Phosphate solubilization and the enhancement of chickpea growth by new rhizospheric microorganisms Bacillus tequilensis and Trichoderma orientale

Authors

  • Ahmed Amine Bekkar Laboratory of Research on Biological Systems and Geomatics (L.R.S.B.G), Department of Agronomy, Faculty of Life and Natural Sciences, University Mustapha Stambouli of Mascara, Algeria https://orcid.org/0000-0002-3896-1195
  • Souad Zaim Laboratory of Research on Biological Systems and Geomatics (L.R.S.B.G), Department of Agronomy, Faculty of Life and Natural Sciences, University Mustapha Stambouli of Mascara, Algeria https://orcid.org/0000-0002-2787-8951

DOI:

https://doi.org/10.2298/ABS230823034B

Keywords:

Phosphate solubilizing microorganisms (PSMs), Co-inoculation, Bacillus tequilensis, Trichoderma orientale, Biofertilization

Abstract

Paper description:

  • Microbial solubilization of phosphate to maintain soil fertility is an eco-friendly and less expensive alternative to chemical fertilizers.
  • Species of soil Bacillus and Trichoderma that colonize mainly in the rhizosphere can solubilize soil-insoluble phosphates.
  • Phosphate-solubilizing microorganisms (PSMs) were assessed in vitro and in vivo. The application of the two strains separately and in combination had a beneficial effect on germination by promoting the development of the seeds and effectively enhancing plant growth.
  • This is the first report on the P-solubilizing potential of the combined microorganisms Bacillus tequilensis and Trichoderma orientale and their capacity to promote plant growth in chickpeas

Abstract: Two Trichoderma strains and three Bacillus strains isolated from the rhizosphere of healthy chickpeas in Algeria were assessed for their phosphate solubilizing capacity in vitro as well as their growth effects on seedlings of the chickpea in pot experiments. The microorganisms tested had higher phosphate-solubilizing activities, with the solubilization index ranging from 2.41 to 7.40. The concentration of solubilized phosphate varied from 30.17 to 157.44 μg/mL. The maximum phosphate-solubilizing activity was observed in the two culture filtrates of Bacillus tequilensis Bt1 (157.44 μg/mL) and Trichoderma orientale T1 (143.33 μg/mL), accompanied by a decrease in pH of the growth medium from 4.51 to 5.75. The application of the strains (B. tequilensis Bt1 and T. orientale T1) separately and in combination had a beneficial effect on germination by promoting the development of the seeds and effectively enhancing plant growth. Chickpea seedlings showed better vegetative growth when treated with a mixture of B. tequilensis Bt1 and T. orientale T1 together than an individual treatment. To our knowledge, this is the first report of the phosphate-solubilizing potential of the combined microorganisms B. tequilensis and T. orientale and their capacity to promote plant growth in chickpeas.

Downloads

Download data is not yet available.

Author Biography

Souad Zaim, Laboratory of Research on Biological Systems and Geomatics (L.R.S.B.G), Department of Agronomy, Faculty of Life and Natural Sciences, University Mustapha Stambouli of Mascara, Algeria

Prof

References

Zaim S, Belabid L, Bellahcene M. Biocontrol of chickpea Fusarium wilt by Bacillus spp. rhizobacteria. J Plant Protect Res. 2013;53:177-183. https://doi.org/10.2478/jppr-2013-0027

Liu Y, Chen J. Phosphorus Cycle. In: Jørgensen SE, Fath BD, editors. Encyclopedia of ecology. Oxford: Academic Press; 2008. p. 2715-24. https://doi.org/10.1016/B978-008045405-4.00754-0

Hodges SC. Soil fertility basics: NC certified crop advisor training. . USA: Soil science extension, North Carolina State University; 2010. 75 p.

