Abstract
Key message
Bacillus spizizenii is for the first time described as a plant growth salt-tolerant bacterium able to alleviate salt stress in crop plants by improving physiological parameters and antioxidant defense mechanisms.
Abstract
Agricultural soil salinization is a serious issue worldwide affecting agricultural yield. Plant growth promoting bacteria can enhance salt tolerance and plant yield. Bacillus spizizenii FMH45 has been shown to inhibit fungal attacks in tomato fruits and to augment tomato seed germination in presence of abiotic stresses. During this study, we reported for the first time B. spizizenii as a salt-tolerant bacterium able to alleviate salt stress in tomato plants. B. spizizenii FMH45 was examined in vitro for its potential to produce several plant growth promoting characters (siderophores, IAA, and phosphate solubilization) and hydrolytic enzymes (cellulase, glucanase and protease) in the presence of saline conditions. FMH45 was also investigated in vivo in pot experiments to evaluate its ability to promote tomato plant growth under salt stress condition. FMH45 inoculation, enhanced tomato seedling length, vigor index, and plant fresh and dry weights when compared to the non-inoculated controls exposed and not exposed to a regular irrigation with salt solutions containing: 0; 3.5; 7; and 10 g L−1 of NaCl. FMH45-treated plants also presented improved chlorophyll content, membrane integrity (MI), and phenol peroxidase (POX) concentrations, as well as reduced malondialdehyde (MDA) and hydrogen peroxide (H2O2) levels under saline conditions with a significant salinity × strain interaction. Furthermore, FMH45 inoculation significantly decreased endogenous Na+ accumulation, increased K+ and Ca2+ uptake, and thereby improved K+/Na+ and Ca2+/Na+ ratios. This study proves that bio-inoculation of FMH45 efficiently increases salt tolerance in tomato plants. This sustainable approach can be applied to other stressed plant species in affected soils.
Graphic abstract
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Abd_Allah EF, Alqarawi AA, Hashem A et al (2018) Endophytic bacterium Bacillus subtilis (BERA 71) improves salt tolerance in chickpea plants by regulating the plant defense mechanisms. J Plant Interact 13:37–44. https://doi.org/10.1080/17429145.2017.1414321
Abdul-Baki AA, Anderson JD (1973) Vigor determination in soybean seed by multiple criteria. Crop Sci 13:630–633. https://doi.org/10.2135/cropsci1973.0011183X001300060013x
Abeer H, Asma AH, Allah A et al (2015) Impact of plant growth promoting Bacillus subtilis on growth and physiological parameters of Bassia indica (indian bassia) grown udder salt stress. Pak J Bot 47:1735–1741
Ait Kaki A, Kacem Chaouche N, Dehimat L et al (2013) Biocontrol and plant growth promotion characterization of Bacillus species isolated from Calendula officinalis rhizosphere. Indian J Microbiol 53:447–452. https://doi.org/10.1007/s12088-013-0395-y
Alexander DB, Zuberer DA (1991) Use of chrome azurol S reagents to evaluate siderophore production by rhizosphere bacteria. Biol Fertil Soils 12:39–45. https://doi.org/10.1007/BF00369386
Amna, Din BU, Sarfraz S et al (2019) Mechanistic elucidation of germination potential and growth of wheat inoculated with exopolysaccharide and ACC- deaminase producing Bacillus strains under induced salinity stress. Ecotoxicol Environ Saf 183:109466. https://doi.org/10.1016/j.ecoenv.2019.109466
Bano A, Fatima M (2009) Salt tolerance in Zea mays (L). following inoculation with rhizobium and pseudomonas. Biol Fertil Soils 45:405–413. https://doi.org/10.1007/s00374-008-0344-9
Ben Khedher S, Mejdoub-Trabelsi B, Tounsi S (2021) 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
Benidire L, Daoui K, Fatemi ZA et al (2015) Effet du stress salin sur la germination et le développement des plantules de Vicia faba L. (Effect of salt stress on germination and seedling of Vicia faba L.). J Mater Environ Sci 6(3):840–851
Bochow H, El-Sayed SF, Junge H et al (2001) Use of Bacillus subtilis as biocontrol agent. IV. Salt-stress tolerance induction by Bacillus subtilis FZB24 seed treatment in tropical vegetable field crops, and its mode of action. J Plant Dis Prot 108:21–30
Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254. https://doi.org/10.1016/0003-2697(76)90527-3
