Appl. Microbiol. Biot. 33: 477–480, 1990.CrossRefGoogle Scholar
  58. Srivastava S., Emery R.J.N., Kurepin L.V. et al.: Pea PR 10.1 is a ribonuclease and its transgenic expression elevates cytokinin levels.–Plant Growth Regul. 49: 17–25, 2006.CrossRefGoogle Scholar
  59. Song T., Martensson L., Eriksson T.: Biodiversity and seasonal variation of the cyanobacterial assemblage in a rice paddy field in Fujian, China.–FEMS Microbiol. Ecol. 54: 131–140, 2005.CrossRefPubMedGoogle Scholar
  60. Subramanaian G., Uma L.: Cyanobacteria in pollution control.–J. Sci. Ind. Res. India 55: 685–692, 1996.Google Scholar
  61. Swarnalakshmi K., Prasanna C.R., Kumar A. et al.: Evaluating the influence of novel cyanobacterial biofilmed biofertilizers on soil fertility and plant nutrition in wheat.–Eur. J. Soil Biol. 55: 107–116, 2013.CrossRefGoogle Scholar
  62. Thajuddin N., Subramanian G.: Cyanobacterial biodiversity and potential applications in biotechnology.–Curr. Sci. 89: 47–57, 2005.Google Scholar
  63. Tukaj Z.: [Exercise Guide for Plant Physiology.] Pp. 1–186. Wydawnictwo Uniwersytetu Gdanskiego, Gdansk 2007. [In Polish]Google Scholar
  64. Uysal O., Uysal F.O., Ekinci K.: Evaluation of microalgae as microbial fertilizer.–Eur. J. Sustain. Dev. 4: 77–82, 2015.Google Scholar
  65. Vasileva I., Ivanova J., Paunov M et al.:Urea from waste waters–perspective nitrogen and carbon source for green algae Scenedesmus sp. cultivation.–Ecol. Safe. 10: 311–319, 2016.Google Scholar
  66. Wilson L.T.: Cyanobacteria: A potential nitrogen source in rice fields.–Texas Rice 6: 9–10, 2006.Google Scholar

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Authors and Affiliations

  1. 1.Research Institute of HorticultureSkierniewicePoland
  2. 2.Laboratory of Plant EcophysiologyUniversity of LodzLodzPoland
  3. 3.SI TechnologyWarsawPoland
  4. 4.Department of Plant Physiology, Faculty of Agriculture and BiologyWarsaw University of Life Sciences SGGWWarsawPoland

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