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Rhizobacteria modify soil biological indices and induce tolerance to osmotic stress in tomato depending on the salinity level and bacteria species

  • Environmental Microbiology - Research Paper
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Abstract

Salinity is a major abiotic stress that impacts crop productivity globally. Plant growth-promoting rhizobacteria (PGPRs) exploit several mechanisms to not only decrease soil salinity but also improve the systemic tolerance of plants to osmotic stress. In this work, the effect of five PGPR strains was investigated on the growth and physiological responses of tomato plants, including stomatal closure, proline, and K+ and Na+ content under a range of salt stress, 0, 2.5, 5, 7.5, and 10 dS m−1. The effect of PGPR strains and salinity levels on the soil biological characteristics was also investigated. Salt stress affected the plant growth and physiological factors and soil biological factors in a dose-dependent manner. The highest saline stress, 10 dS m−1, reduced shoot and root dry weight and root volume up to 51.3, 41.5, and 51.8%, respectively. It also increased stomatal resistance and proline content 2.01- and 3.66-folds and decreased K+/Na+ ratio 4.16-folds, respectively. It also reduced basal respiration, substrate-induced respiration, and microbial biomass carbon up to 2.25-, 4.83-, and 6.7-folds and increased qCO2 3.18-folds, respectively. PGPR strains were able to modulate salt tolerance mechanisms, improve plant growth factors, and improve soil biological indicators. Bacillus megaterium P2 was the best strain in the balancing K+/Na+ uptake at least at 10 dS m−1. However, the efficiency of strains was dependent on the magnitude of salt stress. Therefore, it is possible to introduce PGPR strains based on soil salt level or exploit rhizobacteria consortia to manage salt stress in different conditions.

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References

  1. Egamberdieva D, Lugtenberg B (2014) Use of plant growth-promoting rhizobacteria to alleviate salinity stress in plants. In: Use of microbes for the alleviation of soil stresses, Vol 1. Springer, p 73–96

  2. Bhat MA, Kumar V, Bhat MA, Wani IA, Dar FL, Farooq I, Bhatti F, Koser R, Rahman S, Jan AT (2020) Mechanistic insights of the interaction of plant growth-promoting rhizobacteria (PGPR) with plant roots toward enhancing plant productivity by alleviating salinity stress. Front Microbiol 11:1952. https://doi.org/10.3389/fmicb.2020.01952

  3. Dimkpa C, Weinand T, Asch F (2009) Plant–rhizobacteria interactions alleviate abiotic stress conditions. Plant Cell Environ 32(12):1682–1694

    Article  CAS  Google Scholar 

  4. Zhang H, Kim MS, Sun Y, Dowd SE, Shi H, Pare PW (2008) Soil bacteria confer plant salt tolerance by tissue-specific regulation of the sodium transporter HKT1. Mol Plant Microbe Interact 21(6):737–744. https://doi.org/10.1094/MPMI-21-6-0737

    Article  CAS  PubMed  Google Scholar 

  5. Ha-Tran DM, Nguyen TTM, Hung S-H, Huang E, Huang C-C (2021) Roles of plant growth-promoting rhizobacteria (PGPR) in stimulating salinity stress defense in plants: a review. Int J Mol Sci 22:3154. https://doi.org/10.3390/ijms22063154

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Hirayama T, Shinozaki K (2010) Research on plant abiotic stress responses in the post-genome era: past, present and future. Plant J 61(6):1041–1052

    Article  CAS  Google Scholar 

  7. Sharifi R, Ryu CM (2017) Chatting with a tiny belowground member of the holobiome: communication between plants and growth-promoting rhizobacteria. Adv Bot Res 82:135–160. https://doi.org/10.1016/bs.abr.2016.09.002

    Article  CAS  Google Scholar 

  8. Yang J, Kloepper JW, Ryu CM (2009) Rhizosphere bacteria help plants tolerate abiotic stress. Trends Plant Sci 14(1):1–4. https://doi.org/10.1016/j.tplants.2008.10.004

