Abstract
Agricultural practice is moving toward for more sustainable and eco-friendly approaches. The current work aims to predict the effectiveness of the bacterial cells species Virgibacillus marismortui strain M3-23 and Salinococcus roseus strain M2-15 on Tomato Plant Growth Promotion. The results highlighted that both bacterial species were able to plant growth promotion and development by providing direct and indirect mechanisms including, Auxin, siderophores, antibiosis, lytic enzymes production, in vitro on MS agar plates and in semi-sterile conditions in soilless system. Furthermore, the singly bacterial inoculation strain M3-23 and strain M2-15 tested at 107CFU/mL showed significant improvement of the shoot length, root length, leaf area, chlorophyll contents, water contents, tannin, polyphenols, and flavonoids contents, and antioxidant activity on tomato plant compared to control, un-inoculated plants. Multifactorial analysis, illustrated a correlation between the morphological, and physiological parameters and bacterial treatments. Overall, the strain M3-23 of V marismortui gave the best enhancement of biochemical, physiological and morphological parameters plant’s as compared to the strain M2-15 of S roseus and the control, untreated plants.
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References
Ahmed A, Hasnain S (2010) Auxin producing Bacillus spp, auxin quantification and effect on the growth of Solanum tuberosum. Pure Appl Chem 82(1):313–319. https://doi.org/10.1351/PAC-CON-09-02-06
Ben Hmed M, Rigane G, Ben Salem R et al (2020) Phytochemical and antioxidant activities of schinus molle L. extract. Revue Romaine De Chimie 65(2):173–178. https://doi.org/10.33224/rrch.2020.65.2.01
Berendsen RL, Pierterse CMJ, Bakker PA (2012) The rhizosphere microbiome and plant health. Trends Plant Sci 17:487–186. https://doi.org/10.1016/j.tplants.2012.04.001
Bolivar-Anillo HJ, Gonzalez-Rodriguez VE, Cantoral JM, Garcia-Sanchez D, Collado IG, Garrido C (2021) Endophytic bacteria Bacillus subtilis, isolated from Zea mays, as potential biocontrol agent against Botrytis cinerea. Biology 10:492. https://doi.org/10.3390/biology10060492
Breedt G, Labuschagne N, Coutinho TA (2017) Seed treatment with selected plant growth-promoting rhizobacteria increases maize yield in the field. Ann Appl Biol 171(2):229–236. https://doi.org/10.1111/aab.12366
Cakmakci R, Donnez A, Aydin A et al (2006) Growth promotion of plants by plant growth-promoting rhizobacteria under greenhouse and two different filed soil conditions. Soil Biol Biochem 38(6):1482–1487. https://doi.org/10.1016/j.soilbio.2005.09.019
Carlson R, Tugizimana F, Steenkamp PA, Dubery IA, Labuschagne N (2019) Differential Metabolitic reprogramming in Paenibacillus alvei primed Sorghum bicolor Seedlings in response to Fusarium pseudograminearum infection. Metabolites 23 9(7):150. https://doi.org/10.3390/metabo9070150
Chammam A, Sanguin H, Bellvert F et al (2013) Plant secondary metabolite profiling evidences strain-dependent effect in the Azospirillium-Oryza sativa association. Phytochemistry 87:65–77. https://doi.org/10.1016/j.phytochem.2012.11.009. Epub 2012 Dec 22.
Chea L, Pfeiffer B, Schneider D, Daniel R, Pawelzik E, Naumann M (2021) Morphological and metabolite responses of Potaoes under various Phosphorus levels and their amelioration by Pant Growth Promoting Rhizobacteria. Int J Mol Sci 13(10):5162. https://doi.org/10.3390/ijms22105162
Claus O, Wilke (2019) Fundamentals of Data Visualization: A Primer on Making Informative and Compelling Figures. O’Reilly Media, Inc. California. https://doi.org/10.5038/1936-4660.12.2.18
Essghaier B (2014) Dhieb C, Rebib H, Antimicrobial behavior of intracellular proteins from two moderately halophilic bacteria: strain J31 of Terribacillus halophilus and strain M3-23 of Virgibacillus marismortui. Plant pathology and microbiology 5(1): 1000214.https://doi.org/10.4172/2157-7471.1000214
Essghaier B, Fardeau ML, Cayol JL et al (2009) Biological control of grey mould in strawberry fruits by halophilic bacteria. J Appl Microbiol 106:833–846. https://doi.org/10.1111/j.1365-2672.2008.04053.x
Essghaier B, Rezgui A, Rebib H et al (2017) The ability of halophilic bacteria to induce resistance in tomato plant infected by stem cancer under greenhouse conditions. Mycopath 15 (1):13–21. http://111.68.103.26/…/611
