Comparative Assessment of Gamma-Polyglutamic Acid and Bacillus subtilis cells as Biostimulants to Improve Rice Growth and Soil Quality

• Autorzy: Ngearnpat Neti , Chunhachart Orawan , Kotabin Nuchnapa , Issakul Kritchaya

Identyfikatory

DOI

10.12911/22998993/172054

• Języki publikacji: EN

Abstrakty

EN

Chemical fertilizers have been widely used to improve rice production; however, their excessive use can have harmful environmental effects. Therefore, biostimulants are a sustainable option to promote rice yield and improve soil quality. This research focusses on the use of gamma-polyglutamic acid (γ-PGA) and Bacillus subtilis cells as biostimulants to improve rice growth and soil quality. The sand culture technique was performed to determine germination and growth of rice seedlings, and greenhouse experiments were conducted to evaluate the performance of rice yields. The soil quality was investigated by measuring physical and chemical characteristics. The results demonstrated that γ-PGA and B. subtilis cells were efficient biostimulants for germination by significantly increasing the seedling vigor index. γ-PGA considerably improved the growth parameters of 21-day-old rice seedlings by significantly increasing dry weight, total sugar, total free amino acids and total chlorophyll content compared to the control. In greenhouse experiments, γ-PGA had a positive influence on all physical characteristics and rice grain yield indicators compared to B. subtilis cells and controls. Furthermore, γ-PGA and B. subtilis cells had a stronger impact than controls on improving soil quality, and γ-PGA had a notable effect on soil physical properties rather than on their chemical properties. Based on these findings, γ-PGA outperformed B. subtilis cells as a natural biostimulant to increase rice productivity and improve the quality of paddy soil.

Słowa kluczowe

EN

microbial products; paddy soil; plant growth regulator; rice productivity; soil quality improvement; soil amendment

• Wydawca: Polskie Towarzystwo Inżynierii Ekologicznej ; Lublin University of Technology
• Czasopismo: Journal of Ecological Engineering
• Rocznik: 2023
• Tom: Vol. 24, nr 12
• Strony: 46--59
• Opis fizyczny: Bibliogr. 50 poz., rys., tab.

Twórcy

autor

Ngearnpat Neti

• Department of Microbiology, School of Medical Sciences, University of Phayao, 19 M. 2, T. MaeKa, A. Muang, Phayao 56000, Thailand

autor

Chunhachart Orawan

• Division of Microbiology, Department of Science and Bioinnovation, Faculty of Liberal Arts and Science, Kasetsart University Kamphaeng Saen Campus, 1 M.6, T. Kamphaeng Saen, A. Kamphaeng Saen, Nakhon Pathom, 73140, Thailand
• Bioproducts Science Program, Department of Science and Bioinnovation, Faculty of Liberal Arts and Science, Kasetsart University Kamphaeng Saen Campus, 1 M.6, T. Kamphaeng Saen, A. Kamphaeng Saen, Nakhorn Pathom, 73140, Thailand

autor

Kotabin Nuchnapa

• Bioproducts Science Program, Department of Science and Bioinnovation, Faculty of Liberal Arts and Science, Kasetsart University Kamphaeng Saen Campus, 1 M.6, T. Kamphaeng Saen, A. Kamphaeng Saen, Nakhorn Pathom, 73140, Thailand

autor

Issakul Kritchaya

• School of Energy and Environment, University of Phayao, 19 M. 2, T. MaeKa, A. Muang, Phayao 56000, Thailand

