CoChat
Sign Up
Cited by 58Plant Growth Enhancement TechniquesAgriculture, Plant Science, Crop ManagementAgricultural Science and Fertilization

Spirulina platensis biofertilization for enhancing growth, photosynthetic capacity and yield of Lupinus luteus

Open access
Shedeed, Zeinab A., Gheda, Saly, Elsanadily, Sara, Alharbi, Khadiga, Osman, Mohamed E. H.·2022·Agriculture
DOI 10.3390/agriculture12060781
Open this paper in CoChat — free accountOpen PDF

Abstract

Cyanobacteria can play an important role in sustainable agriculture by improving crop growth and production, as well as environmental quality. The current study was conducted to evaluate the role of Spirulina platensis extract in the improvement of growth, photosynthetic capacity and yield of Lupinus luteus. Different concentrations (0.25, 0.5 and 1.0%) of S. platensis methanolic extract were used for priming seeds and foliar spraying applications. Growth, photosynthetic pigment content and activity were recorded at 35 days of cultivation. The yield measurements and protein profile of seeds were performed at 60 days. For both treatments, the lower concentration (0.25%) of the extract was the most successful in improving all growth metrics and the phytohormonal level of L. luteus. Photosynthetic pigment and capacity, nutrient content and yield components of L. luteus were improved with the extract of 0.25% concentration. However, the growth was significantly inhibited at the higher concentration (1.0%), recording lower values of the measured characters than the control. A positive correlation was observed between the total chlorophyll, photosynthetic rate, yield parameters and carbohydrate accumulation by the application of the S. platensis extracts. The protein profile of seeds revealed that spraying treatment triggered the appearance of a new band of 30.56 KDa. The promotion of growth could be attributed to the nutrients, bioactive molecules and phytohormones in the extract. The use of Spirulina-based stimulators is reliable with the concept of sustainable agriculture by enhancing photosynthetic pigment content and rate ensuring the correlation between the yield and those measured parameters of L. luteus.

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Integrity signals

Registry

Crossref · 10.3390/agriculture12060781

Cites

2 of 2 references verified0 citation errors · 0 not checkable

Statistics

Claims the paper makes

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

  • Terrestrial studies have confirmed the efficacy of spirulina in supporting the growth of a variety of legumes, tomato, and lettuce varieties.

    “Additionally, terrestrial studies have confirmed the efficacy of spirulina in supporting the growth of a variety of legumes, tomato, and lettuce varieties (Shedeed et al., 2022;Bhowmik et al., 2010;Taha et al., 2023;Anitha et al., 2016;Akgul and Akgul, 2019),”

    From Spirulina supported plant growth in regolith simulants and elevated levels of CO2 (2025) · cites this paper as Shedeed et al., 2022

    Section 3.1 (page unavailable) reports that 0.25% Spirulina platensis extract significantly improved growth of Lupinus luteus, a legume, compared with controls. This paper's own experiment does not establish growth benefits for a variety of legumes, tomatoes, or lettuce; it also reports growth inhibition at the highest concentration tested. (LLM, conf=0.87)

    Experimental — accuracy not yet measured

  • Under terrestrial conditions, spirulina fertilization enhances photosynthetic pigment content and improves growth and yield rates.

    “Under terrestrial conditions, plants fertilized with spirulina exhibit increased biomass (Singh, 2014), enhanced photosynthetic pigment content, improved growth and yield rates (Shedeed et al., 2022), greater productivity including marketable yield and nitrogen fixation (Geries and Elsadany, 2021), and elevated micronutrient content (Anitha et al., 2016).”

    From Spirulina supported plant growth in regolith simulants and elevated levels of CO2 (2025) · cites this paper as Shedeed et al., 2022

    The Abstract reports increased photosynthetic pigments, growth and yield in Lupinus luteus treated with 0.25% Spirulina extract. It also reports that 1.0% inhibited growth. The citing sentence generalizes the benefit to plants fertilized with Spirulina without the species and concentration qualifications. (LLM, conf=0.87)

    Experimental — accuracy not yet measured

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The self-check needs the paper’s full text.