Vassileva M, Azcon R, Barea JM, Vasslev N. Rock phosphate solubilization by free and encapsulated cells of Yarowia lipolytica. Proc Biochem. 2000;35(7):693-97. https://doi.org/10.1016/S0032-9592(99)00132-6

Rodriguez H, Fraga R. Phosphate solubilizing bacteria and their role in plant growth promotion. Biotechnol Adv. 1999;17(4-5):319-39.https://doi.org/10.1016/S0734-9750(99)00014-2

Silva IO, da Rocha Amorim EP, Junior NAN, Carnauba JP, de Araújo Neto F, de Lima IV. Molecular identification of isolates of Trichoderma spp as biocontroller of Fusarium falciforme, causal agent of root rot of table manioc (Manihot esculenta Crantz) var. rosinha in the State of Alagoas/Brazil. Res Soc Dev. 2022; 11(13): e124111335217. https://doi.org/10.33448/rsd-v11i13.35217

Haroon U, Munis MFH., Liaquat F, Khizar M, Elahi M, Chaudhary HJ. Biofilm formation and flocculation potential analysis of halotolerant Bacillus tequilensis and its inoculation in soil to mitigate salinity stress of chickpea. Physiol Mol Biol Plants. 2023; 29(2):277-88.

Zaim S, Bekkar AA, Belabid L. Efficacy of Bacillus subtilis and Trichoderma harzianum combination on chickpea Fusarium wilt caused by F. oxysporum f. sp. ciceris. Arch Phytopathol Pflanzenschutz. 2018;51(3-4):217-26. https://doi.org/10.1080/03235408.2018.1447896

Bekkar AA, Zaim S, Belabid L. Induction of systemic resistance in chickpea against Fusarium wilt by Bacillus strains. Arch Phytopathol Pflanzenschutz. 2018;51(1-2):70-80. https://doi.org/10.1080/03235408.2018.1438819

Pikovskaya RI. Mobilization of phosphorus in soil in connection with vital activity of some microbial species. Mikrobiologiya. 1948;17:362-70.

Edi-Premono M, Moawad AM, Vlek PLG. Effect of phosphate solubilizing Pseudomonas putida on the growth of maize and its survival in the rhizosphere. Indones J Crop Sci. 1996;11:13-23.

Olsen SR, Sommers LE. Phosphorus. In: Page AL, Miller RH, Keeney DR, editors. Methods of Soil Analysis, Part 2: Chemical and Microbial Properties. 1st ed. Madison, Wisconsin: American Society of Agronomy; 1982. p. 403-30.

Lane DJ. 16S/23S rRNA sequencing. In: Stackebrandt E, Goodfellow M, editors. Nucleic acid techniques in bacterial systematics. New York: Wiley; 1991. p. 115-75.

White TJ, Bruns T, Lee S, Taylor J. Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innis MA, Gelfand DH, Sninsky JJ, White TJ, editors. PCR Protocols: a guide to methods and applications. San Diego: Academic Press; 1990. p 315-22. https://doi.org/10.1016/b978-0-12-372180-8.50042-1

Carbone I, Kohn LM. A method for designing primer sets for speciation studies in filamentous ascomycetes. Mycologia. 1999;91(3):553-56. https://doi.org/10.1080/00275514.1999.12061051

Kumar S, Stecher G, Li M, Knyaz C, Tamura, K. MEGA X: molecular evolutionary genetics analysis across computing platforms. Mol Biol Evol. 2018;35(6):1547-49. https://doi.org/10.1093/molbev/msy096

Gupta R, Singal R, Shankar A, Kuhad RC, Saxena RK.A modified plate assay for screening phosphate solubilizing microorganisms. J Gen Appl Microbiol. 1994;40(3):255-60. https://doi.org/10.2323/jgam.40.255

Akintokun AK, Akande, GA, Akintokun PO, Popoola TOS, Babalola AO. Solubilization on insoluble phosphate by organic acid-producing fungi isolated from Nigerian soil. Int J Soil Sci. 2007;2(4):301-07. http://dx.doi.org/10.3923/ijss.2007.301.307

de Freitas Duarte N, Paiva CAO, Pagano MC, Correa EJA. Phosphate solubilization by microorganisms. In: Singh HB, Vaishnav A, editors. New and Future Developments in Microbial Biotechnology and Bioengineering: Sustainable Agriculture: Advances in Microbe-based Biostimulants. Amsterdam: Elsevier; 2022. p. 257-82. https://doi.org/10.1016/B978-0-323-85163-3.00019-3

