Skip to main navigation menu Skip to main content Skip to site footer
Plant Science Today (PST)

Research Articles

Vol. 11 No. 2 (2024)

Bacillus cereus: an effective bio-inoculant for promoting salt stress tolerance of rice seedlings under saline soil conditions

DOI
https://doi.org/10.14719/pst.3096
Submitted
17 November 2023
Published
19-02-2024 — Updated on 01-04-2024
Versions

Abstract

Plant growth-promoting rhizobacteria (PGPR) are a powerful tool to maintain sustainable agriculture and promote plant resistance to biotic and abiotic types of stress. Salinity, a major abiotic stress hampers plant growth, development, and yield. Salt-tolerant PGPR are effective agents for ameliorating salinity effects on rice plants. The present study endeavored to isolate, determine halotolerant ability, characterize Plant Growth Promoting (PGP) traits, and finally observe the effect of PGPR strain on plant growth promotion of rice plants under saline and non-saline conditions. Based on the 16S rRNA gene sequencing technique, the rhizobacterial strain DB2 was identified as Bacillus cereus ATCC 14579(T) from NCMR, NCCS Pune. To check the growth-promoting ability, the strain was inoculated with two rice genotypes named Chinsurah Nona I (salt tolerant-non aromatic) and Badshabhog (aromatic) under polyhouse conditions. Results showed a significant increment in relative water content (RWC), total chlorophyll content (TCC), root length (RL), and shoot length (SL) in both rice genotypes inoculated with DB2 under both saline and non-saline conditions. Under non-saline conditions enhancement of RWC, TCC, RL, and SL was better in DB2 inoculated Chinsurah Nona I than in Badshabhog inoculated with DB2. Whereas, DB2-inoculated Badshabhog showed more recovery of RWC, TCC, RL, and SL than DB2-inoculated Chinsurah Nona I under saline conditions. Under salt stress conditions, inoculation with the rhizobacterial strain showed a significant reduction in electrolytic leakage (EL) in rhizobacteria inoculated with both rice genotypes. Moreover, DB2 inoculation showed a significant reduction in Na+ content in the roots of Chinsurah Nona I (44.6%) and Badshabhog (24.5%) rice genotypes. The present study has indicated that the application of salt-tolerant PGPR may be an effective and sustainable solution for rice cultivation under salt-stress conditions.

