Bacillus megaterium RTS1 enhances resistance of Lycopersicon esculentum to salinity stress through the improvement of antioxidant defenses
,
Abstract
Background and Objectives: Plant growth-promoting bacteria (PGPB) may reduce the negative effects of salinity stress. The aim of this study was to optimize Bacillus megaterium RTS1 and characterize the effect of the PGPB on the physiological characteristics of tomato (Lycopersicon esculentum).
Materials and Methods: The Central composite design (CCD) of response surface methodology (RSM) was used to optimize Bacillus megaterium RTS1 to produce maximum cell biomass and spores. Then the effect of the PGPB on the physiological characteristics of tomato (Lycopersicon esculentum), including membrane stability, leaf relative water content percentage, anthocyanin and carotenoids content, chlorophyll photosynthetic parameters, sugar and starch level, superoxide anion and antioxidant activity under salt stress conditions. The NFB medium was inoculated with 5% bacterial culture and the fermentation was carried out in a 10-lit fermenter.
Results: After optimization, the amount of cell biomass by the model was 9.45 log10 CFUs/mL, which showed a 1.2-fold increase compared to the non-optimized medium. Usage of bacteria under the optimal conditions of the culture medium may increase the stability of the membrane and improve the relative water content. Bacteria were able to prevent the excessive increase of anthocyanins. Oxidative stress led to an increase in the content of chlorophyll a, while causing the degradation of chlorophyll b. Bacterial inoculation led to an increase in the level of sugar and starch compared to the control. PGPB showed an increasing effect on the amount of superoxide anion production and caused a significant increase in the antioxidant activity under salinity stress conditions.
Conclusion: The PGPB can be a promising way to boost physiological characteristics of tomato plant under salinity stress. Also, sporulation capacity of Bacillus megaterium with high bacterial cell density in fermenter produce a sustainable product for tomato plants.
1. Singh VK, Singh AK, Kumar A. Disease management of tomato through PGPB: current trends and future perspective. 3 Biotech 2017; 7: 255.
2. Kojima T, Higuchi A, Goto E, Matsumoto Y, Dogru M, Tsubota K. Autologous serum eye drops for the treatment of dry eye diseases. Cornea 2008; 27 Suppl 1: S25-30.
3. DePhillipo NN, Aman ZS, Kennedy MI, Begley JP, Moatshe G, LaPrade RF. Efficacy of vitamin C supplementation on collagen synthesis and oxidative stress after musculoskeletal injuries: a systematic review. Orthop J Sports Med 2018; 6: 2325967118804544.
4. Ordóñez-Santos LE, Martínez-Girón J. Thermal degradation kinetics of carotenoids, vitamin C and provitamin A in tree tomato juice. Int J Food Sci Technol 2020; 55: 201-210.
5. Tito A, Carola A, Bimonte M, Barbulova A, Arciello S, de Laurentiis F, et al. A tomato stem cell extract, containing antioxidant compounds and metal chelating factors, protects skin cells from heavy metal‐induced damages. Int J Cosmet Sci 2011; 33: 543-552.
6. Kumar A, Singh S, Gaurav AK, Srivastava S, Verma JP. Plant growth-promoting bacteria: biological tools for the mitigation of salinity stress in plants. Front Microbiol 2020; 11: 1216.
7. Krishna R, Karkute SG, Ansari WA, Jaiswal DK, Verma JP, Singh M. Transgenic tomatoes for abiotic stress tolerance: status and way ahead. 3 Biotech 2019; 9: 143.
8. Singh A. Soil salinization and waterlogging: A threat to environment and agricultural sustainability. Ecol Indic 2015; 57: 128-130.
9. Cetin M, Kirda C. Spatial and temporal changes of soil salinity in a cotton field irrigated with low-quality water. J Hydrol 2003; 272: 238-249.
10. Shrivastava P, Kumar R. Soil salinity: A serious environmental issue and plant growth promoting bacteria as one of the tools for its alleviation. Saudi J Biol Sci 2015; 22: 123-131.