• https://orcid.org/0000-0002-8101-2147

Bibliografia

• 1. Adesemoye A.O., Kloepper J.W. 2009. Plant-microbes interactions in enhanced fertilizer-use efficiency. Applied Microbiology and Biotechnology, 85(1), 1–12. https://doi.org/ 10.1007/s00253–009–2196–0
• 2. Allard M.R., Tessier L., Lecuyer F., Lakshmanan V., Lucier J.F., Garneau D., Caudwell L., Vlamakis H., Bais H.P., Beauregard P.B. 2016. Bacillus subtilis early colonization of Arabidopsis thaliana roots involves multiple chemotaxis receptors. MBio, 7(6). https:// doi.org/10.1128/mBio.01664–16
• 3. Anantharaman S., Padmarajaiah N., Al-Tayar N.G.S., Shrestha A.K. 2017. Ninhydrin-sodium molybdate chromogenic analytical probe for the assay of amino acids and proteins. Spectrochimica Acta Part A: Molecular and Biomolecular Spectroscopy, 173, 897–903. https://doi.org/10.1016/j.saa.2016.10.040
• 4. Anisuzzaman M., Rafii M.Y., Jaafar N.M., Izan R.S., Ikbal M.F., Haque M.A. 2021. Effect of organic and inorganic fertilizer on the growth and yield components of traditional and improved rice (Oryza sativa L.) genotypes in Malaysia. Agronomy, 11(9), 1830. https://doi.org/10.3390/agronomy11091830
• 5. Atman A., Bakrie B., Indrasti R. 2018. Effect of cow manure dosages as organic fertilizer on the productivity of organic rice in West Sumatra, Indonesia. International Journal of Environment, Agriculture and Biotechnology, 3, 506–511. https://doi.org/10.22161/ijeab/3.2.25
• 6. Aziz S.A., Melati M., Sudarsono W.A. 2014. Growth and yield of organic rice with cow manure application in the first cropping season. Agrivita, 36(1), 19–25. https:// doi.org/10.17503/Agrivita-2014–36–1-p019–025
• 7. Bacilio J.M., Aguilar-Flores S., Ventura-Zapata E., Perez-Campos E., Bouquelet S., Zenteno E. 2003. Chemical characterization of root exudates from rice (Oryza sativa) and their effects on the chemotactic response of endophytic bacteria. Plant and Soil, 249 (2), 271–277. https:// doi.org/10.1023/A:1022888900465
• 8. Backer R., Rokem J.S., Ilangumaran G., Lamont J., Praslickova D., Ricci E., Subramanian S., Smith D.L. 2018. Plant growth-promoting rhizobacteria: Context, mechanisms of action, and roadmap to commercialization of biostimulants for sustainable agriculture. Frontiers of Plant Science, 9. https://doi.org/10.3389/fpls.2018.01473
• 9. Bai N., Zhang H., Li S., Zheng X., Zhang J., Sun L., Lv W. 2020. Effects of application rates of poly-γ-glutamic acid on vegetable growth and soil bacterial community structure. Applied Soil Ecology, 147, 103405. https://doi.org/10.1016/j.apsoil.2019.103405
• 10. Blake G.R., Hartge K.H. 1986. Bulk density. Proceedings of the Klute A. (Eds.), Methods of soil analysis, Part 1–Physical and mineralogical methods, 2nd Ed, Agronomy Monograph 9, American Society of Agronomy–Soil Science Society of America, Madison, Wisconsin, USA, pp. 363–382.
• 11. Carter M.R., Ball B. 1993. Soil porosity. Proceedings of the Carter MR (eds.), Soil Sampling and methods of analysis, Canadian society of soil science, Lewis Publishers, CRC Press, Boca Raton, Florida, USA, pp. 581–588.
• 12. Chen L., Fei L., Mohamed K.S., Liu L., Wang Z., Zhong Y., Dai Z. 2018. The effects of poly (γ-glutamic acid) on spinach productivity and nitrogen use efficiency in North-West China. Plant, Soil and Environment, 64(11), 517–512. https://doi.org/10.17221/371/2018PSE