References

  1. Imran QM, Falak N, Hussain A, Mun BG, Yun BW. Abiotic stress in plants; stress perception to molecular response and role of biotechnological tools in stress resistance. Agronomy. 2021;11(8):1579. https://doi.org/10.3390/agronomy11081579
  2. Shultana R, Tan Kee Zuan A, Yusop MR, Mohd Saud H, Ayanda AF. Effect of salt-tolerant bacterial inoculations on rice seedlings differing in salt-tolerance under saline soil conditions. Agronomy. 2020;10(7):1030. https://doi.org/10.3390/agronomy10071030
  3. Thorat BS, Bagkar TA, Raut SM. Responses of rice under salinity stress: A review. IJCS. 2018;6(4):1441-47.
  4. Zhao S, Zhang Q, Liu M, Zhou H, Ma C, Wang P. Regulation of plant responses to salt stress. International Journal of Molecular Sciences. 2021;22(9):4609. https://doi.org/10.3390%2Fijms22094609
  5. Athar HU, Zulfiqar F, Moosa A, Ashraf M, Zafar ZU, Zhang L et al. Salt stress proteins in plants: An overview. Frontiers in Plant Science. 2022;13:999058. https://doi.org/10.3389%2Ffpls.2022.999058
  6. EL Sabagh A, Islam MS, Skalicky M, Ali Raza M, Singh K, Anwar Hossain M et al. Salinity stress in wheat (Triticum aestivum L.) in the changing climate: Adaptation and management strategies. Frontiers in Agronomy. 2021;3:661932. https://doi.org/10.3389/fagro.2021.661932
  7. Solis CA, Yong MT, Vinarao R, Jena K, Holford P, Shabala L et al. Back to the wild: on a quest for donors toward salinity tolerant rice. Frontiers in Plant Science. 2020;11:323. https://doi.org/10.3389/fpls.2020.00323
  8. Singh P, Pandey V, Parihar P. Microbes derived exopolysaccharides play role in salt stress alleviation in plants. Microbial Polymers: Applications and Ecological Perspectives. 2021:355-72. https://doi.org/10.1007/978-981-16-0045-6_16
  9. Qin H, Li Y, Huang R. Advances and challenges in the breeding of salt-tolerant rice. International Journal of Molecular Sciences. 2020;21(21):8385. https://doi.org/10.3390/ijms21218385
  10. Hmaeid N, Wali M, Mahmoud OM, Pueyo JJ, Ghnaya T, Abdelly C. Efficient rhizobacteria promote growth and alleviate NaCl-induced stress in the plant species Sulla carnosa. Applied Soil Ecology. 2019;133:104-13. https://doi.org/10.1016/j.apsoil.2018.09.011
  11. Singh RP, Jha PN. Alleviation of salinity-induced damage on wheat plant by an ACC deaminase-producing halophilic bacterium Serratia sp. SL-12 isolated from a salt lake. Symbiosis. 2016;69:101-11. https://doi.org/10.1007/s13199-016-0387-x
  12. Vaishnav A, Varma A, Tuteja N, Choudhary DK. PGPR-mediated amelioration of crops under salt stress. In: Choudhary D, Varma A, Tuteja N, editors. Plant-microbe interaction: an approach to sustainable agriculture. Singapore: Springer. 2016;p.205-26. https://doi.org/10.1007/978-981-10-2854-0_10
  13. Whipps JM. Microbial interactions and biocontrol in the rhizosphere. J Exp Bot. 2001;52:487-511. https://doi.org/10.1093/jxb/52.suppl_1.487
  14. Chandra S, Askari K, Kumari M. Optimization of indole acetic acid production by isolated bacteria from Stevia rebaudiana rhizosphere and its effects on plant growth. Journal of Genetic Engineering and Biotechnology. 2018;16(2):581-86. https://doi.org/10.1016/j.jgeb.2018.09.001
  15. Saleem S, Iqbal A, Ahmed F, Ahmad M. Phytobeneficial and salt stress mitigating efficacy of IAA producing salt tolerant strains in Gossypium hirsutum. Saudi Journal of Biological Sciences. 2021;28(9):5317-24. https://doi.org/10.1016/j.sjbs.2021.05.056
  16. Egamberdieva D, Wirth S, Bellingrath-Kimura SD, Mishra J, Arora NK. Salt-tolerant plant growth promoting rhizobacteria for enhancing crop productivity of saline soils. Frontiers in Microbiology. 2019;10:2791. https://doi.org/10.3389/fmicb.2019.02791
  17. Bogino PC, de las Mercedes Oliva M, Sorroche FG, Giordano W. The role of bacterial biofilms and surface components in plant-bacterial associations. International Journal of Molecular Sciences. 2013;14(8):15838-59. https://doi.org/10.3390/ijms140815838
  18. Bhagat N, Raghav M, Dubey S, Bedi N. Bacterial exopolysaccharides: Insight into their role in plant abiotic stress tolerance. J Microbiol Biotechnol. 2021;31:1045-59. https://doi.org/10.4014/jmb.2105.05009
