Journal of Microbiology and Biotechnology

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

DOI QR Code

Biological Inoculant of Salt-Tolerant Bacteria for Plant Growth Stimulation under Different Saline Soil Conditions

  • Wang, Ru (College of Environmental Science and Engineering, Qilu University of Technology (Shandong Academy of Sciences)) ;
  • Wang, Chen (College of Environmental Science and Engineering, Qilu University of Technology (Shandong Academy of Sciences)) ;
  • Feng, Qing (College of Environmental Science and Engineering, Qilu University of Technology (Shandong Academy of Sciences)) ;
  • Liou, Rey-May (Department of Research and Development Centre of Ecological Engineering and Technology, Chia Nan University of Pharmacy and Science) ;
  • Lin, Ying-Feng (Department of Research and Development Centre of Ecological Engineering and Technology, Chia Nan University of Pharmacy and Science)
  • Received : 2020.09.21
  • Accepted : 2020.12.22
  • Published : 2021.03.28
Download PDF
⟨ Previous Next ⟩

Abstract

Using salt-tolerant bacteria to protect plants from salt stress is a promising microbiological treatment strategy for saline-alkali soil improvement. Here, we conducted research on the growth-promoting effect of Brevibacterium frigoritolerans on wheat under salt stress, which has rarely been addressed before. The synergistic effect of B. frigoritolerans combined with representative salt-tolerant bacteria Bacillus velezensis and Bacillus thuringiensis to promote the development of wheat under salt stress was also further studied. Our approach involved two steps: investigation of the plant growth-promoting traits of each strain at six salt stress levels (0, 2, 4, 6, 8, and 10%); examination of the effects of the strains (single or in combination) inoculated on wheat in different salt stress conditions (0, 50, 100, 200, 300, and 400 mM). The experiment of plant growth-promoting traits indicated that among three strains, B. frigoritolerans had the most potential for promoting wheat parameters. In single-strain inoculation, B. frigoritolerans showed the best performance of plant growth promotion. Moreover, a pot experiment proved that the plant growth-promoting potential of co-inoculation with three strains on wheat is better than single-strain inoculation under salt stress condition. Up to now, this is the first report suggesting that B. frigoritolerans has the potential to promote wheat growth under salt stress, especially combined with B. velezensis and B. thuringiensis.

