Journal of Microbiology and Biotechnology

The Korean Society for Microbiology and Biotechnology (한국미생물·생명공학회)
권호 표지
DOI QR코드

DOI QR Code

Evaluation of Bacillus velezensis for Biological Control of Rhizoctonia solani in Bean by Alginate/Gelatin Encapsulation Supplemented with Nanoparticles

  • Moradi-Pour, Mojde (Department of Plant Protection, Faculty of Agriculture, Vali-e-Asr University of Rafsanjan) ;
  • Saberi-Riseh, Roohallah (Department of Plant Protection, Faculty of Agriculture, Vali-e-Asr University of Rafsanjan) ;
  • Esmaeilzadeh-Salestani, Keyvan (Chair of Crop Science and Plant Biology, Institute of Agriculture and Environmental Sciences, Estonian University of Life Sciences) ;
  • Mohammadinejad, Reza (Research Center of Tropical and Infectious Diseases, Kerman University of Medical Sciences) ;
  • Loit, Evelin (Chair of Crop Science and Plant Biology, Institute of Agriculture and Environmental Sciences, Estonian University of Life Sciences)
  • Received : 2021.05.03
  • Accepted : 2021.08.10
  • Published : 2021.10.28
Download PDF
⟨ Previous Next ⟩

Abstract

Plant growth promoting rhizobacteria (PGPR) are a group of bacteria that can increase plant growth; but due to unfavorable environmental conditions, PGPR are biologically unstable and their survival rates in soil are limited. Therefore, the suitable application of PGPR as a plant growth stimulation is one of the significant challenges in agriculture. This study presents an intelligent formulation based on Bacillus velezensis VRU1 encapsulation enriched with nanoparticles that was able to control Rhizoctonia solani on the bean. The spherical structure of the capsule was observed based on the Scanning Electron Microscope image. Results indicated that with increasing gelatin concentration, the swelling ratio and moisture content were increased; and since the highest encapsulation efficiency and bacterial release were observed at a gelatin concentration of 1.5%, this concentration was considered in mixture with alginate for encapsulation. The application of this formulation which is based on encapsulation and nanotechnology appears to be a promising technique to deliver PGPR in soil and is more effective for plants.

Keywords

Acknowledgement

The authors acknowledge Vali-e-Asr University of Rafsanjan for providing the research materials and funds. Authors are grateful for the financial support obtained from the Estonian Ministry of Rural Affairs within the BioFoodOnMars project supported by the EU-FACCE-SURPLUS and FACCE-JPI.