    Article  CAS  PubMed  Google Scholar 

  9. Han Q-Q, Lü X-P, Bai J-P, Qiao Y, Paré PW, Wang S-M, Zhang J-L, Wu Y-N, Pang X-P, Xu W-B (2014) Beneficial soil bacterium Bacillus subtilis (GB03) augments salt tolerance of white clover. Front Plant Sci 5:525. https://doi.org/10.3389/fpls.2014.00525

  10. Campos CAB, Fernandes PD, Gheyi HR, Blanco FF, Gonçalves CB, Campos SAF (2006) Yield and fruit quality of industrial tomato under saline irrigation. Scientia Agricola 63:146–152

    Article  CAS  Google Scholar 

  11. Rahman MM, Hossain M, Hossain KFB, Sikder MT, Shammi M, Rasheduzzaman M, Hossain MA, Alam AM, Uddin MK (2018) Effects of NaCl-salinity on tomato (Lycopersicon esculentum Mill.) plants in a pot experiment. Open Agric 3(1):578–585

    Article  Google Scholar 

  12. Jafari S, Chorom M, Enayatizamir N, Motamedi H (2013) Evaluating the effects of Bacillus Subtilis and Corynebacterium glutamicum on soil microbial indexes in different levels of salinity. J Agric Eng 35(2):55–70

    Google Scholar 

  13. Vafadar R, Ghavidel A, Goli E, Soltani AA (2017) The effect of Pseudomonas fluorescens and Pseudomonas putida on some soil biological properties and plant growth indices of wheat under salt stress. J Agric Sci Sustain Prod 27(4):65–79

    Google Scholar 

  14. Ali S, Charles TC, Glick BR (2014) Amelioration of high salinity stress damage by plant growth-promoting bacterial endophytes that contain ACC deaminase. Plant Physiol Biochem 80:160–167

    Article  CAS  Google Scholar 

  15. Chandra P, Wunnava A, Verma P, Chandra A, Sharma RK (2021) Strategies to mitigate the adverse effect of drought stress on crop plants—influences of soil bacteria: a review. Pedosphere 31(3):496–509

    Article  Google Scholar 

  16. Yan N, Marschner P, Cao W, Zuo C, Qin W (2015) Influence of salinity and water content on soil microorganisms. Int Soil Water Conser Res 3(4):316–323

    Article  Google Scholar 

  17. Yuan B-C, Li Z-Z, Liu H, Gao M, Zhang Y-Y (2007) Microbial biomass and activity in salt affected soils under arid conditions. Appl Soil Ecol 35(2):319–328

    Article  Google Scholar 

  18. Shah S, Shah Z (2011) Changes in soil microbial characteristics with elevated salinity. Sarhad J Agric 27(2):233–244

    Google Scholar 

  19. Anderson TH, Domsch KH (1993) The metabolic quotient for CO2 (qCO2) as a specific activity parameter to assess the effects of environmental conditions, such as pH, on the microbial biomass of forest soils. Soil Biol Biochem 25(3):393–395

    Article  Google Scholar 

  20. Sharifi R, Lee SM, Ryu CM (2018) Microbe-induced plant volatiles. New Phytol 220(3):684–691

    Article  Google Scholar 

  21. Picard C, Baruffa E, Bosco M (2008) Enrichment and diversity of plant-probiotic microorganisms in the rhizosphere of hybrid maize during four growth cycles. Soil Biol Biochem 40(1):106–115

    Article  CAS  Google Scholar 

  22. Chen J, Sharifi R, Khan MSS, Islam F, Bhat JA, Kui L, Majeed M (2022) Wheat microbiome: structure, dynamics, and role in improving performance under stress environments. Front Microbiol 12:821546. https://doi.org/10.3389/fmicb.2021.821546

  23. Tewari S, Arora NK (2014) Multifunctional exopolysaccharides from Pseudomonas aeruginosa PF23 involved in plant growth stimulation, biocontrol and stress amelioration in sunflower under saline conditions. Curr Microbiol 69(4):484–494. https://doi.org/10.1007/s00284-014-0612-x

    Article  CAS  PubMed  Google Scholar 

  24. Singh JS, Pandey VC, Singh D (2011) Efficient soil microorganisms: a new dimension for sustainable agriculture and environmental development. Agr Ecosyst Environ 140(3–4):339–353