11. Zhang J, Zhang R, He Q, Ji B, Wang H, Yang K. Adaptation to salinity: Response of biogas production and microbial communities in anaerobic digestion of kitchen waste to salinity stress. J Biosci Bioeng 2020; 130: 173-178.
12. Tavakkoli E, Fatehi F, Coventry S, Rengasamy P, McDonald GK. Additive effects of Na+ and Cl–ions on barley growth under salinity stress. J Exp Bot 2011; 62: 2189-2203.
13. Oney-Birol S. Exogenous L-carnitine promotes plant growth and cell division by mitigating genotoxic damage of salt stress. Sci Rep 2019; 9: 17229.14. Czarnocka W, Karpiński S. Friend or foe? Reactive oxygen species production,
scavenging and signaling in plant response to environmental stresses. Free Radic Biol Med 2018; 122: 4-20.
15. Shilev S. Plant-growth-promoting bacteria mitigating soil salinity stress in plants. Appl Sci 2020; 10: 7326.
16. Gamalero E, Glick BR. Recent advances in bacterial amelioration of plant dought and salt stress. Biology (Basel) 2022; 11: 437.
17. Sevim G, Ozdemir-Kocak F, Unal D. Chapter 15 -Hormonal signaling molecules triggered by plant growth-promoting bacteria, in Phytohormones and Stress Responsive Secondary Metabolites. 2023, Elsevier. p. 187-196.
18. Bolstridge N, Card S, Stewart A, Jones EE. Use of rifampicinresistant bacterial biocontrol strains for monitoring survival in soil and colonisation of pea seedling roots. N Z Plant Prot 2009; 62: 34-40.
19. Yasmin H, Naeem S, Bakhtawar M, Jabeen Z, Nosheen A, Naz R, et al. Halotolerant rhizobacteria Pseudomonas pseudoalcaligenes and Bacillus subtilis mediate systemic tolerance in hydroponically grown soybean (Glycine max L.) against salinity stress. PLoS One 2020; 15(4): e0231348.
20. Yavarian S, Jafari P, Akbari N, Feizabadi MM. Selective screening and characterization of plant growth promoting bacteria for growth enhancement of tomato, Lycopersicon esculentum. Iran J Microbiol 2021; 13: 121-129.
21. Garrity G. Bergey's Manual® of Systematic Bacteriology. Volume 2. 2007: PartB.
22. Biesta-Peters EG, Reij MW, Joosten H, Gorris LG, Zwietering MH. Comparison of two optical-density-based methods and a plate count method for estimation of growth parameters of Bacillus cereus. Appl Environ Microbiol 2010; 76: 1399-1405.
23. Abou-Taleb KA, Mashhoor WA, Nasr SA, Sharaf MS. Production of vitamin B12 by Propionibacterium freudenreichii and Bacillus megaterium. J Agric Sci Mansoura Univ 2005; 30: 4149-4162.
24. Ramadas NV, Soccol CR, Pandey A. A statistical approach for optimization of polyhydroxybutyrate production by Bacillus sphaericus NCIM 5149 under submerged fermentation using central composite design. Appl Biochem Biotechnol 2010; 162: 996-1007.
25. Bajaj IB, Singhal RS. Enhanced production of poly (γ-glutamic acid) from Bacillus licheniformis NCIM 2324 by using metabolic precursors. Appl Biochem Biotechnol 2009; 159: 133-141.
26. Abusham RA, Rahman RN, Salleh AB, Basri M. Optimization of physical factors affecting the production of thermo-stable organic solvent-tolerant protease from a newly isolated halo tolerant Bacillus subtilis strain Rand. Microb Cell Fact 2009; 8: 20.
27. Carrasco-Fernández J, Guerra M, Castro GF, Bustamante L, Barra-Bucarei L, Ceballos R, et al. Plant growth promoting rhizobacteria from Juan Fernández archipelago improve germination rate of endangered plant Solanum fernandezianum Phil. Chil J Agric Res 2020; 80: 41-49.