• 13. Chowdhury S.P., Hartmann A., Gao X., Borriss R. 2015. Biocontrol mechanism by root-associated Bacillus amyloliquefaciens FZB42-a review. Frontiers in Microbiology, 6:780. https://doi.org/10.3389/fmicb.2015.00780
• 14. Chunhachart O., Kotabin N., Yadee N., Tahara Y., Issakul K. 2014. Effect of lead and γ-polyglutamic acid produced from Bacillus subtilis on growth of Brassica chinensis L. APCBEE Procedia, 10, 269–274. https://doi.org/10.1016/j.apcbee.2014.10.051
• 15. Ding Y., Wang J., Liu Y., Chen S. 2005. Isolation and identification of nitrogen fixing bacilli from plant rhizospheres in Beijing region. Journal of Applied Microbiology, 99, 1271–1281. https://doi.org/10.1111/j.1365–2672.2005.02738.x
• 16. Food and Agriculture Organization of the United Nations. 2017. World fertilizer trends and outlook to 2020. Rome, Italy. Available from: https://www.fao.org/3/i6895e/i6895e.pdf.
• 17. Forde B.G. 2014. Glutamate signaling in roots. Journal of Experimental Botany, 65(3), 779–787. https://doi.org/10.1093/jxb/ert335
• 18. Hayat R., Ali S., Amara U., Khalid R., Ahmed I. 2010. Soil beneficial bacteria and their role in plant growth promotion: a review. Annals of Microbiology. 60: 579–598. https://doi.org/10.1007/s13213–010–0117–1
• 19. Iqbal A., He L., Ali I., Ullah S., Khan A., Khan Az., Akhtar K.,Wei S., Zhao Q., Zhang J., Jiang L. 2020. Manure combined with chemical fertilizer increases rice productivity by improving soil health, post-anthesis biomass yield, and nitrogen metabolism. PloS One, 15(10), e0238934. https://doi.org/10.1371/journal.pone.0238934
• 20. Joshi R., Singh J., Vig A.P. 2015. Vermicompost as an effective organic fertilizer and biocontrol agent: effect on growth, yield and quality of plants. Reviews in Environmental Science and Bio/Technology, 14(1), 137–159. https://doi.org/10.1007/s11157–014–9347–1
• 21. Kang S.M., Radhakrishnan R., You Y.H., Joo G.J., Lee I.J., Lee K.E., Kim J.H. 2014. Phosphate solubilizing Bacillus megaterium mj1212 regulates endogenous plant carbohydrates and amino acids contents to promote mustard plant growth. Indian Journal of Microbiology, 54, 427–433. https://doi.org/10.1007/s12088–014-0476–6
• 22. Kashyap B.K., Solanki M.K., Pandey A.K., Prabha S., Kumar P., Kumari B. 2019. Bacillus as plant growth promoting rhizobacteria (PGPR): A promising green agriculture technology. In: Ansari RA, Mahmood I. (Eds.). Plant Health under Biotic Stress, Vol. 2: Microbial Interactions, Springer, Singapore, 219–236. https://doi.org/10.1007/978–981–13–6040–4_11
• 23. Kotabin N., Issakul K., Pawelzik E., Tahara Y., Chunhachart O. 2017. Alleviation of cadmium toxicity in rice by γ-polyglutamic acid produced by Bacillus subtilis. EnvironmentAsia, 10(1), 63–72. https://doi.org/10.14456/ea.2017.8
• 24. Kurzyna-Szklarek M., Cybulska J., Zdunek A. 2022. Analysis of the chemical composition of natural carbohydrates – An overview of methods. Food Chemistry, 394, 133466. https://doi.org/https://doi.org/10.1016/j.foodchem.2022.133466
• 25. Li M., Fu Q., Singh V.P., Liu D., Li T., Li J. 2020. Sustainable management of land, water, and fertilizer for rice production considering footprint family assessment in a random environment. Journal of Cleaner Production, 258, 120785. https://doi.org/10.1016/j.jclepro.2020.120785