Cites

Flagged first, then by citations

Research works printed but not linked: 63

  1. Win, T.T.; Barone, G.D.; Secundo, F.; Fu, P. Algal biofertilizers and plant growth stimulants for sustainable agriculture. Indust. Biotechnol. 2018, 14, 4. [CrossRef] · DOI
  2. Kumar, G.; Shekh, A.; Jakhu, S.; Sharma, Y.; Kapoor, R.; Sharma, T.R. Bioengineering of microalgae: Recent advances, perspectives, and regulatory challenges for industrial application. Front. Bioeng. Biotechnol. 2020, 8, 914. [CrossRef] [PubMed] · DOI · Paper page
  3. Singh, S. A review on possible elicitor molecules of cyanobacteria: Their role in improving plant growth and providing tolerance against biotic or abiotic stress. J. Appl. Microbiol. 2014, 117, 1221-1244. [CrossRef] [PubMed] · DOI · Paper page
  4. Santini, G.; Biondi, N.; Rodolfi, L.; Mario, R. Tredici Cyanobacteria: An emerging strategy to improve yields and sustainability in agriculture. Plants 2021, 10, 643. [CrossRef] · DOI
  5. Ranjan, K.; PriyaRamakrishnan, P.; Shivay, S. Cyanobacterial inoculation modifies the rhizosphere microbiome of rice planted to a tropical alluvial soil. Appl. Soil Ecol. 2016, 108, 195-203. [CrossRef] · DOI
  6. Tuhy, L.; Smoraj, M.; Witkowska, Z.; Chojnacka, K. Biofortification of maize with micronutrients by Spirulina. Open Chem. 2015, 13, 1119-1126. [CrossRef] · DOI
  7. Górka, B.; Korzeniowska, K.; Lipok, J.; Wieczorek, P.P. The Biomass of Algae and Algal Extracts in Agricultural Production. In Algae Biomass: Characteristics and Applications; Springer Science and Business Media LLC: Berlin/Heildeberg, Germany, 2018; pp. 103-114.
  8. Renuka, N.; Guldhe, A.; Prasanna, R.; Singh, P.; Bux, F. Microalgae as multi-functional options in modern agriculture: Current trends, prospects and challenges. Biotechnol. Adv. 2018, 36, 1255-1273. [CrossRef] · DOI
  9. Anitha, L.; Bramari, G.S.; Kalpana, P. Effect of supplementation of Spirulina platensis to enhance the zinc status in plants of Amaranthus gangeticus, Phaseolus aureus and Tomato. Adv. Biosc. Biotechnol. 2016, 7, 289-299. [CrossRef] · DOI · Paper page
  10. Battacharyya, D.; Babgohari, M.Z.; Rathor, P.; Prithiviraj, B. Seaweed extracts as biostimulants in horticulture. Sci. Hortic. 2015, 196, 39-48. [CrossRef] · DOI
  11. Niewiadomska, A.; Sulewska, H.; Wolna-Maruwka, A.; Ratajczak, K.; Waraczewska, Z.; Budka, A. The Influence of Bio-Stimulants and Foliar Fertilizers on Yield, Plant Features, and the Level of Soil Biochemical Activity in White Lupine (Lupinus albus L.) cultivation. Agronomy 2020, 10, 150. [CrossRef] · DOI
  12. Panda, D.; Pramanik, K.; Nayak, B.R. Use of seaweed extracts as plant growth regulators for sustainable agriculture. Int. J. Bio-Resour. Stress Manag. 2012, 3, 404-411.
  13. Godlewska, K.; Michalak, I.; Pacyga, P.; Baślady ńska, S.; Chojnacka, K. Potential applications of cyanobacteria: Spirulina platensis filtrates and homogenates in agriculture. World J. Microbiol. Biotechnol. 2019, 35, 1-18. [CrossRef] [PubMed] · DOI · Paper page
  14. Ahsan, M.; Habib, B.; Parvin, M.; Hasan, R. A Review on Culture, Production and Use of Spirulina as Food for Humans and Feeds for Domestic Animals and Fish; FAO: Rome, Italy, 2008.
  15. Fenner, K.; Canonica, S.; Wackett, L.P.; Elsner, M. Evaluating pesticide degradation in the environment: Blindspots and emerging opportunities. Science 2013, 341, 752-758. [CrossRef] [PubMed] · DOI