    Article  Google Scholar 

  25. Sharifi R, Ryu C-M (2018) Sniffing bacterial volatile compounds for healthier plants. Curr Opin Plant Biol 44:88–97

    Article  CAS  Google Scholar 

  26. Silva R, Filgueiras L, Santos B, Coelho M, Silva M, Estrada-Bonilla G, Vidal M, Baldani JI, Meneses C (2020) Gluconacetobacter diazotrophicus changes the molecular mechanisms of root development in Oryza sativa L. growing under water stress. Int J Mol Sci 21(1):333

    Article  CAS  Google Scholar 

  27. Filgueiras L, Silva R, Almeida I, Vidal M, Baldani JI, Meneses CHSG (2020) Gluconacetobacter diazotrophicus mitigates drought stress in Oryza sativa L. Plant Soil 451(1):57–73. https://doi.org/10.1007/s11104-019-04163-1

    Article  CAS  Google Scholar 

  28. Glick BR, Jacobson CB, Schwarze MM, Pasternak J (1994) 1-Aminocyclopropane-1-carboxylic acid deaminase mutants of the plant growth promoting rhizobacterium Pseudomonas putida GR12-2 do not stimulate canola root elongation. Can J Microbiol 40(11):911–915

    Article  CAS  Google Scholar 

  29. Bouyoucos GJ (1962) Hydrometer method improved for making particle size analyses of soils. Agron J 54(5):464–465

    Article  Google Scholar 

  30. Bremmer JM, Mulvaney CS (1982) Nitrogen—Total. In: Page AL (ed) Methods of soil analysis: part 2 chemical and microbiological properties. American society of agronomy. Soil Science Society of America, Madison, Wisconsin, pp 595–624. https://doi.org/10.2134/agronmonogr9.2.2ed.c31

  31. Walkley A (1947) A critical examination of a rapid method for determining organic carbon in soils—effect of variations in digestion conditions and of inorganic soil constituents. Soil Sci 63(4):251–264

    Article  CAS  Google Scholar 

  32. Mclean E (1983) Soil pH and Lime Requirement. In: Page A (ed) Methods of soil analysis, Part 2: Chemical and microbiological properties. pp 199–224. https://doi.org/10.2134/agronmonogr9.2.2ed.c12

  33. Richards LA (1969) Diagnosis and improvement of saline and alkali soils. United States Department Of Agriculture, Washington

    Google Scholar 

  34. Allison L, Moodie C (1965) Carbonate. In :Norman AG (ed) Methods of soil analysis, Part 2: chemical and microbiological properties. pp 1379–1396. https://doi.org/10.2134/agronmonogr9.2.c40

  35. Chapman H (1965) Total exchangeable bases. In: Norman AG (ed) Methods of soil analysis, part 2: chemical and microbiological properties. American Society of Agronomy, pp 902–904. https://doi.org/10.2134/agronmonogr9.2.c7

  36. Olsen SR, Dean LA (1965) Phosphorus. In: Methods of soil analysis, vol 9. American Society of Agronomy, p 920–926

  37. Chapman HD (1965) Cation exchange capacity. In: Black CA (ed) Methods of soil analysis. American Society of Agronomy, Madison, pp 891–901. https://doi.org/10.2134/agronmonogr9.2.c6

  38. Amani-Mehr M (2016) Biological control of tomato damping-off caused by Pythium aphanidermatum with rhizobacteria isolated from tomato rhizosphere. MSc. thesis, Razi University, Kermanshah, Iran

  39. Mahmoudighadi P, Zarin-taj A, Abdoulkarim K (2011) The effect of Thiobacillus on tomato growth and yield under salinity condition. Salt J 3:63–70

    Google Scholar 

  40. Bates LS, Waldren RP, Teare ID (1973) Rapid determination of free proline for water-stress studies. Plant Soil 39(1):205–207