  19. Mahmud FA, Islam MA, Rubel MH, Mukharjee SK, Kumar M, Bhattacharya P, Ahmed F. Effects of halotolerant rhizobacteria on rice seedlings under salinity stress. Science of the Total Environment. 2023;892:163774. https://doi.org/10.1016/j.scitotenv.2023.163774
  20. Gupta A, Tiwari RK, Shukla R, Singh AN, Sahu PK. Salinity alleviator bacteria in rice (Oryza sativa L.), their colonization efficacy, and synergism with melatonin. Frontiers in Plant Science. 2023;13:1060287.https://doi.org/10.3389/fpls.2022.1060287
  21. Hong BH, Joe MM, Selvakumar G, Kim KY, Choi JH, Sa TM. Influence of salinity variations on exocellular polysaccharide production, biofilm formation and flocculation in halotolerant bacteria. Journal of Environmental Biology. 2017;38(4):657. https://doi.org/10.22438/jeb/38/4/MRN-284
  22. Bric JM, Bostock RM, Silverstone SE. Rapid in situ assay for indoleacetic acid production by bacteria immobilized on a nitrocellulose membrane. Applied and Environmental Microbiology. 1991;57(2):535-38. https://doi.org/10.1128/aem.57.2.535-538.1991
  23. RI P. Mobilization of phosphorus in soil in connection with the vital activity of some microbial species. Microbiologiya. 1948;17:362-70.
  24. Premono ME, Moawad AM, Vlek PL. Effect of phosphate-solubilizing Pseudomonas putida on the growth of maize and its survival in the rhizosphere. Indonesian J Crop Sci. 1996;11:13-23.
  25. Rao Rajaramamohan V, Rao JL. Nitrogen fixation (C2H2 reduction) in soil samples from rhizosphere of rice grown under alternate flooded and non-flooded conditions. Plant and Soil. 1984;81:111-18. https://doi.org/10.1007/BF02206900.
  26. Cappuccino JC, Sherman N. In: Microbiology: A Laboratory Manual, 3rd ed., Benjamin/cummings Pub. Co., New York. 1992; p. 125-79.
  27. DuBois M, Gilles KA, Hamilton JK, Rebers PT, Smith F. Colorimetric method for determination of sugars and related substances. Analytical Chemistry. 1956;28(3):350-56. https://doi.org/10.1021/ac60111a017
  28. Lorck H. Production of hydrocyanic acid by bacteria. Physiologia Plantarum. 1948;1(2):142-46. https://doi.org/10.1111/j.1399-3054.1948.tb07118.x
  29. Caten CE, Jinks JL. Spontaneous variability of single isolates of Phytophthora infestans. I. cultural variation. Canadian Journal of Botany. 1968;46(4):329-48. https://doi.org/10.1139/b68-055
  30. Sapkota A. Catalase Test- Principle, Procedure, Types, Results, Uses. 2022.
  31. Chaiharn M, Chunhaleuchanon S, Kozo A, Lumyong S. Screening of rhizobacteria for their plant growth promoting activities. Current Applied Science and Technology. 2008;8(1):18-23.
  32. Sambrook J, Fritsch EF, Maniatis T. Molecular cloning: a laboratory manual. Cold Spring Harbor NY, Cold Spring Harbor Laboratory. 1989;11:31.
  33. Yoon SH, Ha SM, Kwon S, Lim J, Kim Y, Seo H, Chun J. Introducing EzBioCloud: a taxonomically united database of 16S rRNA gene sequences and whole-genome assemblies. International Journal of Systematic and Evolutionary Microbiology. 2017;67(5):1613. https://doi.org/10.1099%2Fijsem.0.001755
  34. Kumar S, Stecher G, Li M, Knyaz C, Tamura K. MEGA X: molecular evolutionary genetics analysis across computing platforms. Molecular Biology and Evolution. 2018;35(6):1547. https://doi.org/10.1093%2Fmolbev%2Fmsy096
  35. Jukes TH, Cantor CR. Evolution of protein molecules. In: Munro HN, editor. Mammalian Protein Metabolism. New York: Academic Press. 1969;p. 21-132. https://doi.org/10.1016/B978-1-4832-3211-9.50009-7
  36. Teulat B, Zoumarou-Wallis N, Rotter B, Ben Salem M, Bahri H, This D. QTL for relative water content in field-grown barley and their stability across Mediterranean environments. Theoretical and Applied Genetics. 2003;108:181-88. https://doi.org/10.1007/s00122-003-1417-7
  37. Yang G, Rhodes D, Joly RJ. Effects of high temperature on membrane stability and chlorophyll fluorescence in glycine betaine-deficient and glycine betaine-containing maize lines. Functional Plant Biology. 1996;23(4):437-43. https://doi.org/10.1071/PP9960437)
  38. Arnon DI. Copper enzymes in isolated chloroplasts. Polyphenoloxidase in Beta vulgaris. Plant Physiology. 1949 Jan;24(1):1. https://doi.org/10.1104%2Fpp.24.1.1
  39. El Mahi H, Pérez-Hormaeche J, De Luca A, Villalta I, Espartero J, Gámez-Arjona F, et al. A critical role of sodium flux via the plasma membrane Na+/H+ exchanger SOS1 in the salt tolerance of rice. Plant Physiology. 2019;180(2):1046-65. https://doi.org/10.1104/pp.19.00324