Keywords

References

  1. Raheem A, Ali B. 2015. Halotolerant rhizobacteria: Beneficial plant metabolites and growth enhancement of Triticum aestivum L. in salt amended soils. Arch Agron Soil Sci. 61: 1691-1705. https://doi.org/10.1080/03650340.2015.1036044
  2. Sharma A, Singh P, Kumar S, Kashyap PL, Srivastava AK, Chakdar H, et al. 2015. Deciphering diversity of salt-tolerant Bacilli from saline soils of Eastern Indo-gangetic plains of India. Geomicrobiol J. 32: 170-180. https://doi.org/10.1080/01490451.2014.938205
  3. Manninen M, Sandholm TM. 1994. Methods for the detection of Pseudomonas siderophores. J. Microbiol. Methods 19: 223-234. https://doi.org/10.1016/0167-7012(94)90073-6
  4. Masood S, Khan A, Sirajuddin, Zhao X, Javed MT, Khan KS, et al. 2016. Bacillus pumilus enhances tolerance in rice (Oryza sativa L.) to combined stresses of NaCl and high boron due to limited uptake of Na+. Environ. Exp. Bot. 124: 120-129. https://doi.org/10.1016/j.envexpbot.2015.12.011
  5. Nautiyal CS, Srivastava S, Chauhan PS, Seem K, Mishra A, Sopory SK. 2013. Plant growth-promoting bacteria Bacillus amyloliquefaciens NBRISN13 modulates gene expression profile of leaf and rhizosphere community in rice during salt stress. Plant Physiol. Biochem. 66: 1-9. https://doi.org/10.1016/j.plaphy.2013.01.020
  6. Vimal SR, Gupta J, Singh JS. 2018. Effect of salt tolerant Bacillus sp. and Pseudomonas sp. on wheat (Triticum aestivum L.) growth under soil salinity: A comparative study. Microbiol. Res. 9: 1-14.
  7. Jariyal M, Gupta VK, Mandal K, Jindal V. 2015. Brevibacterium frigoritolerans as a novel organism for the bioremediation of phorate. Bull. Environ. Contam. Toxicol. 95: 680-686. https://doi.org/10.1007/s00128-015-1617-2
  8. Tong X, Yuan L, Luo L, Yin X. 2014. Characterization of a selenium-tolerant rhizosphere strain from a novel Se-hyperaccumulating plant Cardamine hupingshanesis. Scientific WorldJournal. 2014: 108562.
  9. Kasai K, Mori N, Nakamura C. 1998. Changes in the respiratory pathways during germination and early seedling growth of common wheat under normal and NaCI-stressed conditions. Cereal Res. Commun. 26: 217-224. https://doi.org/10.1007/bf03543491
  10. Wang S, Feng Q, Zhou Y, Mao X, Chen Y, Xu H. 2017. Dynamic changes in water and salinity in saline-alkali soils after simulated irrigation and leaching. PLoS One. 12: e0187536. https://doi.org/10.1371/journal.pone.0187536
  11. Jha Y, Subramanian RB. 2013. Paddy plants inoculated with PGPR show better growth physiology and nutrient content under saline conditions. Chil J. Agr. Res. 73: 213-219. https://doi.org/10.4067/S0718-58392013000300002
  12. Meng Q, Jiang H, Hao J. 2016. Effects of Bacillus velezensis strain BAC03 in promoting plant growth. Biol. Control. 98: 18-26. https://doi.org/10.1016/j.biocontrol.2016.03.010
  13. Gopalakrishnan S, Humayun P, Kiran BK, Kannan IGK, Vidya MS, Deepthi K, et al. 2011. Evaluation of bacteria isolated from rice rhizosphere for biological control of charcoal rot of sorghum caused by Macrophomina phaseolina (Tassi) Goid. World J. Microbiol. Biotechnol. 27: 1313-1321. https://doi.org/10.1007/s11274-010-0579-0
  14. Meena, Tara N, Saharan BS. 2017. Plant growth promoting traits shown by bacteria Brevibacterium frigrotolerans SMA23 Isolated from Aloe vera rhizosphere. Agric. Sci. Digest. 37: 226-231.
  15. Zhang C, Li XL, Yin LF, Liu C, Zou HW, Wu ZY, et al. 2019. Analysis of the complete genome sequence of Brevibacterium frigoritolerans ZB201705 isolated from drought- and salt-stressed rhizosphere soil of maize. Ann. Microbiol. 69: 1489-1496. https://doi.org/10.1007/s13213-019-01532-0
  16. Feng Q, Song YC, Bae BU. 2016. Influence of applied voltage on the performance of bioelectrochemical anaerobic digestion of sewage sludge and planktonic microbial communities at ambient temperature. Bioresour. Technol. 220: 500-508. https://doi.org/10.1016/j.biortech.2016.08.085
  17. Yang J, Yang S. 2017. Comparative analysis of Corynebacterium glutamicum genomes: a new perspective for the industrial production of amino acids. BMC Genomics 18(Suppl 1): 940. https://doi.org/10.1186/s12864-016-3255-4