• 26. Lou X., Zhao J., Lou X., Xia X., Feng Y., Li, H. 2022. The biodegradation of soil organic matter in soil-dwelling humivorous fauna [Mini Review]. Frontiers in Bioengineering and Biotechnology, 9. https://doi.org/10.3389/fbioe.2021.808075
• 27. Lynch J.P., Brown K.M. 2012. New roots for agriculture: exploiting the root phenome. Philosophical Transactions of the Royal Society B: Biological Sciences, 367(1595), 1598–1604. https://doi.org/10.1098/rstb.2011.0243
• 28. Nelson D.W., Sommers L.E. 1996. Total Carbon, Organic Carbon, and Organic Matter. In: Methods of Soil Analysis. Sparks D.L., Page A.L., Helmke P.A., Loeppert R.H., Soltanpour P.N., Tabatabai M.A., Johnston C.T., Sumner M.E. (Eds). https://doi.org/10.2136/sssabookser5.3.c34
• 29. Othman N.M.I., Othman R., Saud H.M., Wahab P.E.M. 2017. Effects of root colonization by zinc-solubilizing bacteria on rice plant (Oryza sativa MR219) growth. Agriculture and Natural Resources, 51(6), 532–537. https://doi.org/10.1016/j.anres.2018.05.004
• 30. Pereira A.E.S., Sandoval-Herrera I.E., Zavala-Betancourt S.A., Oliveira H.C., Ledezma-Pérez A.S., Romero J., Fraceto L.F. 2017. γ-Polyglutamic acid/chitosan nanoparticles for the plant growth regulator gibberellic acid: Characterization and evaluation of biological activity. Carbohydrate Polymers, 157, 1862–1873. https://doi.org/10.1016/j.carbpol.2016.11.073
• 31. Poveda J., and González-Andrés F. 2021. Bacillus as a source of phytohormones for use in agriculture. Applied Microbiology and Biotechnology, 105(23), 8629–8645. https://doi.org/10.1007/s00253–021–11492–8
• 32. Rahman S., Barmon B.K. 2019. Greening modern rice farming using vermicompost and its impact on productivity and efficiency: An empirical analysis from Bangladesh. Agriculture 9(11), 239. https://doi.org/10.3390/agriculture9110239
• 33. Saeid A., Prochownik E., Dobrowolska-Iwanek J. 2018. Phosphorus solubilization by Bacillus species. Molecules, 23(11), 2897. https://doi.org/10.3390/molecules23112897
• 34. Shang L., Wan L., Zhou X., Li S., Li X. 2020. Effects of organic fertilizer on soil nutrient status, enzyme activity, and bacterial community diversity in Leymus chinensis steppe in Inner Mongolia, China. PloS One, 15(10), e0240559. https://doi.org/10.1371/journal.pone.0240559
• 35. Su Y., Liu C., Fang H., Zhang D. 2020. Bacillus subtilis: a universal cell factory for industry, agriculture, biomaterials and medicine. Microbial Cell Factories, 19(1), 173. https://doi.org/10.1186/s12934–020–01436–8
• 36. Suebpongsang P., Ekasingh B., Cramb R. 2020. Commercialization of rice farming in Northeast Thailand. In: Cramb R. (Ed.), White Gold: The commercialisation of rice farming in the lower Mekong basin. Springer, Singapore, 39–68. https://doi.org/10.1007/978–981–15–0998–8_2
• 37. Sun Y.L., Hong S.K. 2010. Effects of plant growth regulators and L-glutamic acid on shoot organogenesis in the halophyte Leymus chinensis (Trin.). Plant Cell, Tissue and Organ Culture, 100(3), 317–328. https://doi: 10.1007/s11240–009–9653–4
• 38. Van Reeuwijk L. 2002. Procedures for soil analysis. International soil reference and information center (ISRIC), FAO, Wageningen, The Netherlands. Available from https://www.isric.org/sites/default/files/IS-RIC_TechPap09.pdf. Accessed Sep. 11, 2022.