28. Hasan SA, Jabeen S. Degradation kinetics and pathway of phenol by Pseudomonas and Bacillus species.
Biotechnol Biotechnol Equip 2015; 29: 45-53.
29. Premjit Y, Pandey S, Mitra J. Recent trends in Folic acid (Vitamin B9) encapsulation, controlled release, and mathematical modelling. Food Rev Int 2022; p. 1-35.
30. Odamtten GT, Nartey LK, Kwagyen WM, Anyebuno G, Kyei Baffour V. Resident microbial load, toxigenic potential and possible quality control measures of six imported seasoning powders on the Ghanaian market. J Nutr Health Food Eng 2018; 8: 24-35.
31. Abdelkrim S, Jebara SH, Jebara M. Antioxidant systems responses and the compatible solutes as contributing factors to lead accumulation and tolerance in Lathyrus sativus inoculated by plant growth promoting rhizobacteria. Ecotoxicol Environ Saf 2018; 166: 427-436.
32. Sims DA, Gamon JA. Relationships between leaf pigment content and spectral reflectance across a wide range of species, leaf structures and developmental stages. Remote Sens Environ 2002; 81: 337-354.
33. Irigoyen JJ, Einerich DW, Sánchez‐Díaz M. Water stress induced changes in concentrations of proline and total soluble sugars in nodulated alfalfa (Medicago sativd) plants. Physiol Plant 1992; 84: 55-60.
34. Osaki M, Shinano T, Kaneda T, Yamada S, Nakamura T. Ontogenetic changes of photosynthetic and dark respiration rates in relation to nitrogen content in individual leaves of field crops. Photosynthetica 2001; 39: 205-213.
35. Gajewska E, Skłodowska M. Antioxidative responses and proline level in leaves and roots of pea plants subjected to nickel stress. Acta Physiol Plant 2005; 27: 329-340.
36. Harkat-Madouri L, Asma B, Madani K, Bey-Ould Si Said Z, Rigou P, Grenier D, et al. Chemical composition, antibacterial and antioxidant activities of essential oil of Eucalyptus globulus from Algeria. Ind Crops Prod 2015; 78: 148-153.
37. Jiang M, Song Y, Kanwar MK, Ahammed GJ, Shao S, Zhou J. Phytonanotechnology applications in modern agriculture. J Nanobiotechnology 2021; 19: 430.
38. Gul Z, Tang Z-H, Arif M, Ye Z. An insight into abiotic stress and influx tolerance mechanisms in plants to cope in saline environments. Biology (Basel) 2022; 11: 597.
39. Coffeen WC, Wolpert TG. Purification and characterization of serine proteases that exhibit caspase-like activity and are associated with programmed cell death in Avena sativa. Plant Cell 2004; 16: 857-873.
40. Shabala S, Pottosin I. Regulation of potassium transport in plants under hostile conditions: implications for abiotic and biotic stress tolerance. Physiol Plant 2014; 151: 257-279.
41. Zhao C, Zhang H, Song C, Zhu JK, Shabala S. Mechanisms of plant responses and adaptation to soil salinity. Innovation (Camb) 2020; 1: 100017.
42. Turan MA, Awad Elkarim AH, Taban N, Taban S. Effect of salt stress on growth, stomatal resistance, proline and chlorophyll concentrations on maize plant. Afr J Agric Res 2009; 4: 893-897.
43. Zhao X, Nishimura Y, Fukumoto Y, Li J. Effect of high temperature on active oxygen species, senescence and photosynthetic properties in cucumber leaves. Environ Exp Bot 2011; 70: 212-216.
44. Ali MA, Fahad S, Haider I, Ahmed N, Ahmed S, Hussain S, et al. Oxidative stress and antioxidant defense in plants exposed to metal/metalloid toxicity. Reactive Oxygen, Nitrogen and Sulfur Species in Plants: Production, Metabolism, Signaling and Defense Mechanisms, 2019: p. 353-370.
45. Mangal V, Lai MK, Tiwari RK, Altaf MA, Sood S, Kumar D, et al. Molecular insights into the role of reactive oxygen, nitrogen and sulphur species in conferring salinity stress tolerance in plants. J Plant Growth Regul 2023; 42: 554-574.