  40. Ammar FO. Preparation of bacteria for scanning electron microscope and common reagents preparation protocols. 2017. http://dx.doi.org/10.13140/RG.2.2.16802.84160
  41. Chinachanta K, Shutsrirung A, Herrmann L, Lesueur D, Pathom-Aree W. Enhancement of the aroma compound 2-acetyl-1-pyrroline in Thai jasmine rice (Oryza sativa) by rhizobacteria under salt stress. Biology. 2021;10(10):1065. https://doi.org/10.3390/biology10101065
  42. Subramanian S, Souleimanov A, Smith DL. Proteomic studies on the effects of lipo-chitooligosaccharide and thuricin 17 under unstressed and salt-stressed conditions in Arabidopsis thaliana. Frontiers in Plant Science. 2016;7:1314. https://doi.org/10.3389/fpls.2016.01314
  43. Nawaz A, Shahbaz M, Asadullah, Imran A, Marghoob MU, Imtiaz M, Mubeen F. Potential of salt tolerant PGPR in growth and yield augmentation of wheat (Triticum aestivum L.) under saline conditions. Frontiers in Microbiology. 2020;11:2019. https://doi.org/10.3389/fmicb.2020.02019
  44. Kubi HA, Khan MA, Adhikari A, Imran M, Kang SM, Hamayun M, Lee IJ. Silicon and plant growth-promoting rhizobacteria Pseudomonas psychrotolerans CS51 mitigates salt stress in Zea mays L. Agriculture. 2021;11(3):272. https://doi.org/10.3390/agriculture11030272
  45. Arora M, Kaushik A, Rani N, Kaushik CP. Effect of cyanobacterial exopolysaccharides on salt stress alleviation and seed germination. Journal of Environmental Biology. 2010;31(5):701-04.
  46. Wang R, Wang C, Feng Q, Liou RM, Lin YF. Biological inoculant of salt-tolerant bacteria for plant growth stimulation under different saline soil conditions. J Microbiol Biotechnol. 2021;31(3):398-407. https://doi.org/10.4014/jmb.2009.09032
  47. Bhattacharyya C, Bakshi U, Mallick I, Mukherji S, Bera B, Ghosh A. Genome-guided insights into the plant growth promotion capabilities of the physiologically versatile Bacillus aryabhattai strain AB211. Frontiers in Microbiology. 2017;411. https://doi.org/10.3389/fmicb.2017.00411
  48. Khadiri M, Boubaker H, Askarne L, Ezrari S, Radouane N, Farhaoui A et al. Bacillus cereus B8W8 an effective bacterial antagonist against major postharvest fungal pathogens of fruit. Postharvest Biology and Technology. 2023;200:112315. https://doi.org/10.1016/j.postharvbio.2023.112315
  49. Ali B, Hafeez A, Afridi MS, Javed MA, Sumaira, Suleman F, Nadeem M, et al. Bacterial-mediated salinity stress tolerance in maize (Zea mays L.): A fortunate way toward sustainable agriculture. ACS Omega. 2023. https://doi.org/10.1021/acsomega.3c00723
  50. Gou WE, Tian LI, Ruan ZH, Zheng PE, Chen FU, Zhang L et al. Accumulation of choline and glycine betaine and drought stress tolerance induced in maize (Zea mays) by three plant growth-promoting rhizobacteria (PGPR) strains. Pak J Bot. 2015;47(2):581-86.
  51. Soltys-Kalina D, Plich J, Strzelczyk-?yta D, ?liwka J, Marczewski W. The effect of drought stress on the leaf relative water content and tuber yield of a half-sib family of ‘Katahdin’-derived potato cultivars. Breeding Science. 2016;66(2):328-31. https://doi.org/10.1270/jsbbs.66.328
  52. Demidchik V, Straltsova D, Medvedev SS, Pozhvanov GA, Sokolik A, Yurin V. Stress-induced electrolyte leakage: the role of K+-permeable channels and involvement in programmed cell death and metabolic adjustment. Journal of Experimental Botany. 2014;65(5):1259-70. https://doi.org/10.1093/jxb/eru004
  53. Hannachi S, Steppe K, Eloudi M, Mechi L, Bahrini I, Van Labeke MC. Salt stress-induced changes in photosynthesis and metabolic profiles of one tolerant (‘Bonica’) and one sensitive (‘Black beauty’) eggplant cultivars (Solanum melongena L.). Plants. 2022;11(5):590. https://doi.org/10.3390/plants11050590
  54. Hatsugai N, Katagiri F. Quantification of plant cell death by electrolyte leakage assay. Bio-Protocol. 2018 Mar 5;8(5):e2758. https://doi.org/10.21769%2FBioProtoc.2758
  55. Kushwaha P, Kashyap PL, Kuppusamy P, Srivastava AK, Tiwari RK. Functional characterization of endophytic bacilli from pearl millet (Pennisetum glaucum) and their possible role in multiple stress tolerance. Plant Biosystems- An International Journal Dealing with all Aspects of Plant Biology. 2020 Jul 3;154(4):503-14. https://doi.org/10.1080/11263504.2019.1651773

Downloads

Download data is not yet available.