    Article  CAS  Google Scholar 

  41. Skoog DA, West DM, Holler FJ, Crouch SR (2007) Analytical chemistry: an introduction. New ge International PVT,, UK

  42. Raiesi F, Beheshti A (2015) Microbiological indicators of soil quality and degradation following conversion of native forests to continuous croplands. Ecol Ind 50:173–185

    Article  CAS  Google Scholar 

  43. Alef K, Nannipieri P (1995) Methods in applied soil microbiology and biochemistry. Academic Press

    Google Scholar 

  44. Zhang H, Kim MS, Krishnamachari V, Payton P, Sun Y, Grimson M, Farag MA, Ryu CM, Allen R, Melo IS, Pare PW (2007) Rhizobacterial volatile emissions regulate auxin homeostasis and cell expansion in Arabidopsis. Planta 226(4):839–851. https://doi.org/10.1007/s00425-007-0530-2

    Article  CAS  PubMed  Google Scholar 

  45. Lima ACP, Medici LO, Pereira DAGdSB, Lima EdA (2020) Root growth in tomato seedlings in response to bacterial inoculation Serratia sp. Res Soc Dev 9(7):e89973634. https://doi.org/10.33448/rsd-v9i7.3634

    Article  Google Scholar 

  46. Asli S, Neumann PM (2010) Rhizosphere humic acid interacts with root cell walls to reduce hydraulic conductivity and plant development. Plant Soil 336:313–322

    Article  CAS  Google Scholar 

  47. Ashraf M, Foolad M (2007) Roles of glycine betaine and proline in improving plant abiotic stress resistance. Environ Exp Bot 59(2):206–216

    Article  CAS  Google Scholar 

  48. Zhang H, Murzello C, Sun Y, Kim MS, Xie X, Jeter RM, Zak JC, Dowd SE, Pare PW (2010) Choline and osmotic-stress tolerance induced in Arabidopsis by the soil microbe Bacillus subtilis (GB03). Mol Plant Microbe Interact 23(8):1097–1104. https://doi.org/10.1094/MPMI-23-8-1097

    Article  CAS  PubMed  Google Scholar 

  49. Sharifi R, Jeon J-S, Ryu C-M (2021) Belowground plant–microbe communications via volatile compounds. J Exp Bot. https://doi.org/10.1093/jxb/erab465

    Article  Google Scholar 

  50. de la Porte A, Schmidt R, Yergeau É, Constant P (2020) A gaseous milieu: extending the boundaries of the rhizosphere. Trends Microbiol 28(7):536–542

    Article  Google Scholar 

  51. Chen Y, Bonkowski M, Shen Y, Griffiths BS, Jiang Y, Wang X, Sun B (2020) Root ethylene mediates rhizosphere microbial community reconstruction when chemically detecting cyanide produced by neighbouring plants. Microbiome 8(1):4. https://doi.org/10.1186/s40168-019-0775-6

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  52. Kong HG, Song GC, Sim H-J, Ryu C-M (2021) Achieving similar root microbiota composition in neighbouring plants through airborne signalling. ISME J 15(2):397–408

    Article  CAS  Google Scholar 

  53. Sharifi R, Ryu C-M (2018) Revisiting bacterial volatile-mediated plant growth promotion: lessons from the past and objectives for the future. Ann Bot 122(3):349–358. https://doi.org/10.1093/aob/mcy108

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Funding

This study was funded by Razi University, Kermanshah, Iran (grant number 26.4.97).

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Authors

Contributions

Sheida Naseri, conceptualization, data collection, and methodology. Ali Beheshti Ale Agha, conceptualization, supervision, investigation, and data collection. Rouhallah Sharifi, conceptualization, supervision, methodology, investigation, and writing — review and editing. Sohbat Bahraminedjad, supervision, methodology, and validation.

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Correspondence to Ali Beheshti Ale Agha or Rouhallah Sharifi.

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Responsible Editor: Luc F.M. Rouws

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Naseri, S., Agha, A.B.A., Sharifi, R. et al. Rhizobacteria modify soil biological indices and induce tolerance to osmotic stress in tomato depending on the salinity level and bacteria species. Braz J Microbiol 53, 1473–1481 (2022). https://doi.org/10.1007/s42770-022-00781-7

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