46. Gill SS, Tuteja N. Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiol Biochem 2010; 48: 909-930.
47. Costa-Santos M, Mariz-Ponte N, Celeste Dias M, Moura L, Marques G, Santos C. Effect of Bacillus spp. and Brevibacillus sp. on the Photosynthesis and Redox Status of Solanum lycopersicum. Horticulturae 2021; 7: 24.
48. Katsenios N, Andreou V, Sparangis P, Djordjevic N, Giannoglou M, Chanioti S, et al. Evaluation of plant growth promoting bacteria strains on growth, yield and quality of industrial tomato. Microorganisms 2021; 9: 2099.
49. Pandhair V, Sekhon BS. Reactive oxygen species and antioxidants in plants: an overview. J Plant Biochem Biotechnol 2006; 15: 71-78.
50. Mohamed IA, Shalby N, Ei-Badri AM, Salem MH, Nauman Khan M, Nawaz MA, et al. Stomata and xylem vessels traits improved by melatonin application contribute to enhancing salt tolerance and fatty acid composition of Brassica napus L. plants. Agronomy 2020; 10: 1186.
51. Ayuso-Calles M, Flores-Felix J, Rivas R. Overview of the Role of Rhizobacteria in Plant Salt Stress Tolerance. Agronomy 2021; 11: 1759.
52. Zawoznik MS, Ameneiros M, Benavides MP, Vázquez S, Groppa MD. Response to saline stress and aquaporin expression in Azospirillum-inoculated barley seedlings. Appl Microbiol Biotechnol 2011; 90: 1389-1397.
53. Tiwari S, Prasad V, Chauhan PS, Lata C. Bacillus amyloliquefaciens confers tolerance to various abiotic stresses and modulates plant response to phytohormones through osmoprotection and gene expression regulation in rice. Front Plant Sci 2017; 8: 1510.
54. Mahmoud OMB, Hidri R, Talbi-Zribi O, Taamalli W, Abdelli C, Djebali A. Auxin and proline producing rhizobacteria mitigate salt-induced growth inhibition of barley plants by enhancing water and nutrient status. S Afr J Bot 2020; 128: 209-217.
55. Upadhyay SK, Singh JS, Singh DP. Exopolysaccharide-producing plant growth-promoting rhizobacteria under salinity condition. Pedosphere 2011; 21: 214-222.
56. Kasotia A, Varma A, Tuteja N, Kumar Choudhary D. Amelioration of soybean plant from saline-induced condition by exopolysaccharide producing Pseudomonas-mediated expression of high affinity K+-transporter (HKT1) gene. Curr Sci 2016; 111: 1961-1967.
2. Kojima T, Higuchi A, Goto E, Matsumoto Y, Dogru M, Tsubota K. Autologous serum eye drops for the treatment of dry eye diseases. Cornea 2008; 27 Suppl 1: S25-30.
3. DePhillipo NN, Aman ZS, Kennedy MI, Begley JP, Moatshe G, LaPrade RF. Efficacy of vitamin C supplementation on collagen synthesis and oxidative stress after musculoskeletal injuries: a systematic review. Orthop J Sports Med 2018; 6: 2325967118804544.
4. Ordóñez-Santos LE, Martínez-Girón J. Thermal degradation kinetics of carotenoids, vitamin C and provitamin A in tree tomato juice. Int J Food Sci Technol 2020; 55: 201-210.
5. Tito A, Carola A, Bimonte M, Barbulova A, Arciello S, de Laurentiis F, et al. A tomato stem cell extract, containing antioxidant compounds and metal chelating factors, protects skin cells from heavy metal‐induced damages. Int J Cosmet Sci 2011; 33: 543-552.
6. Kumar A, Singh S, Gaurav AK, Srivastava S, Verma JP. Plant growth-promoting bacteria: biological tools for the mitigation of salinity stress in plants. Front Microbiol 2020; 11: 1216.