References

  1. Salalha W, Kuhn J, Dror Y, Zussman E. 2006. Encapsulation of bacteria and viruses in electrospun nanofibers. Nanotechnology 17: 4675-4681. https://doi.org/10.1088/0957-4484/17/18/025
  2. Ab Rahmana SFS, Singha E, Pieterseb CMJ, Schenk PM. 2018. Emerging microbial biocontrol strategies for plant pathogens. Plant Sci. J. 267: 102-111. https://doi.org/10.1016/j.plantsci.2017.11.012
  3. Ben Khedher S, Mejdoub-Trabelsi B, Tounsi S. 2020. Biological potential of Bacillus subtilis V26 for the control of Fusarium wilt and tuber dry rot on potato caused by Fusarium species and the promotion of plant growth. Biol. Control 152: 104444. https://doi.org/10.1016/j.biocontrol.2020.104444
  4. Cray JA, Connor MC, Stevenson A, Jonathan DR, Houghton Drauzio EN, Rangel Louise R, et al. 2016. Biocontrol agents promote growth of potato pathogens, depending on environmental conditions. Microb. Biotechnol. 9: 330-354. https://doi.org/10.1111/1751-7915.12349
  5. Nakkeeran S, Dilantha Fernando WG, Siddiqui ZA. 2005. Plant growth promoting rhizobacteria formulation and its scope in commercialization for the management of pest and disease. ZA, Siddiqui (Ed.), pp. 257-296. PGPR: Biocontrol and Biofertilization. Springer.
  6. Locatelli GO, dos Santos GF, Botelho PS, Finkler CLL, Bueno LA. 2018. Development of Trichoderma sp. formulations in encapsulated granules (CG) and evaluation of conidia shelf-life. Biol. Control. 117: 21-29. https://doi.org/10.1016/j.biocontrol.2017.08.020
  7. Vejan P, Khadiran T, Abdullah R, Ismail S, Dadrasnia A. 2019. Encapsulation of plant growth promoting Rhizobacteria-prospects and potential in agricultural sector: a review. J. Plant Nutr. 42: 2600-2623. https://doi.org/10.1080/01904167.2019.1659330
  8. John RP, Tyagi RD, Brar SK, Surampalli RY, Prevost D. 2011. Bio-encapsulation of microbial cells for targeted agricultural delivery. Crit. Rev. Biotechnol. 31: 211-226. https://doi.org/10.3109/07388551.2010.513327
  9. Vemmer M, Patel AV. 2013. Review of encapsulation methods suitable for microbial biological control agents. Biol. Control. 67: 380-389. https://doi.org/10.1016/j.biocontrol.2013.09.003
  10. Gagne-Bourque F, Xu M, Dumont MJ, Jabaji S. 2015. Pea protein alginate encapsulated Bacillus subtilis B26, a plant biostimulant, provides controlled release and increased storage survival. J. Fertil. Pestic. 6: 157.
  11. Yao-jing W, Ming-da L, Dong L. 2009. Effects of silicon enrichment on photosynthetic characteristics and yield of Strawberry. Chinese Acad. Agric. Sci. 12: 92-93.
  12. Haghighi M, da Silva JAT. 2014. The effect of carbon nanotubes on the seed germination and seedling growth of four vegetable species. J. Crop Sci. Biotechnol. 17: 201-208. https://doi.org/10.1007/s12892-014-0057-6
  13. Khodakovskaya M, Dervishi E, Mahmood M, Xu Y, Li Z, Watanabe F, et al. 2009. Carbon nanotubes are able to penetrate plant seed coat and dramatically affect seed germination and plant growth. ACS Nano 3: 3221-3227. https://doi.org/10.1021/nn900887m
  14. Saberi-Rise R, Moradi-Pour, M. 2020. The effect of Bacillus subtilis Vru1 encapsulated in alginate-bentonite coating enriched with titanium nanoparticles against Rhizoctonia solani on bean. Int. J. Biol. Macromol. 152: 1089-1097. https://doi.org/10.1016/j.ijbiomac.2019.10.197
  15. Keel C, Weller DM, Natsch A, Defago G, Cook RJ, Thomashow LS. 1996. Conservation of the 2,4-diacetylphloroglucinol biosynthesis locus among fluorescent Pseudomonas isolates from diverse geographic locations. Appl. Environ. Microbiol. 62: 552-563. https://doi.org/10.1128/aem.62.2.552-563.1996
  16. Patten CL, Glick BR. 1996. Bacterial biosynthesis of indole-3-acetic acid. Can. J. Microbiol. 42: 207-220. https://doi.org/10.1139/m96-032
  17. Arora NK, Verma M. 2017. Modified microplate method for rapid and efficient estimation of siderophore produced by bacteria. 3Biotech 7: 381.
  18. Son HJ, Park GT, Cha MS, Heo MS. 2006. Solubilization of insoluble inorganic phosphates by a novel salt- and pH-tolerant Pantoea agglomerans R-42 isolated from soybean rhizosphere. Bioresour. Technol. 97: 204-210. https://doi.org/10.1016/j.biortech.2005.02.021