  16. Mala, R.; Ruby, A.S.; Mahalakshmi, R.; Rajeswari, S. Agronomic biofortification of Amaranthus dubius with macro nutrients and vitamin A. In Proceedings of the IOP Conference Series: Materials Science and Engineering, Narsimha Reddy Engineering College, Secunderabad, India, 3-4 July 2017.
  17. Bhowmik, D.; Dubey, J.; Mehra, S. Evaluating potential of Spirulina as inoculant for pulses. Acad. J. Plant Sci. 2010, 3, 161-164.
  18. Geries, L.S.M.; Elsadany, A.Y. Maximizing growth and productivity of onion (Allium cepa L.) by Spirulina platensis extract and nitrogen-fixing endophyte Pseudomonas stutzeri. Arch. Microbiol. 2021, 203, 169-181. [CrossRef] · DOI · Paper page
  19. Hama, J.R.; Bjarne, W.S. Natural alkaloids from narrow-leaf and yellow lupins transfer to soil and soil solution in agricultural fields. Environ. Sci. Eur. 2020, 32, 126. [CrossRef] · DOI
  20. Knecht, K.T.; Sanchez, P.; Kinder, D.H. Lupine Seeds (Lupinus spp.): History of Use, Use as An Antihyperglycemic Medicinal, and Use as a Food Plant Nuts and Seeds in Health and Disease Prevention. In Nuts and Seeds in Health and Disease Prevention, 2nd ed.; Academic Press: Cambridge, MA, USA, 2020; pp. 393-402.
  21. Lucas, M.M.; Stoddard, F.L.; Annicchiarico, P.; Frías, J.; Martínez-Villaluenga, C.; Sussmann, D.; Duranti, M.; Seger, A.; Zander, P.M.; Pueyo, J.J. The future of lupin as a protein crop in Europe. Front. Plant Sci. 2015, 6, 705. [CrossRef] · DOI
  22. Zarrouk, C. Contribution a L'etude D'une Cyanobacterie: Influence de Divers Facteurs Physiques et Chimiques Sur la Croissance et la Photosynthese de Spirulina Maxima (Setchell et Gardner) Geitler. Ph.D Thesis, University of Paris, Paris, France, 1966.
  23. Pant, G.; Kumar, G.; Karthik, L.; Prasuna, R.G.; Bhaskara, K.V. Antioxidant activity of methanolic extract of blue green algae Anabaena sp. (Nostocaceae). Eur. J. Exp. Biol. 2011, 1, 156-162.
  24. Metzner, H.; Rau, H.; Senger, H. Studies on synchronization of some pigment-deficient Chlorella mutants. Planta 1965, 65, 186. [CrossRef] · DOI
  25. Essa, H.L.; Abdelfattah, M.S.; Marzouk, A.S.; Shedeed, Z.A.; Guirguis, H.A.; El-Sayed, M.M.H. Biogenic copper nanoparticles from Avicennia marina leaves: Impact on seed germination, detoxification enzymes, chlorophyll content and uptake by wheat seedlings. PLoS ONE 2021, 16, e0249764. [CrossRef] [PubMed] · DOI
  26. Laemmli, U.K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 1970, 227, 680e5. [CrossRef] [PubMed] · DOI · Paper page
  27. Wasfy, W.S.; Orrin, E.S. Identification of plant hormones from Cotton ovules. Plant Physiol. 1975, 55, 550-554.
  28. Ronga, D.; Biazzi, E.; Parati, K.; Carminati, D.; Carminati, E.; Tava, A. Microalgal Biostimulants and Biofertilisers in Crop Productions. Agronomy 2019, 9, 192. [CrossRef] · DOI · Paper page
  29. Supraja, K.V.; Bunushree, B.; Balasubramanian, P. Efficacy of microalgal extracts as biostimulants through seed treatment and foliar spray for tomato cultivation. Ind. Crop. Prod. 2020, 151, 112453.
  30. Wally, O.S.D.; Critchley, A.T.; Hiltz, D.; Craigie, J.S.; Han, X.; Zaharia, L.I.; Abrams, S.R.; Prithiviraj, B. Regulation of phytohor- mone bio-synthesis and accumulation in Arabidopsis following treatment with commercial extract from the marine macroalga Ascophyllum nodosum. J. Plant Growth Regul. 2013, 32, 324-339. [CrossRef] · DOI