Essghaier B, Zouaoui M, Najjari A et al (2021) Potentialities and characterization of an antifungal chitinase produced by a halotolerant. Bacillus licheniformis Current microbiology 78(3):1–9. https://doi.org/10.1007/s00284-020-02329-0
Etesami H, Gwyn A, Beattie (2018) Mining halophytes for plant growth promoting halotolerant bacteria to enhance the salinity tolerance of non-halophilic crops. Front Microbiol 9:148. https://doi.org/10.3389/fmicb.2018.00148
Gay AP, Hunk B (1994) Acclimation of Lolium temelentum to enhanced carbon dioxide concentration. J Exp Bot 45:1133–1141
Ghazghazi H, Essghaier B, Riguene H, Rigane G, Elaloui M, Oueslati M, Naser BsalemR, Khouja Z (2019) MA Phytochemical analysis, antioxidant and antimicrobial activities of eucalyptus essential oil: comparative study between eucalyptus marginata and eucalyptus paucilora. Rev. Roum.Chim 64(12):1055–1062. https://doi.org/10.33224/rrch.2019.64.12.05
Gharsallah C, Fakhfakh H, Grubb D, Gorsane F (2016) Effect of salt stress on into concentration, proline content, antioxidant enzyme activities and gene expression in tomato cultivars. AoB PLANTS8/PLW055. https://doi.org/10.1093/aobpla/plw055
Gharsallah C, Gharsallh Chouchane S, Werghi S, Mehrez M, Fakhfakh H, Gorsane F (2020) Tomato contrasting genotypes responses under combined salinity and viral stresses. Physiol Mol Biol Plants 26(7):1411–1424. https://doi.org/10.1007/s12298-020-00835-w
Glick BR, Cheng Z, Czarny J et al (2007) Promotion of plant growth by ACC deaminase-producing soil bacteria. Eur J Plant Pathol 119:329–339. https://doi.org/10.1080/07352680701572966
Gordon SA, Weber RP (1951) Colorimetric estimation of indole acetic acid. Plant Physiol 26(1):192–195. https://doi.org/10.1104/pp.26.1.192
Goswami D, Dhandhukia P, Patel P et al (2014) Screening of PGPR from saline desert of Kutch: growth promotion in Arachis hypogea by Bacillus licheniformis A2. Microbiol Res 169:66–75. https://doi.org/10.1016/j.micres.2013.07.004
Hafiz A, Tahir S, Qin G et al (2017) Plant growth promotion by volatile organic compounds produced by Bacillus subtilis SYST2. Front Microbiol 8:171. https://doi.org/10.3386/fmicrob.2017.00171
Hussain K, Ashraf M, Ashraf MY (2008) Relationship between growth and ion relation in pearl millet (Pennisetum glaucum L. R. Br.) at different growth stages under salt stress. Afr J Plant Sci 2:23–27
Jha B, Singh VK, Weiss A et al (2015) Zhihengliuella somnathii sp. nov., a halotolerant actinobacterium from the rhizosphere of a halophyte Salicornia brachiata. Int J Syst Evol Microbiol 65:3137–3142. https://doi.org/10.1099/ijsem.0.000391
Khedher O, Rigane G, Ben SR et al (2020) Optimization of polyphenols recovery from Schinus molle L. peel using response surface methodology (RSM). Chem Afr 3:813–820. https://doi.org/10.1007/s42250-020?00170?3
Kim DJ, Lee MW, Choi JS et al (2017) Inhibitory activity of hinokitiol against biofilm formation in fluconazole-resistant Candida species. PLoS ONE 12: (2017) e0171244. https://doi.org/10.1371/journal.pone.0171444
Kumar V, Singh S, Singh J et al (2015) Potential of plant Growth Promoting traits by bacteria isolated from Heavy Metal Contaminated soils. Bull Environ Contam Toxicol 94:807–814. https://doi.org/10.1007/s00128-015-1523-7
Lê S, Josse J, Husson F (2008) FactoMine R: An R Package for Multivariate Analysis. J Stat Softw 25(1):1–18. https://doi.org/10.18637/jss.v025.i01
Mendiburu F, Muhammad Y (2020) Agricolae: Statistical Procedures for Agricultural Research. R package version 1.4.0
Mhlongo MI, Piater LA, Steenkamp PA, Labuschagne N, Dubery IA (2020) Metabolic profiling of PGPR treated Tomato plants reveal priming related adaptations of secondary metabolites and aromatic amino acids. Metabolites 10(5):210. https://doi.org/10.3390/metabo10050210
Monnier N, Furlan A, Buchoux S et al (2019) Exploring the dual interaction of natural rhamnolipids with plant and fungal biomimetic 491plasma membranes through biophysical studies. Int J Mol Sci 20(5):1009. https://doi.org/10.3390/ijms20051009
Mosaddiqur R, Sabir AA, Muka JK et al (2018) Plant probiotic bacteria Bacillus and Paraburkholderia improve growth, yield and content of antioxidants in strawberry fruit. Sci Rep 8:2504. https://doi.org/10.1038/s41598-018-20235-1