  19. Berg G, Krechel A, Ditz M, Richard A, Ulrich SA, Hallmann J. 2005. Endophytic and ectophytic potato-associated bacterial communities differ in structure and antagonistic function against plant pathogenic fungi. FEMS Microbiol. Ecol. 51: 215-229. https://doi.org/10.1016/j.femsec.2004.08.006
  20. Toharisman A, Suhartono MT, Spindler-Barth M, Hwang JK, Pyun YR. 2005. Purification and characterization of a thermostable chitinase from Bacillus licheniformis Mb-2. World J. Microbiol. Biotechnol. 21: 733-738. https://doi.org/10.1007/s11274-004-4797-1
  21. Rajeshkumar S, Malarkodi C. 2014. In vitro antibacterial activity and mechanism of silver nanoparticles against food borne pathogens. Bioinorganic Chemistry and Applications. 10.
  22. Tu L, He Y, Yang H, Wu Z, Yi L. 2015. Preparation and characterization of alginate-gelatin microencapsulated Bacillus subtilis SL-13 by emulsification/internal gelation. J. Biomater. Sci. Polym. Ed. 26: 735-749. https://doi.org/10.1080/09205063.2015.1056075
  23. Wu Z, Guo L, Qin S, Li C. 2012. Encapsulation of R. planticola Rs-2 from alginate-starch bentonite and its controlled release and swelling behavior under simulated soil conditions. J. Ind. Microbiol. Biotechnol. 39: 317-327. https://doi.org/10.1007/s10295-011-1028-2
  24. Szybalski W, Bryson V. 1952. Genetic studies on microbial cross resistance to toxic agents i.: cross resistance of Escherichia coli to fifteen antibiotics1, 2. J. Bacteriol. 64: 489-499. https://doi.org/10.1128/jb.64.4.489-499.1952
  25. Nelson B, Helms T, Christiianson T, Kural I. 1996. Characterization and pathogenicity of Rhizoctonia from soybean. Plant Dis. 80: 74-80. https://doi.org/10.1094/PD-80-0074
  26. Ben Khedher S, Kilani-Feki O, Dammakn M, Jabnoun-Khiareddine H, Daami- Remadi M, Tounsi S. 2015. Efficacy of Bacillus subtilis V26 as a biological control agent against Rhizoctonia solani on potato. C R Biol. 338: 784-792. https://doi.org/10.1016/j.crvi.2015.09.005
  27. Veliz EA, Martinez-Hidalgo P, Hirsch AM. 2017. Chitinase producing bacteria and their role in biocontrol. AIMS Microbiol. 3: 689-705. https://doi.org/10.3934/microbiol.2017.3.689
  28. Venturi V, Keel C. 2016. Signaling in the rhizosphere. Trends Plant Sci. 21: 187-198. https://doi.org/10.1016/j.tplants.2016.01.005
  29. Gowtham HG, Duraivadivel P, Hariprasad P, Niranjana SR. 2017. A novel split-pot bioassay to screen indole acetic acid producing rhizobacteria for the improvement of plant growth in tomato [Solanum lycopersicum L.]. Sci Hortic. 224: 351-357. https://doi.org/10.1016/j.scienta.2017.06.017
  30. Bari LM, Rakan AH, Faeza NT. 2019. Biological control of Fusarium wilt in tomato by entophytic rhizobacteria. Energy Procedia 157: 171-179. https://doi.org/10.1016/j.egypro.2018.11.178
  31. Shi F, Yin Z, Jiang H, Fan B. 2014. Screening, identification of P-dissolving fungus P83 strain and its effects on phosphate solubilization and plant growth promotion. Acta Microbiol. Sin. 54: 1333-1343.
  32. Sivasakthi S, Kanchana D, Usharani G, Saranraj P. 2013. Production of plant growth promoting substance by Pseudomonas fluorescens and Bacillus subtilis isolates from paddy rhizosphere soil of cuddalore district, Tamil Nadu, India. Int. J. Microbiol. Res. 4: 227-233. https://doi.org/10.9735/0975-5276.4.5.227-230
  33. Novo LA, Castro PM, Alvarenga P, da Silva EF. 2018. Plant growth-promoting rhizobacteria-assisted phytoremediation of mine soils, In Prasad MNV, de Campos Favas PJ, Maiti SK (Eds.), pp. 281-295. Bio-geotechnologies for mine site rehabilitation. Elsevier Inc., Amsterdam.
  34. Moradi Pour M, Saberi-Riseh R, Mohammadinejad R, Hosseini A. 2019. Investigating the formulation of alginate- gelatin encapsulated Pseudomonas fluorescens (VUPF5 and T17-4 strains) for controlling Fusarium solani on potato. Int. J. Biol. Macromol. 133: 603-613. https://doi.org/10.1016/j.ijbiomac.2019.04.071
  35. Thu HE, Ng SF. 2013. Gelatine enhances drug dispersion in alginate bilayer film via the formation of crystalline microaggregates. Int. J. Pharm. 454: 99-106. https://doi.org/10.1016/j.ijpharm.2013.06.082
  36. Phadke KV, Manjeshwar LS, Aminabhavi TM. 2014. Biodegradable polymeric microspheres of gelatin and carboxymethyl guar gum for controlled release of theophylline. Polym. Bull. 71: 1625-1643. https://doi.org/10.1007/s00289-014-1145-y