Bric JM, Bostock RM, Silverstone SE (1991) Rapid in situ assay for indoleacetic acid production by bacteria immobilized on a nitrocellulose membrane. Appl Environ Microbiol 57:535–538. https://doi.org/10.1128/AEM.57.2.535-538.1991
Chalbi N, Hessini K, Gandour M et al (2013) Are changes in membrane lipids and fatty acid composition related to salt-stress resistance in wild and cultivated barley? J Plant Nutr Soil Sci 176:138–147. https://doi.org/10.1002/jpln.201100413
Damodaran T, Mishra VK, Jha SK et al (2019) Identification of rhizosphere bacterial diversity with promising salt tolerance, PGP traits and their exploitation for seed germination enhancement in sodic soil. Agric Res 8:36–43. https://doi.org/10.1007/s40003-018-0343-5
Dimkpa C, Weinand T, Asch F (2009) Plant–rhizobacteria interactions alleviate abiotic stress conditions. Plant Cell Environ 32:1682–1694. https://doi.org/10.1111/j.1365-3040.2009.02028.x
Dodd IC, Pérez-Alfocea F (2012) Microbial amelioration of crop salinity stress. J Exp Bot 63:3415–3428. https://doi.org/10.1093/jxb/ers033
Dunlap CA, Bowman MJ, Zeigler DR (2020) Promotion of Bacillus subtilis subsp. inaquosorum, Bacillus subtilis subsp. spizizenii and Bacillus subtilis subsp. stercoris to species status. Antonie Van Leeuwenhoek 113:1–12. https://doi.org/10.1007/s10482-019-01354-9
Fan P, Chen D, He Y et al (2016) Alleviating salt stress in tomato seedlings using Arthrobacter and Bacillus megaterium isolated from the rhizosphere of wild plants grown on saline–alkaline lands. Int J Phytoremediation 18:1113–1121. https://doi.org/10.1080/15226514.2016.1183583
Feki K, Tounsi S, Brini F (2018) Comparison of an antioxidant system in tolerant and susceptible wheat seedlings in response to salt stress. Span J Agric Res 15:e0805. https://doi.org/10.5424/sjar/2017154-11507
Gaspar T, Xhaufflaire A (1966) Effect of kinetin on growth, auxin catabolism, peroxidase and catalase activities. Planta 72:252–257. https://doi.org/10.1007/BF00386751
Geddie JL, Sutherland IW (1993) Uptake of metals by bacterial polysaccharides. J Appl Bacteriol 74:467–472. https://doi.org/10.1111/j.1365-2672.1993.tb05155.x
Han Q-Q, Lü X-P, Bai J-P et al (2014) Beneficial soil bacterium Bacillus subtilis (GB03) augments salt tolerance of white clover. Front Plant Sci. https://doi.org/10.3389/fpls.2014.00525
Hariprasad P, Niranjana SR (2009) Isolation and characterization of phosphate solubilizing rhizobacteria to improve plant health of tomato. Plant Soil 316:13–24. https://doi.org/10.1007/s11104-008-9754-6
Hashem A, Abd_Allah EF, Alqarawi AA, et al (2016) Induction of Osmoregulation and Modulation of Salt Stress in Acacia gerrardii Benth. by Arbuscular Mycorrhizal Fungi and Bacillus subtilis (BERA 71). In: BioMed Res. Int. https://www.hindawi.com/journals/bmri/2016/6294098/. Accessed 18 May 2020
Hayat R, Ali S, Amara U et al (2010) Soil beneficial bacteria and their role in plant growth promotion: a review. Ann Microbiol 60:579–598. https://doi.org/10.1007/s13213-010-0117-1
Hu L, Huang Z, Liu S, Fu J (2012) Growth response and gene expression in antioxidant-related enzymes in two bermudagrass genotypes differing in salt tolerance. J Am Soc Hortic Sci 137(3):134–143
Jacobsen S-E, Jensen CR, Liu F (2012) Improving crop production in the arid Mediterranean climate. Field Crops Res 128:34–47. https://doi.org/10.1016/j.fcr.2011.12.001
Jamil A, Riaz S, Ashraf M, Foolad MR (2011) Gene expression profiling of plants under salt stress. Crit Rev Plant Sci 30:435–458. https://doi.org/10.1080/07352689.2011.605739
Kamran M, Parveen A, Ahmar S et al (2020) An overview of hazardous impacts of soil salinity in crops, tolerance mechanisms, and amelioration through selenium supplementation. Int J Mol Sci 21:148. https://doi.org/10.3390/ijms21010148
Kumar P, Sharma PK (2020) Soil salinity and food security in India. Front Sustain Food Syst. https://doi.org/10.3389/fsufs.2020.533781
Kumar A, Verma JP (2018) Does plant—microbe interaction confer stress tolerance in plants: a review? Microbiol Res 207:41–52. https://doi.org/10.1016/j.micres.2017.11.004
Lata C, Jha S, Dixit V et al (2011) Differential antioxidative responses to dehydration-induced oxidative stress in core set of foxtail millet cultivars [Setaria italica (L.)]. Protoplasma 248:817–828. https://doi.org/10.1007/s00709-010-0257-y
Lovelli S, Scopa A, Perniola M et al (2012) Abscisic acid root and leaf concentration in relation to biomass partitioning in salinized tomato plants. J Plant Physiol 169:226–233. https://doi.org/10.1016/j.jplph.2011.09.009