• 39. Vibhuti V., Shahi C., Bargali K., Bargali S.S. 2015. Seed germination and seedling growth parameters of rice (Oryza sativa) varieties as affected by salt and water stress. The Indian Journal of Agricultural Sciences, 85, 102–108. Available from: https://epubs.icar.org.in/index.php/IJAgS/article/view/46046/19956
• 40. Walch-Liu P., Liu L.H., Remans T., Tester M., Forde B.G. 2006. Evidence that L -glutamate can act as an exogenous signal to modulate root growth and branching in Arabidopsis thaliana. Plant and Cell Physiology, 47(8), 1045–1057. https://doi.org/10.1093/pcp/pcj075
• 41. Wang J., Li R., Zhang H., Wei G., Li Z. 2020. Beneficial bacteria activate nutrients and promote wheat growth under conditions of reduced fertilizer application. BMC Microbiology, 20(1), 38. https://doi.org/10.1186/s12866–020–1708-z
• 42. Wang L., Chen S., Yu B. 2022. Poly-γ-glutamic acid: Recent achievements, diverse applications and future perspectives. Trends in Food Science & Technology, 119, 1–12. https://doi.org/10.1016/j.tifs.2021.11.009
• 43. Wintermans J.F.G.M., De Mots A. 1965. Spectrophotometric characteristics of chlorophylls a and b and their phenophytins in ethanol. Biochimica et Biophysica Acta (BBA) – Biophysics including Photosynthesis,109(2), 448–453. https://doi.org/10.1016/0926–6585(65)90170–6
• 44. Xu Z., Lei P., Feng X., Li S., Xu H. 2016. Analysis of the metabolic pathways affected by poly (γ-glutamic acid) in Arabidopsis thaliana based on GeneChip microarray. Journal of Agricultural and Food Chemistry, 64, 6257–6266. https://doi.org/10.1021/acs.jafc.6b02163
• 45. Xu Z., Lei P., Feng X., Xu X., Liang J., Chi B., Xu H. 2014. Calcium involved in the poly(γ-glutamic acid)-mediated promotion of Chinese cabbage nitrogen metabolism. Plant Physiology and Biochemistry, 80, 144–152. https://doi.org/10.1016/j.plaphy.2014.03.036
• 46. Xu Z., Lei P., Feng X., Xu X., Xu H., Yang H., Tang W. 2013a. Effect of poly (γ-glutamic acid) on microbial community and nitrogen pools of soil. Acta Agriculturae Scandinavica – Section B Soil and Plant Science, 63(8), 657–668. https:// doi.org/10.1080/09064710.2013.849752
• 47. Xu Z., Wan C., Xu X., Feng X., Xu H. 2013b. Effect of poly (γ-glutamic acid) on wheat productivity, nitrogen use efficiency and soil microbes. Journal of Plant Nutrition and Soil Science, 13, 744–755. https://doi.org/10.4067/S0718–95162013005000059.
• 48. Yang Y.M., Pollard A., Höfler C., Poschet G., Wirtz M., Hell R., Sourjik V. 2015. Relation between chemotaxis and consumption of amino acids in bacteria. Molecular Microbiology, 96 (6), 1272–1282. https://doi.org/10.1111/mmi.13006
• 49. Yu Y., Yan F., Chen Y., Jin C., Guo J.H., Chai Y. 2016. Poly-γ-glutamic acids contribute to biofilm formation and plant root colonization in selected environmental isolates of Bacillus subtilis. Frontiers in Microbiology, 7(1811). https://doi.org/10.3389/fmicb.2016.01811
• 50. Zhang L., Yang X., Gao D., Wang L., Li J., Wei Z., Shi Y. 2017. Effects of polyglutamic acid (γ-PGA) on plant growth and its distribution in a controlled plant-soil system. Scientific Reports, 7(1), 6090–6090. https://doi.org/10.1038/s41598–017–06248–2

Uwagi

Opracowanie rekordu ze środków MNiSW, umowa nr SONP/SP/546092/2022 w ramach programu "Społeczna odpowiedzialność nauki" - moduł: Popularyzacja nauki i promocja sportu (2024).