  18. Penrose DM, Glick BR. 2003. Methods for isolating and characterizing ACC deaminase-containing plant growth-promoting rhizobacteria. Physiol. Plant. 118: 10-15. https://doi.org/10.1034/j.1399-3054.2003.00086.x
  19. Gordon SA, Weber RP. 1951. Colorimetric estimation of indoleacetic acid. Plant Physiol. 26: 192-195. https://doi.org/10.1104/pp.26.1.192
  20. Prakash J, Arora NK. 2019. Phosphate-solubilizing Bacillus sp. enhances growth, phosphorus uptake and oil yield of Mentha arvensis L. 3 Biotech. 9: 126. https://doi.org/10.1007/s13205-019-1660-5
  21. Fiske CH, Subbarow Y. 1925. The colorimetric determination of phosphorus. J. Biol. Chem. 66: 375-400. https://doi.org/10.1016/S0021-9258(18)84756-1
  22. Greaves JE, Greaves JD. 1930. The microflora of leached alkali soil. Bot. Gaz. 90: 224-230. https://doi.org/10.1086/334096
  23. Mudhulkar R, Rajapitamahuni S, Srivastava S, Bharadwaj SVV, Boricha VP, Mishra S, et al. 2018. Identification of a new siderophore acinetoamonabactin produced by a salt-tolerant bacterium Acinetobacter soli. ChemistrySelect. 3: 8207-8211. https://doi.org/10.1002/slct.201801527
  24. Anderson JA, Peters DC. 1994. Ethylene production from wheat seedlings infested with biotypes of schizaphis graminum (Homoptera: aphididae). Environ. Entomol. 23: 992-998. https://doi.org/10.1093/ee/23.4.992
  25. Manivel G, Raj DML, Prathiviraj R, Senthilraja P. 2020. Distribution of phylogenetic proximity upon species-rich marine ascomycetes with reference to pichavaram mangrove soil sediment of southern India. Gene Rep. 21:100878. https://doi.org/10.1016/j.genrep.2020.100878
  26. Ye M, Tang X, Yang R, Zhang H, Li F, Tao F, et al. 2018. Characteristics and application of a novel species of Bacillus: Bacillus velezensis. ACS Chem. Biol. 13: 500-505. https://doi.org/10.1021/acschembio.7b00874
  27. Jariyal M, Gupta VK, Mandal K, Jindal V, Banta G, Singh B. 2014.Isolation and characterization of novel phorate-degrading bacterial species from agricultural soil. Environ. Sci. Pollut. Res. 21: 2214-2222. https://doi.org/10.1007/s11356-013-2155-2
  28. Yallapragada VVB, Gowda U, Wong D, O'Faolain L, Tangney M, Devarapu GCR. 2019. ODX: A fitness tracker-based device for continuous bacterial growth monitoring. Anal. Chem. 91: 12329-12335. https://doi.org/10.1021/acs.analchem.9b02628
  29. Biesta-Peters EG, Reij MW, Joosten H, Gorris LGM, Zwietering MH. 2010. Comparison of two optical-density-based methods and a plate count method for estimation of growth parameters of Bacillus cereus. Appl. Environ. Microbiol. 76: 1399-1405. https://doi.org/10.1128/AEM.02336-09
  30. Gonzalez-Perez CJ, Tanori-Cordova J, Aispuro-Hernandez E, Vargas-Arispuro I, Martinez-Tellez MA. 2019. Morphometric parameters of foodborne related-pathogens estimated by transmission electron microscopy and their relation to optical density and colony forming units. J. Microbiol. Methods 165: 105691. https://doi.org/10.1016/j.mimet.2019.105691
  31. Masmoudi F, Abdelmalek N, Tounsi S, Dunlap CA, Trigui M. 2019. Abiotic stress resistance, plant growth promotion and antifungal potential of halotolerant bacteria from a Tunisian solar saltern. Microbiol. Res. 229: 126331. https://doi.org/10.1016/j.micres.2019.126331
  32. Raza FA, Amin A, Faisal M. 2015. Desiccation-tolerant rhizobacteria from cholistan desert, Pakistan, and their impact on Zea mays L. Pol. J. Environ. Stud. 24: 1773-1781. https://doi.org/10.15244/pjoes/26386
  33. Tiryaki D, Aydin I, Atici O. 2019. Psychrotolerant bacteria isolated from the leaf apoplast of cold-adapted wild plants improve the cold resistance of bean (Phaseolus vulgaris L.) under low temperature. Cryobiology 86: 111-119. https://doi.org/10.1016/j.cryobiol.2018.11.001
  34. Mahajan S, Tuteja N. 2005. Cold, salinity and drought stresses: An overview. Arch. Biochem. Biophys. 444: 139-158. https://doi.org/10.1016/j.abb.2005.10.018
  35. Glick BR. 2003. Phytoremediation: synergistic use of plants and bacteria to clean up the environment. Biotechnol. Adv. 21: 383-393. https://doi.org/10.1016/S0734-9750(03)00055-7
  36. Qin Y, Druzhinina IS, Pan X, Yuan Z. 2016. Microbially mediated plant salt tolerance and microbiome-based solutions for saline agriculture. Biotechnol. Adv. 34: 1245-1259. https://doi.org/10.1016/j.biotechadv.2016.08.005