Madhava Rao KV, Sresty TVS (2000) Antioxidative parameters in the seedlings of pigeonpea (Cajanus cajan (L.) Millspaugh) in response to Zn and Ni stresses. Plant Sci 157:113–128. https://doi.org/10.1016/S0168-9452(00)00273-9
Masmoudi F, Abdelmalek N, Tounsi S et al (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
Mendis HC, Thomas VP, Schwientek P et al (2018) Strain-specific quantification of root colonization by plant growth promoting rhizobacteria Bacillus firmus I-1582 and Bacillus amyloliquefaciens QST713 in non-sterile soil and field conditions. PLoS ONE 13:e0193119. https://doi.org/10.1371/journal.pone.0193119
Metwali EMR, Abdelmoneim TS, Bakheit MA, Kadasa NMS (2015) Alleviation of salinity stress in faba bean (Vicia faba L.) plants by inoculation with plant growth promoting rhizobacteria (PGPR). Plant Omics 8(5):449
Mohamed HI, Gomaa EZ (2012) Effect of plant growth promoting Bacillus subtilis and Pseudomonas fluorescens on growth and pigment composition of radish plants (Raphanus sativus) under NaCl stress. Photosynthetica 50:263–272. https://doi.org/10.1007/s11099-012-0032-8
Numan M, Bashir S, Khan Y et al (2018) Plant growth promoting bacteria as an alternative strategy for salt tolerance in plants: a review. Microbiol Res 209:21–32. https://doi.org/10.1016/j.micres.2018.02.003
Parida AK, Das AB (2005) Salt tolerance and salinity effects on plants: a review. Ecotoxicol Environ Saf 60:324–349. https://doi.org/10.1016/j.ecoenv.2004.06.010
Paulitz TC, Bélanger RR (2001) Biological control in greenhouse systems. Annu Rev Phytopathol 39:103–133. https://doi.org/10.1146/annurev.phyto.39.1.103
Ramadoss D, Lakkineni VK, Bose P et al (2013) Mitigation of salt stress in wheat seedlings by halotolerant bacteria isolated from saline habitats. Springerplus 2:6. https://doi.org/10.1186/2193-1801-2-6
Rigaud J, Puppo A (1975) Indole-3-acetic acid catabolism by soybean bacteroids. J Gen Microbiol 88:223–228. https://doi.org/10.1099/00221287-88-2-223
Rodríguez H, Fraga R, Gonzalez T, Bashan Y (2006) Genetics of phosphate solubilization and its potential applications for improving plant growth-promoting bacteria. Plant Soil 287:15–21. https://doi.org/10.1007/s11104-006-9056-9
Rojas-Solis D, Vences-Guzmán MÁ, Sohlenkamp C, Santoyo G (2020) Antifungal and plant growth-promoting Bacillus under saline stress modify their membrane composition. J Soil Sci Plant Nutr. https://doi.org/10.1007/s42729-020-00246-6
Ruiz-Lozano JM, Porcel R, Azcón C, Aroca R (2012) Regulation by arbuscular mycorrhizae of the integrated physiological response to salinity in plants: new challenges in physiological and molecular studies. J Exp Bot 63:4033–4044. https://doi.org/10.1093/jxb/ers126
Saadallah K, Drevon J-J, Abdelly C (2001) Nodulation et croissance nodulaire chez le haricot (Phaseolus vulgaris ) sous contrainte saline. Agronomie 21:627–634. https://doi.org/10.1051/agro:2001154
Saravanakumar D, Samiyappan R (2007) ACC deaminase from Pseudomonas fluorescens mediated saline resistance in groundnut (Arachis hypogea) plants. J Appl Microbiol 102:1283–1292. https://doi.org/10.1111/j.1365-2672.2006.03179.x
See-Too W-S, Convey P, Pearce DA et al (2016) Complete genome of Planococcus rifietoensis M8T, a halotolerant and potentially plant growth promoting bacterium. J Biotechnol 221:114–115. https://doi.org/10.1016/j.jbiotec.2016.01.026
Shrivastava P, Kumar R (2015) Soil salinity: a serious environmental issue and plant growth promoting bacteria as one of the tools for its alleviation. Saudi J Biol Sci 22:123–131. https://doi.org/10.1016/j.sjbs.2014.12.001
Singh RP, Jha PN (2017) Analysis of fatty acid composition of PGPR Klebsiella sp. SBP-8 and its role in ameliorating salt stress in wheat. Symbiosis 73:213–222. https://doi.org/10.1007/s13199-017-0477-4
Sinha AK (1972) Colorimetric assay of catalase. Anal Biochem 47:389–394. https://doi.org/10.1016/0003-2697(72)90132-7
Spaepen S, Bossuyt S, Engelen K et al (2014) Phenotypical and molecular responses of Arabidopsis thaliana roots as a result of inoculation with the auxin-producing bacterium Azospirillum brasilense. New Phytol 201:850–861. https://doi.org/10.1111/nph.12590
Swain MR, Ray RC, Nautiyal CS (2008) Biocontrol efficacy of Bacillus subtilis strains isolated from cow dung against postharvest Yam (Dioscorea rotundata L.) pathogens. Curr Microbiol 57:407–411. https://doi.org/10.1007/s00284-008-9213-x