  31. 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. 2000, 2, 944-951. [CrossRef] · DOI
  32. Singh, D.P.; Prabha, R.; Yandigeri, M.S.; Arora, D.K. Cyanobacteria-mediated phenylpropanoids and phytohormones in rice (Oryza sativa) enhance plant growth and stress tolerance. Antonie Van Leeuwenhoek 2011, 100, 557-568. [CrossRef] · DOI
  33. Sergeeva, E.; Liaimer, A.; Bergman, B. Evidence for production of the phytohormone indole-3-acetic acid by cyanobacteria. Planta 2002, 215, 229-238. [CrossRef] · DOI
  34. Ghaderiardakani, F.; Collas, E.; Damiano, D.K.; Tagg, K.; Graham, N.S.; Coates, J.C. Effects of green seaweed extract on Arabidopsis early development suggest roles for hormone signalling in plant responses to algal fertilizers. Sci. Rep. 2019, 9, 1983. [CrossRef] · DOI
  35. Likhitkar, V.S.; Tarar, J.L. Effect of presoaking seed treatment with Nostoc muscorum extracts on cotton. Ann. Plant Physiol. 1995, 9, 113-116.
  36. Adam, M.S. The promotive effect of the cyanobacterium Nostoc muscorum on the growth of some crop plants. Acta Microbiol. Pol. 1999, 48, 163-171.
  37. Dreakeiwicz, M. Chlorophyllase: Occurrence, functions, mechanism of action, effect of external and internal factors. Photosynthet- ica 1994, 30, 321-332.
  38. Rana, A.; Joshi, M.; Prasanna, R.; Shivay, Y.S.; Nain, L. Biofortification of wheat through inoculation of plant growth promoting rhizobacteria and cyanobacteria. Eur. J. Soil Biol. 2012, 50, 118-126. [CrossRef] · DOI
  39. Osman, M.E.H.; Abo-Shady, A.M.; Maysa, M.F.; El-Nagar, M.M.F. The treatment of broad bean seeds with algal suspensions to study their effects on certain growth and yield parameters. J. Environ. Sci. 2020, 49, 1-7. [CrossRef] · DOI
  40. Salvi, L.; Brunetti, C.; Cataldo, E.; Storchi, P.; Mattii, G.B. Eco-physiological traits and phenylpropanoid profiling on potted Vitis vinifera L. cv Pinot Noir Subjected to Ascophyllum nodosum treatments under post-version low water availability. Appl. Sci. 2020, 10, 4473. [CrossRef] · DOI
  41. Abul Faiz, M.D.; Rakibuzzaman, M.D.; Wasin, E.S.; Asmaul, M.S.T.; Mahato, A.K. Foliar application of Spirulina and Oscillatoria on growth and yield of okra as bio-fertilizer. J. Biosci. Agri. Res. 2019, 22, 1840-1844.
  42. Agwa, O.K.; Ogugbue, C.J.; Williams, E.E. Field evidence of Chlorella vulgaris potentials as a biofertilizer for Hibiscus esculentus. Int. J. Agric. Res. 2017, 12, 181-189. [CrossRef] · DOI
  43. Puglisi, I.; Bella, E.; Rovetto, E.I.; Lo Piero, A.R.; Baglieri, A. Biostimulant effect and biochemical response in lettuce seedlings treated with a Scenedesmus quadricauda extract. Plants 2020, 9, 123. [CrossRef] · DOI
  44. Spinelli, F.; Fiori, G.; Noferini, M.; Sprocatti, M.; Costa, G. A novel type of seaweed extract as a natural alter-native to the use of iron chelates in strawberry production. Sci. Hortic. 2010, 125, 263-269. [CrossRef] · DOI
  45. Fan, D.; Hodges, D.M.; Critchley, A.T.; Prithiviraj, B.A. Commercial extract of brown macroalga (Ascophyllum nodosum) affects yield and the nutritional quality of spinach in vitro. Commun. Soil Sci. Plant Anal. 2013, 44, 1873-1884. [CrossRef] · DOI
  46. Villarruel-López, A.; Ascencio, F.; Nuño, K. Microalgae, a potential natural functional food Source-A Review. Pol. J. Food Nutr. Sci. 2017, 67, 251-263. [CrossRef] · DOI
  47. Fredeen, A.L.; Raab, T.K.; Rao, I.M.; Terry, N. Effects of phosphorus nutrition on photosynthesis in Glycine max L. Merr. Planta 1990, 181, 399-405. [CrossRef] [PubMed] · DOI