Maharana R, Dhal NK. Solubilization of rock phosphate by phosphate solubilizing bacteria isolated from effluent treatment plant sludge of a fertilizer plant. Folia Microbiol (Praha). 2022;67:605-15. https://doi.org/10.1007/s12223-022-00953-w

Elias F, Woyessa D, Muleta D. Phosphate solubilization potential of rhizosphere fungi isolated from plants in Jimma Zone, Southwest Ethiopia. Int J Microbiol. 2016;2016:5472601. http://dx.doi.org/10.1155/2016/5472601

Ahmad A, Moin SF, Liaqat I, Saleem S, Muhammad F, Mujahid T, Zafar U. Isolation, Solubilization of Inorganic Phosphate, and Production of Organic Acids by Individual and Co-inoculated Microorganisms. Geomicrobiol J. 2023;40(3):111-21. https://doi.org/10.1080/01490451.2022.2124329

Vassileva M, Mendes GDO, Deriu MA, Benedetto GD, Flor-Peregrin E, Mocali S, Martos V, Vassilev N. Fungi, P-solubilization, and plant nutrition. Microorganisms. 2022;10(9):1716. https://doi.org/10.3390/microorganisms10091716

Jain R, Saxena J, Sharma V. The ability of two fungi to dissolve hardly soluble phosphates in solution. Mycology. 2017;8(2):104-10.https://doi.org/10.1080/21501203.2017.1314389

Vazquez P, Holquin G, Puente ME, Lopez-Cortez A, Bashan Y. Phosphate solubilizing microorganism associated with the rhizosphere of mangroves in a semi arid coastal lagoon. Biol Fertil Soils. 2000;30:460-68. https://doi.org/10.1007/s003740050024

Yan Z, Zheng XW, Chen JY, Han JS, Han BZ. Effect of different Bacillus strains on the profile of organic acids in a liquid culture of Daqu. J Inst Brew. 2013;119(1-2):78-83. https://doi.org/10.1002/jib.58

Reed RC, Bradford KJ, Khanday I. Seed germination and vigor: ensuring crop sustainability in a changing climate. Heredity. 2022;128:450-59. https://doi.org/10.1038/s41437-022-00497-2

Konappa N, Krishnamurthy S, Arakere UC, Chowdappa S, Ramachandrappa NS. Efficacy of indigenous plant growth-promoting rhizobacteria and Trichoderma strains in eliciting resistance against bacterial wilt in a tomato. Egypt J Biol Pest Control. 2020;30:106. https://doi.org/10.1186/s41938-020-00303-3

Windham MT, Elad R, Baker R.A mechanism for increased plant growth induced by Trichoderma spp. Phytopatholgy. 1986;76:518-21. http://dx.doi.org/10.1094/Phyto-76-518

Mastouri F, Björkman T, Harman GE. Seed treatment with Trichoderma harzianum alleviates biotic, abiotic, and physiological stresses in germinating seeds and seedlings. Phytopathology. 2010;100:1213-21. https://doi.org/10.1094/PHYTO-03-10-0091

Marra LM, de Oliveira-Longatti SM, Soares CRFS, Olivares FL, Moreira FMDS. The amount of phosphate solubilization depends on the strain, C-source, organic acids and type of phosphate. Geomicrobiol J. 2019;36(3):232-42. https://doi.org/10.1080/01490451.2018.1542469

Rudresh DL, Shivaprakash MK, Prasad RD. Effect of combined application of Rhizobium, phosphate solubilizing bacterium and Trichoderma spp. on growth, nutrient uptake and yield of chickpea (Cicer aritenium L.). Appl Soil Ecol. 2005;28(2):139-46. https://doi.org/10.1016/j.apsoil.2004.07.005

Moreira FM, Cairo PAR, Borges AL, da Silva LD, Haddad F. Investigating the ideal mixture of soil and organic compound with Bacillus sp. and Trichoderma asperellum inoculations for optimal growth and nutrient content of banana seedlings. S Afr J Bot. 2021;137:249-56. https://doi.org/10.1016/j.sajb.2020.10.021

Escalas A, Hale L, Voordeckers JW, Yang Y, Firestone MK, Alvarez-Cohen L, Zhou J. Microbial functional diversity: from concepts to applications. Ecol Evolut. 2019;9(20):12000-16. https://doi.org/10.1002/ece3.5670