Tariq M, Noman M, Ahmed T et al (2017) Antagonistic features displayed by Plant Growth Promoting Rhizobacteria (PGPR): a review. J Plant Sci Phytopathol. https://doi.org/10.29328/journal.jpsp.1001004
Teather RM, Wood PJ (1982) Use of congo red-polysaccharide interactions in enumeration and characterization of cellulolytic bacteria from the bovine rument. Appl Env Microbiol 43(4):777–780
Tiwari S, Lata C, Chauhan PS, Nautiyal CS (2016) Pseudomonas putida attunes morphophysiological, biochemical and molecular responses in Cicer arietinum L. during drought stress and recovery. Plant Physiol Biochem 99:108–117. https://doi.org/10.1016/j.plaphy.2015.11.001
van den Berg DJC, Smits A, Pot B et al (1993) Isolation, screening and identification of lactic acid bacteria from traditional food fermentation processes and culture collections. Food Biotechnol 7:189–205. https://doi.org/10.1080/08905439309549857
Velikova V, Yordanov I, Edreva A (2000) Oxidative stress and some antioxidant systems in acid rain-treated bean plants. Plant Sci 151:59–66. https://doi.org/10.1016/S0168-9452(99)00197-1
Vessey JK (2003) Plant growth promoting rhizobacteria as biofertilizers. Plant Soil 255:571–586. https://doi.org/10.1023/A:1026037216893
Wang W, Vinocur B, Altman A (2003) Plant responses to drought, salinity and extreme temperatures: towards genetic engineering for stress tolerance. Planta 218:1–14. https://doi.org/10.1007/s00425-003-1105-5
Wellburn AR (1994) The spectral determination of chlorophylls a and b, as well as total carotenoids, using various solvents with spectrophotometers of different resolution. J Plant Physiol 144:307–313
Wen Z, Duan T, Christensen MJ, Nan Z (2015) Bacillus subtilis subsp. spizizenii MB29 controls alfalfa root rot caused by Fusarium semitectum. Biocontrol Sci Technol 25:898–910. https://doi.org/10.1080/09583157.2015.1020759
Xiong L, Zhu J-K (2002) Molecular and genetic aspects of plant responses to osmotic stress. Plant Cell Environ 25:131–139. https://doi.org/10.1046/j.1365-3040.2002.00782.x
Xiong Y-W, Li X-W, Wang T-T et al (2020) Root exudates-driven rhizosphere recruitment of the plant growth-promoting rhizobacterium Bacillus flexus KLBMP 4941 and its growth-promoting effect on the coastal halophyte Limonium sinense under salt stress. Ecotoxicol Environ Saf 194:110374. https://doi.org/10.1016/j.ecoenv.2020.110374
Acknowledgements
The authors would like to thank Heather Walker for her technical expertise in genome sequencing. This research was supported in part by the U.S. Department of Agriculture, Agricultural Research Service. Any opinions, findings, conclusions, or recommendations expressed in this publication are those of the author(s) and do not necessarily reflect the view of the U.S. Department of Agriculture. The mention of firm names or trade products does not imply that they are endorsed or recommended by the USDA over other firms or similar products not mentioned. USDA is an equal opportunity provider and employer.
Funding
This work was supported by grants from the Tunisian Ministry of Higher Education and Scientific Research. The authors declare that they have no conflict of interests regarding the present study.
Author information
Authors and Affiliations
Contributions
FM conceived and designed the work with guidance from MT and ST, FM carried out all the experiments and analysed the data with MT, FM wrote the manuscript along with CAD, MT and ST supervised the project and provided intellectual input and the overall intellectual context. All authors reviewed the manuscript.
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interests regarding the present study.
Ethics approval and consent to participate
The authors declare no ethical conflicts; authors declare that they have consented to participate in the manuscript and publish it.
Additional information
Communicated by Prakash Lakshmanan.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Masmoudi, F., Tounsi, S., Dunlap, C.A. et al. Halotolerant Bacillus spizizenii FMH45 promoting growth, physiological, and antioxidant parameters of tomato plants exposed to salt stress. Plant Cell Rep 40, 1199–1213 (2021). https://doi.org/10.1007/s00299-021-02702-8
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00299-021-02702-8