Mendiburu T, Skoog F (1962) A revised Medium for rapid growth and bioassays with Tobacco tissus cultures Physiologia Plantarum, 15(3):473–497. https://doi.org/10.1111/j.1399-3054.1962.tb08052.x
Qiao J, Yu X, Liang X et al (2017) Addition of plant growth promoting Bacillus subtilis PTS-394 on tomato rhizosphere has no durable impact on composition of root microbiome. BMC Microbiol 17:131. https://doi.org/10.1186/s12866-017-1039-x
Qin Y, Druzhinina IS, Pan X et al (2016) Microbially mediated plant salt tolerance and microbiome –based solutions for samine agriculture. Biotechnol Adv 34:1245–1259. https://doi.org/10.1016/j.biotechadv.2016.08.005
Ramadoss D, Lakkineni VK, Bose P et al (2013) Mitigation of salt stress in wheat seedlings by halotolerant bacteria isolated from saline habitats. Springer plus 2:1–7. https://doi.org/10.1186/2193-1801-2-6
Rolli E, Marasco R, Vigani G et al (2015) Improved plant resistance to drought is promoted by the root –associated microbiome as a water stress-dependent trait. Environ Microbiol 17:316–331. https://doi.org/10.1111/1462-2920.12439
Rufus J, Akinrinlola, Gary Y, Yuen et al (2018) Evaluation of Bacillus strains for plant growth promotion and predictability of efficacy by in vitro physiological traits. Int J Microbiol 17(2):316–331. https://doi.org/10.1155/2018/568674
Ruppel S, Franken P, Witzel K (2013) Properties of the halophyte microbiome and their implications for plant salt tolerance. Funct Plant Biol 40:940–951. https://doi.org/10.1071/FP12355
Sadeghi A, Karimi E, Dahaji PA et al (2012) Plant growth promoting activity of an auxin and siderophores producing isolate of Streptomyces under saline soil conditions. World J Microbiol Biotechnol 28:1503–1509. https://doi.org/10.1007/s11274-011-0952-7
Sadfi-Zouaoui N, Essghaier B, Hajlaoui MR et al (2008) Ability of moderately halophilic bacteria to control grey mould disease on tomato fruits. J Phytopathol 156:42–52. https://doi.org/10.1111/j.1439-0434.2007.01329.x
Schellenberger R, Crouzet J, Nickzad A et al (2020) The bacterial virulence factors rhamnolipids and their (R)-3-hydroxyalkanoate precursors activate Arabidopsis innate immunity through two independent mechanisms. BioRXiv the preprint server for biology. December 20, 2020. https://doi.org/10.1101/2020.12.18.423392
Sharma S, Kulkarni J, Jha B (2016) Halotolerant rhizobacteria promote growth and enhance salinity tolerance in peanut. Front Microbiol 7:1600. https://doi.org/10.3389/fmicb.2016.01600
Wasti S, Mimouni H, Smiti S, Zid E, BenAhmed H (2012) Enhanced salt tolerance of tomatoes by exogenous salicylic acid applied through rooting medium. OMICS Apr 16(4):200–207. https://doi.org/10.1089/om.2011.0071
Wickham H (2016) ggplot2: Elegant Graphics for Data Analysis. Springer-Verlag, New York
Yahyaoui A, Arfaoui M, Rigane O et al (2019) Investigation on the Chemical Composition and Antioxidant Capacity of Extracts from Crataegus azarolus L.: Effect of Growing Location of an Important Tunisian Medicinal Plant. Chem Afr 2:361)
Zahid M, Abbasi MK, Hameed S et al (2015) Isolation and identification of indigenous plant growth promoting rhizobacteria from Himalayan region of Kachmir and their effect on improving growth and nutrient contents of maize (Zea mays L). Front Microbiol 17(6):207. https://doi.org/10.3389/fmicb.2015.00207
Zameer M, Hina Z, Bushra T et al (2016) PGPR Potentially improve growth of tomato plants in salt –stressed Environment. Turkish J Agric –Food Sci Technol 4(6):455–463
Zhu F, Qu L, Hong X et al (2011) Isolation and characterization of a phosphate-solubilizing halophilic bacterium Kushneria sp YCWA18 from Daqiao Saltern on the coast of Yellow sea of China. Evid Based Complement Alternative Medicine 211:ID615032. https://doi.org/10.1155/2011/6150
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This work was supported by funds from the Ministry of Higher Education and Scientific Research of Tunisia.
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Essghaier, B., Mrah, S., ben Jalloul, A. et al. Ability of Virgibacillus marismortui and Salinococcus roseus for plant growth promotion by evaluating their effect on physiological and morphological parameters in vitro and in soilless system. Biologia 77, 2257–2267 (2022). https://doi.org/10.1007/s11756-022-01061-3
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DOI: https://doi.org/10.1007/s11756-022-01061-3