Wani P, Khan M, Zaidi A. Co-inoculation of nitrogen-fixing and phosphate-solubilizing bacteria to promote growth, yield and nutrient uptake in chickpea. Acta Agronomica Hungarica. 2007;55(3):315-23. https://doi.org/10.1556/AAgr.55.2007.3.7

Elkoca E, Kantar F, Sahin F. Influence of nitrogen fixing and phosphorus solubilizing bacteria on the nodulation, plant growth, and yield of chickpea. J Plant Nutr. 2007;31(1):157-71. https://doi.org/10.1080/01904160701742097

Gupta SB, Thakur KS, Tedia K, Singh K.Influence of Trichoderma viride on Performance of chick pea in wilt complex area. Ann Pl Protec Sci. 2006;14(1):120-24.

Peix A, Rivas-Boyero AA, Mateos PF, Rodriguez-Barrueco C, Martinez-Molina E, Velazquez E. Growth promotion of chickpea and barley by a phosphate solubilizing strain of Mesorhizobium mediterraneum under growth. Soil Biol Biochem. 2001;33(1):103-10. https://doi.org/10.1016/S0038-0717(00)00120-6

Gull M, Hafeez FY, Saleem M, Malik KA. Phosphorus uptake and growth promotion of chickpea by co-inoculation of mineral phosphate solubilising bacteria and a mixed rhizobial culture. Aust J Exp Agric. 2004;44(6):623-628. https://doi.org/10.1071/EA02218

Singh O, Gupta M, Mittal V, Kiran S, Nayyar H, Gulati A, Tewari R. Novel phosphate solubilizing bacteria ‘Pantoea cypripedii PS1’ along with Enterobacter aerogenes PS16 and Rhizobium ciceri enhance the growth of chickpea (Cicer arietinum L.). Plant Growth Regul. 2014;73:79-89. https://doi.org/10.1007/s10725-013-9869-5

Kapri A, Tewari L. Phosphate solubilization potential and phosphatase activity of rhizospheric Trichoderma spp. Braz J Microbiol. 2010;41:787-95. https://doi.org/10.1590/S1517-83822010005000001

Midekssa MJ, Löscher CR, Schmitz RA, Assefa F. Phosphate solubilization and multiple plant growth promoting properties of rhizobacteria isolated from chickpea (Cicer aeritinum L.) producing areas of Ethiopia. Afr J Biotechnol. 2016;15(35):1899-912. https://doi.org/10.5897/AJB2015.15172

Mouria B, Ouazzani-Touhami A, Douira A. Effet de diverses souches du Trichoderma sur la croissance d'une culture de tomate en serre et leur aptitude à coloniser les racines et le substrat. Phytoprotection. 2008;88(3):103-10. https://doi.org/10.7202/018955ar

Gravel V, Antoun V, Tweddell RJ. Growth stimulation and fruit yield improvement of greenhouse tomato plants by inoculation with Pseudomonas putida or Trichoderma atroviride: possible role of indole acetic acid (IAA). Soil Biol Biochem. 2007;39(8):1968-77. https://doi.org/10.1016/j.soilbio.2007.02.015

Poveda J, González-Andrés F. Bacillus as a source of phytohormones for use in agriculture. Appl Microbiol Biotechnol. 2021;105(23):8629-45. https://doi.org/10.1007/s00253-021-11492-8

Wani PA, Khan MS. Bacillus species enhance growth parameters of chickpea (Cicer arietinum L.) in chromium stressed soils. Food Chem Toxicol. 2010;48(11):3262-67. https://doi.org/10.1016/j.fct.2010.08.035

Downloads

Published

2023-12-13

How to Cite

1.
Bekkar AA, Zaim S. Phosphate solubilization and the enhancement of chickpea growth by new rhizospheric microorganisms Bacillus tequilensis and Trichoderma orientale. Arch Biol Sci [Internet]. 2023Dec.13 [cited 2024Dec.22];75(4):419-2. Available from: https://serbiosoc.org.rs/arch/index.php/abs/article/view/9027

Issue

Section

Articles