  48. Priyadarshani, I.; Rath, B. Commercial and industrial applications of micro algae-A review. J. Algal. Biomass Utln. 2012, 89-100.
  49. Sun, T.; Rao, S.; Zhou, X.; Li, L. Plant carotenoids: Recent advances and future perspective Molecul. Horticulture 2022, 2, 3. [CrossRef] · DOI
  50. Li, Y.; He, N.; Hou, J.; Xu, L.; Liu, C.; Zhang, J.; Wang, Q.; Zhang, X.; Wu, X. Factors influencing leaf chlorophyll content in natural forests at the biome scale. Front. Ecol. Evol. 2018, 6, 64. [CrossRef] · DOI
  51. Mikiciuk, M.; Dobrolmilska, R. Assessment of yield and physiological indices of small-sized tomato cv. 'Bianka F1' under the influence of biostimulators of marine algae origin. Acta Sci. Pol. Hort. Cultus. 2014, 13, 31-41.
  52. Xu, C.; Leskovar, D.I. Effect of A. nodosum extracts on spinach growth, physiology and nutrition value under drought stress. Sci. Hort. 2015, 183, 39-47. [CrossRef] · DOI
  53. Wong, S.C.; Cowan, I.R.; Farquhar, G.D. Stomatal conductance correlates with photosynthetic capacity. Nature 1979, 282, 424-426. [CrossRef] · DOI
  54. Qu, M.; Hamdani, S.; Li, W.; Wang, S.; Tang, J.; Chen, Z.; Song, Q.; Li, M.; Zhao, H.; Chang, T.; et al. Rapid stomatal response to fluctuating light: An under-explored mechanism to improve drought tolerance in rice. Funct. Plant Biol. 2016, 43, 727-773. [CrossRef] · DOI
  55. Mutale-joan, C.; Redouane, B.; Najib, E.; Yassine, K.; Lyamlouli, K.; Laila, S.; Zeroual, Y.; Hicham, E. Screening of microalgae liquid extracts for their bio stimulant properties on plant growth, nutrient uptake and metabolite profile of Solanum lycopersicum L. Sci. Rep. 2020, 10, 2820. [CrossRef] [PubMed] · DOI
  56. Sakoda, K.; Yamori, W.; Shimada, T.; Sugano, S.S.; Hara-Nishimura, I.; Tanaka, Y. Stomatal density affects gas diffusion and CO2 assimilation dynamics in Arabidopsis under fluctuating light. bioRxiv 2020. [CrossRef] · DOI
  57. Pego, J.V.; Kortstee, A.J.; Huijser, C.; Smeekens, S. Photosynthesis, sugars and the regulation of gene expression. J. Exp. Bot. 2000, 51, 407-416. [CrossRef] [PubMed] · DOI
  58. Araya, T.; Noguchi, K.; Terashima, I. Effects of carbohydrate accumulation on photosynthesis differ between sink and source leaves of Phaseolus vulgaris L. Plant Cell Physiol. 2006, 47, 644-652. [CrossRef] [PubMed] · DOI
  59. Osman, M.E.H.; El-Sheekh, M.; El-Naggar, A.; Gheda, S. Effect of two species of cyanobacteria as biofertilizers on some metabolic activities, growth, and yield of pea plant. Biol. Fert. Soils 2010, 6, 861-875. [CrossRef] · DOI
  60. Popova, L.P.; Stoinova, Z.G.; Maslenkova, L.T. Involvement of abscisic acid in photosynthetic process in Hordeum vulgare L. during salinity stress. J. Plant Growth Regul. 1995, 4, 211-218. [CrossRef] · DOI
  61. Duranti, M.; Consonni, A.; Magni, C.; Sessa, F.; Scarafoni, A. The major proteins of lupin seed: Characterization and molecular properties for use as functional and nutraceutical ingredients. Trends Food Sci. Technol. 2008, 19, 624-633. [CrossRef] · DOI
  62. Melo, T.S.; Ferreira, R.B.; Teixeira, A.N. The seed storage proteins from Lupinus albus. Phytochemistry 1994, 37, 641-648. [CrossRef] · DOI
  63. Dobiesz, W.; Piotrowicz-Cieślak, A.I. Proteins in relation to vigor and viability of white Lupin (Lupinus albus L.) Seed Stored for 26 Years. Front. Plant Sci. 2017, 8, 1392. [CrossRef] · DOI