  37. Glick BR, Cheng Z, Czarny J, Duan J. 2007. Promotion of plant growth by ACC deaminase-producing soil bacteria. Eur. J. Plant Pathol. 119: 329-339. https://doi.org/10.1007/s10658-007-9162-4
  38. Glick BR, Penrose DM, Li J. 1998. A model for the lowering of plant ethylene concentrations by plant growth-promoting bacteria. J. Theor. Biol. 190: 63-68. https://doi.org/10.1006/jtbi.1997.0532
  39. Glick BR. 2012. Plant growth-promoting bacteria: mechanisms and applications. Scientifica (Cairo). 2012: 963401. https://doi.org/10.6064/2012/963401
  40. Kende H. 1993. Ethylene biosynthesis. Plant Mol.Biol. 44: 283-307.
  41. Marques APGC, Pires C, Moreira H, Antonio O.S.S. Rangel, Castro PML. 2010. Assessment of the plant growth promotion abilities of six bacterial isolates using Zea mays as indicator plant. Soil Biol. Biochem. 42: 1229-1235. https://doi.org/10.1016/j.soilbio.2010.04.014
  42. Xie H, Pasternak JJ, Glick BR. 1996. Isolation and characterization of mutants of the plant growth-promoting rhizobacterium Pseudomonas putida GR 12-2 that overproduce indoleacetic acid. Curr. Microbiol. 32: 67-71. https://doi.org/10.1007/s002849900012
  43. Malboobi MA, Behbahani M, Madani H, Owlia P, Deljou A, Yakhchali B, et al. 2009. Performance evaluation of potent phosphate solubilizing bacteria in potato rhizosphere. World J. Microbiol. Biotechnol. 25: 1479-1484. https://doi.org/10.1007/s11274-009-0038-y
  44. Wang T, Liu M, Li H. 2014. Inoculation of phosphate-solubilizing bacteria Bacillus thuringiensis B1 increases available phosphorus and growth of peanut in acidic soil. Soil Plant Sci. 64: 252-259.
  45. Delfim J, Schoebitz M, Paulino L, Hirzel J, Zagal E. 2018. Phosphorus availability in wheat, in volcanic soils inoculated with phosphate-solubilizing Bacillus thuringiensis. Sustainability. 10: 144. https://doi.org/10.3390/su10010144
  46. Zaidi A, Khan MS, Ahemad M, Oves M. 2009. Plant growth promotion by phosphate solubilizing bacteria. Acta Microbiol. Immunol. Hung. 56: 263-284. https://doi.org/10.1556/AMicr.56.2009.3.6
  47. Hongrittipun P, Youpensuk S, Rerkasem B. 2014. Screening of nitrogen fixing endophytic bacteria in Oryza sativa L. J. Agric. Sci. 6: 66-74.
  48. Duhan JS, Dudeja SS, Khurana AL. 1998. Siderophore production in relation to N2 fixation and iron uptake in Pigeon Pea-Rhizobium Symbiosis. Folia Microbiol. 43: 421-426. https://doi.org/10.1007/BF02818585
  49. Parray JA, Jan S, Kamili AN, Qadri RA, Egamberdieva D, Ahmad P. 2016. Current perspectives on plant growth-promoting rhizobacteria. J. Plant Growth Regul. 35: 877-902. https://doi.org/10.1007/s00344-016-9583-4
  50. Indiragandhi P, Anandham R, Madhaiyan M, Sa TM. 2008. Characterization of plant growth-promoting traits of bacteria isolated from larval guts of diamondback moth Plutella xylostella (lepidoptera: plutellidae). Curr. Microbiol. 56: 327-333. https://doi.org/10.1007/s00284-007-9086-4
  51. Sandy M, Butler A. 2009. Microbial iron acquisition: marine and terrestrial siderophores. Chem. Rev. 109: 4580-4595. https://doi.org/10.1021/cr9002787
  52. Ansari FA, Ahmad I, Pichtel J. 2019. Growth stimulation and alleviation of salinity stress to wheat by the biofilm forming Bacillus pumilus strain FAB10. Appl. Soil. Ecol. 143: 45-54. https://doi.org/10.1016/j.apsoil.2019.05.023
  53. Sindhu SS, Gupta SK, Dadarwal KR. 1999. Antagonistic effect of Pseudomonas spp. on pathogenic fungi and enhancement of growth of green gram (Vigna radiata). Biol. Fertil. Soils. 29: 62-68. https://doi.org/10.1007/s003740050525
  54. Gongora CE, Broadway RM. 2002. Plant growth and development influenced by transgenic insertion of bacterial chitinolytic enzymes. Mol. Breed. 9: 123-135. https://doi.org/10.1023/A:1026732124713
  55. Badri DV, Weir TL, van der Lelie D, Vivanco JM. 2009. Rhizosphere chemical dialogues: plant-microbe interactions. Curr. Opin. Biotechnol. 20: 642-650. https://doi.org/10.1016/j.copbio.2009.09.014

Cited by

  1. Control Efficacy of Bacillus velezensis AFB2-2 against Potato Late Blight Caused by Phytophthora infestans in Organic Potato Cultivation vol.37, pp.6, 2021, https://doi.org/10.5423/ppj.ft.09.2021.0138