7. Krishna R, Karkute SG, Ansari WA, Jaiswal DK, Verma JP, Singh M. Transgenic tomatoes for abiotic stress tolerance: status and way ahead. 3 Biotech 2019; 9: 143.
8. Singh A. Soil salinization and waterlogging: A threat to environment and agricultural sustainability. Ecol Indic 2015; 57: 128-130.
9. Cetin M, Kirda C. Spatial and temporal changes of soil salinity in a cotton field irrigated with low-quality water. J Hydrol 2003; 272: 238-249.
10. Shrivastava P, Kumar R. Soil salinity: A serious environmental issue and plant growth promoting bacteria as one of the tools for its alleviation. Saudi J Biol Sci 2015; 22: 123-131.
11. Zhang J, Zhang R, He Q, Ji B, Wang H, Yang K. Adaptation to salinity: Response of biogas production and microbial communities in anaerobic digestion of kitchen waste to salinity stress. J Biosci Bioeng 2020; 130: 173-178.
12. Tavakkoli E, Fatehi F, Coventry S, Rengasamy P, McDonald GK. Additive effects of Na+ and Cl–ions on barley growth under salinity stress. J Exp Bot 2011; 62: 2189-2203.
13. Oney-Birol S. Exogenous L-carnitine promotes plant growth and cell division by mitigating genotoxic damage of salt stress. Sci Rep 2019; 9: 17229.14. Czarnocka W, Karpiński S. Friend or foe? Reactive oxygen species production,
scavenging and signaling in plant response to environmental stresses. Free Radic Biol Med 2018; 122: 4-20.
15. Shilev S. Plant-growth-promoting bacteria mitigating soil salinity stress in plants. Appl Sci 2020; 10: 7326.
16. Gamalero E, Glick BR. Recent advances in bacterial amelioration of plant dought and salt stress. Biology (Basel) 2022; 11: 437.
17. Sevim G, Ozdemir-Kocak F, Unal D. Chapter 15 -Hormonal signaling molecules triggered by plant growth-promoting bacteria, in Phytohormones and Stress Responsive Secondary Metabolites. 2023, Elsevier. p. 187-196.
18. Bolstridge N, Card S, Stewart A, Jones EE. Use of rifampicinresistant bacterial biocontrol strains for monitoring survival in soil and colonisation of pea seedling roots. N Z Plant Prot 2009; 62: 34-40.
19. Yasmin H, Naeem S, Bakhtawar M, Jabeen Z, Nosheen A, Naz R, et al. Halotolerant rhizobacteria Pseudomonas pseudoalcaligenes and Bacillus subtilis mediate systemic tolerance in hydroponically grown soybean (Glycine max L.) against salinity stress. PLoS One 2020; 15(4): e0231348.
20. Yavarian S, Jafari P, Akbari N, Feizabadi MM. Selective screening and characterization of plant growth promoting bacteria for growth enhancement of tomato, Lycopersicon esculentum. Iran J Microbiol 2021; 13: 121-129.
21. Garrity G. Bergey's Manual® of Systematic Bacteriology. Volume 2. 2007: PartB.
22. Biesta-Peters EG, Reij MW, Joosten H, Gorris LG, Zwietering MH. Comparison of two optical-density-based methods and a plate count method for estimation of growth parameters of Bacillus cereus. Appl Environ Microbiol 2010; 76: 1399-1405.
23. Abou-Taleb KA, Mashhoor WA, Nasr SA, Sharaf MS. Production of vitamin B12 by Propionibacterium freudenreichii and Bacillus megaterium. J Agric Sci Mansoura Univ 2005; 30: 4149-4162.
24. Ramadas NV, Soccol CR, Pandey A. A statistical approach for optimization of polyhydroxybutyrate production by Bacillus sphaericus NCIM 5149 under submerged fermentation using central composite design. Appl Biochem Biotechnol 2010; 162: 996-1007.
25. Bajaj IB, Singhal RS. Enhanced production of poly (γ-glutamic acid) from Bacillus licheniformis NCIM 2324 by using metabolic precursors. Appl Biochem Biotechnol 2009; 159: 133-141.