Cited by

Sorted by citations

Authors
Shedeed, Z. A., Gheda, S., Elsanadily, S., Alharbi, K., & Osman, M. E. H.
Affiliations
  • Helwan University (EG)
  • Tanta University (EG)
  • Princess Nourah bint Abdulrahman University (SA)
Corresponding author
Alharbi, Khadiga
ORCID
Venue
Agriculture
Publisher
MDPI AG
Published
2022-05-29
Volume
12
Issue
6
Pages
781
ISSN
2077-0472 (ISSN-L)
DOI
10.3390/agriculture12060781
OpenAlex
W4281623015
Cited by
58
References
2
Citations by year
2026: 19 · 2025: 17 · 2024: 11 · 2023: 7 · 2022: 4
FWCI
5.15
Type
journal article
Language
en
Open access
Licence
Locations
  • Agriculture (publishedVersion, cc-by)
  • RePEc: Research Papers in Economics (submittedVersion)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
Funders
  • Helwan University
  • Tanta University
  • Faculty of Science, Tanta University
Topics
  • Life Sciences › Agricultural and Biological Sciences › Plant Science › Plant Growth Enhancement Techniques
  • Life Sciences › Agricultural and Biological Sciences › Plant Science › Agriculture, Plant Science, Crop Management
  • Life Sciences › Agricultural and Biological Sciences › Soil Science › Agricultural Science and Fertilization
Keywords
Spirulina platensis, Lupinus luteus, biofertilizers, cyanobacterial extracts, seed priming, foliar application, photosynthetic pigments, chlorophyll, photosynthetic capacity, seed yield, seed protein profile, plant hormones, carbohydrate accumulation, legume growth

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review