  37. Nallathambi G, Ramachandran T, Rajendran V, Palanivelu R. 2011. Effect of silica nanoparticles and BTCA on physical properties of cotton fabrics. Mater. Res. 14: 552-559. https://doi.org/10.1590/S1516-14392011005000086
  38. Chen ML, Oh WC. 2011. Synthesis and highly visible-induced photocatalytic activity of CNT-CdSe composite for methylene blue solution. Nanoscale Res. Lett. 6: 398. https://doi.org/10.1186/1556-276X-6-398
  39. Van Elsas J, Trevors J, Jain D, Wolters A, Heijnen C, Van L. 1992. Survival of, and root colonization by, alginate-encapsulated Pseudomonas fluorescens cells following introduction into the soil. Biol. Fertil. Soils. 14: 14-22. https://doi.org/10.1007/BF00336297
  40. Bharti N, Sharma SK, Saini S, Verma A, Nimonkar Y, Prakash O. 2017. Microbial plant probiotics: problems in application and formulation, In Kumar V, Kumar M, Sharma S, Prasad R (Eds.), pp. 317-335. Probiotics and Plant Health. Springer, Singapore.
  41. Tabassum B, Khan A, Tariq M, Ramzan M, Khan MSI, Shahid N, et al. 2017. Bottlenecks in commercialisation and future prospects of PGPR. Appl. Soil Ecol. 121: 102-117. https://doi.org/10.1016/j.apsoil.2017.09.030
  42. Lobo CB, Ju'arez Tomas MS, Viruel E, Ferrero MA, Lucca ME. 2018. Development of low-cost formulations of plant growth-promoting bacteria to be used as inoculants in beneficial agricultural technologies. Microbiol. Res. 219: 12-25. https://doi.org/10.1016/j.micres.2018.10.012
  43. Saberi-riseh R, Moradi-Pour M. 2020. The effect of Bacillus subtilis Vru1 encapsulated in alginate - bentonite coating enriched with titanium nanoparticles against Rhizoctonia solani on bean. Int. J. Biol. Macromol. 152: 1089-1097. https://doi.org/10.1016/j.ijbiomac.2019.10.197
  44. Monica RC, Cremonini R. 2009. Nanoparticles and higher plants. Caryologia. 62: 161-165. https://doi.org/10.1080/00087114.2004.10589681
  45. Torney F, Trewyn BG, Lin VSY, Wang K. 2007. Mesoporous silica nanoparticles deliver DNA and chemicals into plants. Nat. Nanotechnol. 2: 295-300. https://doi.org/10.1038/nnano.2007.108
  46. Bao-shan L, shao-qi D, Chun-hui L, Li-jun F, Shu-chun Q, Min Y. 2004. Effect of TMS (nanostructured silicon dioxide) on growth of Changbai Larch seedlings. J. For. Res. 15: 138-140. https://doi.org/10.1007/BF02856749
  47. Manzer H, Siddiqui M, Al-Whaibi H, Firoz M, Al-Khaishany MY. 2015. Role of nanoparticles in plants. Nanotechnol. Plant Sci. 2015: 19-35.
  48. Moradi Pour M, Saberi-Riseh R, Mohammadinejad R, Hosseini A. 2019. Nano-encapsulation of plant growth-promoting rhizobacteria and their metabolites using alginate-silica nanoparticles and carbon nanotube improves UCB11 pistachio micropropagation. J. Microbiol. Biotechnol. 29: 1096-1103. https://doi.org/10.4014/jmb.1903.03022
  49. Nair R, Varghese SH, Nair BG, Maekawa T, Yoshida Y, Kumar DS. 2010. Nanoparticulate material delivery to plants. Plant Sci. J. 179: 154-163. https://doi.org/10.1016/j.plantsci.2010.04.012
  50. Morla S, Ramachandra Rao CSV, Chakrapani R. 2011. Factors affecting seed germination and seedling growth of tomato plants cultured in vitro conditions. ACS Chem. Bio. Physiol. 1: 328-334.
  51. Tripathi S, Sarkar S. 2014. Influence of water-soluble carbon dots on the growth of wheat plant. Appl. Nanosci. 5: 609-616. https://doi.org/10.1007/s13204-014-0355-9
  52. Begum P, Fugetsu B. 2012. Phytotoxicity of multi-walled carbon nanotubes on red spinach (Amaranthus tricolor L) and the role of ascorbic acid as an antioxidant. J. Hazard. Mater. 243: 212-222. https://doi.org/10.1016/j.jhazmat.2012.10.025
  53. Kermani SA, Hokmabadi H. Jahromi MG. 2017. The evaluation of the effect of multiwall carbon nano tube (MWCNT) on in vitro proliferation and shoot tip necrosis of pistachio rootstock UCB-1 (Pistacia integrima× P. atlantica). J. Nuts 8: 49-59.
  54. Tiwari DK, Dasgupta-Schubert N, Villasenor-Cendejas LM, Villegas J, Carreto-Montoya L, Borjas-Garcia SE. 2014. Interfacing carbon nanotubes (CNT) with plants: enhancement of growth, water and ionic nutrient uptake in maize (Zea Mays) and implications for nano agriculture. Appl. Nanosci. 4: 577-591. https://doi.org/10.1007/s13204-013-0236-7