26. Abusham RA, Rahman RN, Salleh AB, Basri M. Optimization of physical factors affecting the production of thermo-stable organic solvent-tolerant protease from a newly isolated halo tolerant Bacillus subtilis strain Rand. Microb Cell Fact 2009; 8: 20.
27. Carrasco-Fernández J, Guerra M, Castro GF, Bustamante L, Barra-Bucarei L, Ceballos R, et al. Plant growth promoting rhizobacteria from Juan Fernández archipelago improve germination rate of endangered plant Solanum fernandezianum Phil. Chil J Agric Res 2020; 80: 41-49.
28. Hasan SA, Jabeen S. Degradation kinetics and pathway of phenol by Pseudomonas and Bacillus species.
Biotechnol Biotechnol Equip 2015; 29: 45-53.
29. Premjit Y, Pandey S, Mitra J. Recent trends in Folic acid (Vitamin B9) encapsulation, controlled release, and mathematical modelling. Food Rev Int 2022; p. 1-35.
30. Odamtten GT, Nartey LK, Kwagyen WM, Anyebuno G, Kyei Baffour V. Resident microbial load, toxigenic potential and possible quality control measures of six imported seasoning powders on the Ghanaian market. J Nutr Health Food Eng 2018; 8: 24-35.
31. Abdelkrim S, Jebara SH, Jebara M. Antioxidant systems responses and the compatible solutes as contributing factors to lead accumulation and tolerance in Lathyrus sativus inoculated by plant growth promoting rhizobacteria. Ecotoxicol Environ Saf 2018; 166: 427-436.
32. Sims DA, Gamon JA. Relationships between leaf pigment content and spectral reflectance across a wide range of species, leaf structures and developmental stages. Remote Sens Environ 2002; 81: 337-354.
33. Irigoyen JJ, Einerich DW, Sánchez‐Díaz M. Water stress induced changes in concentrations of proline and total soluble sugars in nodulated alfalfa (Medicago sativd) plants. Physiol Plant 1992; 84: 55-60.
34. Osaki M, Shinano T, Kaneda T, Yamada S, Nakamura T. Ontogenetic changes of photosynthetic and dark respiration rates in relation to nitrogen content in individual leaves of field crops. Photosynthetica 2001; 39: 205-213.
35. Gajewska E, Skłodowska M. Antioxidative responses and proline level in leaves and roots of pea plants subjected to nickel stress. Acta Physiol Plant 2005; 27: 329-340.
36. Harkat-Madouri L, Asma B, Madani K, Bey-Ould Si Said Z, Rigou P, Grenier D, et al. Chemical composition, antibacterial and antioxidant activities of essential oil of Eucalyptus globulus from Algeria. Ind Crops Prod 2015; 78: 148-153.
37. Jiang M, Song Y, Kanwar MK, Ahammed GJ, Shao S, Zhou J. Phytonanotechnology applications in modern agriculture. J Nanobiotechnology 2021; 19: 430.
38. Gul Z, Tang Z-H, Arif M, Ye Z. An insight into abiotic stress and influx tolerance mechanisms in plants to cope in saline environments. Biology (Basel) 2022; 11: 597.
39. Coffeen WC, Wolpert TG. Purification and characterization of serine proteases that exhibit caspase-like activity and are associated with programmed cell death in Avena sativa. Plant Cell 2004; 16: 857-873.
40. Shabala S, Pottosin I. Regulation of potassium transport in plants under hostile conditions: implications for abiotic and biotic stress tolerance. Physiol Plant 2014; 151: 257-279.
41. Zhao C, Zhang H, Song C, Zhu JK, Shabala S. Mechanisms of plant responses and adaptation to soil salinity. Innovation (Camb) 2020; 1: 100017.
42. Turan MA, Awad Elkarim AH, Taban N, Taban S. Effect of salt stress on growth, stomatal resistance, proline and chlorophyll concentrations on maize plant. Afr J Agric Res 2009; 4: 893-897.
43. Zhao X, Nishimura Y, Fukumoto Y, Li J. Effect of high temperature on active oxygen species, senescence and photosynthetic properties in cucumber leaves. Environ Exp Bot 2011; 70: 212-216.
44. Ali MA, Fahad S, Haider I, Ahmed N, Ahmed S, Hussain S, et al. Oxidative stress and antioxidant defense in plants exposed to metal/metalloid toxicity. Reactive Oxygen, Nitrogen and Sulfur Species in Plants: Production, Metabolism, Signaling and Defense Mechanisms, 2019: p. 353-370.
45. Mangal V, Lai MK, Tiwari RK, Altaf MA, Sood S, Kumar D, et al. Molecular insights into the role of reactive oxygen, nitrogen and sulphur species in conferring salinity stress tolerance in plants. J Plant Growth Regul 2023; 42: 554-574.
46. Gill SS, Tuteja N. Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiol Biochem 2010; 48: 909-930.
47. Costa-Santos M, Mariz-Ponte N, Celeste Dias M, Moura L, Marques G, Santos C. Effect of Bacillus spp. and Brevibacillus sp. on the Photosynthesis and Redox Status of Solanum lycopersicum. Horticulturae 2021; 7: 24.
48. Katsenios N, Andreou V, Sparangis P, Djordjevic N, Giannoglou M, Chanioti S, et al. Evaluation of plant growth promoting bacteria strains on growth, yield and quality of industrial tomato. Microorganisms 2021; 9: 2099.
49. Pandhair V, Sekhon BS. Reactive oxygen species and antioxidants in plants: an overview. J Plant Biochem Biotechnol 2006; 15: 71-78.
50. Mohamed IA, Shalby N, Ei-Badri AM, Salem MH, Nauman Khan M, Nawaz MA, et al. Stomata and xylem vessels traits improved by melatonin application contribute to enhancing salt tolerance and fatty acid composition of Brassica napus L. plants. Agronomy 2020; 10: 1186.
51. Ayuso-Calles M, Flores-Felix J, Rivas R. Overview of the Role of Rhizobacteria in Plant Salt Stress Tolerance. Agronomy 2021; 11: 1759.
52. Zawoznik MS, Ameneiros M, Benavides MP, Vázquez S, Groppa MD. Response to saline stress and aquaporin expression in Azospirillum-inoculated barley seedlings. Appl Microbiol Biotechnol 2011; 90: 1389-1397.
53. Tiwari S, Prasad V, Chauhan PS, Lata C. Bacillus amyloliquefaciens confers tolerance to various abiotic stresses and modulates plant response to phytohormones through osmoprotection and gene expression regulation in rice. Front Plant Sci 2017; 8: 1510.
54. Mahmoud OMB, Hidri R, Talbi-Zribi O, Taamalli W, Abdelli C, Djebali A. Auxin and proline producing rhizobacteria mitigate salt-induced growth inhibition of barley plants by enhancing water and nutrient status. S Afr J Bot 2020; 128: 209-217.
55. Upadhyay SK, Singh JS, Singh DP. Exopolysaccharide-producing plant growth-promoting rhizobacteria under salinity condition. Pedosphere 2011; 21: 214-222.
56. Kasotia A, Varma A, Tuteja N, Kumar Choudhary D. Amelioration of soybean plant from saline-induced condition by exopolysaccharide producing Pseudomonas-mediated expression of high affinity K+-transporter (HKT1) gene. Curr Sci 2016; 111: 1961-1967.
| Files | ||
| Issue | Vol 15 No 5 (2023) | |
| Section | Original Article(s) | |
| DOI | https://doi.org/10.18502/ijm.v15i5.13874 | |
| Keywords | ||
| Plant growth-promoting bacteria (PGPBs); Bacillus megaterium; Lycopersicon esculentum; Salinity stress | ||
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How to Cite
1.
Yavarian S, Jafari P, Akbari N. Bacillus megaterium RTS1 enhances resistance of Lycopersicon esculentum to salinity stress through the improvement of antioxidant defenses. Iran J Microbiol. 2023;15(5):685-696.
