Abstract
Plant growth-promoting rhizobacteria (PGPR) are known for growth promotion and mitigating environmental stresses. Here, we examined the propitiousness of three indigenous salt-tolerant PGPR, i.e., Bacillus subtilis (NBRI 28B), B. subtilis (NBRI 33 N), and B. safensis (NBRI 12 M) for plant growth promotion and salt stress amelioration in Zea mays. Results of the in vitro plant growth-promoting attribute revealed NBRI 12 M demonstrated the highest values at 1 M salt (NaCl) concentration. Furthermore, the greenhouse experiment using three Bacillus strains confirmed plant growth-promoting and salt stress-ameliorating ability, through colonizing successfully and mitigating the adverse effects of ethylene by modulating 1-aminocyclopropane-1-carboxylic acid (ACC) accumulation, ACC-oxidase (ACO), and ACC-synthase (ACS) activities under salt stress. Bacillus sp. inoculation has also induced plant response for defense enzymes, chlorophyll, proline and soluble sugar under salt stress. Among three Bacillus strains, NBRI 12 M not only demonstrated higher values for plant growth-promoting (PGP) attributes but also the same was observed in the greenhouse experiment. Thus, the outcomes of this comparative study represent for the first time that salt-tolerant Bacillus strains exhibiting multiple PGP attributes under salt stress along with high rhizosphere competence can alleviate salt stress by reducing the stress ethylene level in the host plant.
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Abiala MA, Odebode AC, Hsu SF, Blackwood CB (2015) Phytobeneficial properties of bacteria isolated from the rhizosphere of maize in southwestern Nigerian soils. Appl Environ Microbiol 81:4736–4743
Aebi H (1984) Catalase in vitro. Methods Enzymol 105:121–126
Arnon DI (1949) Copper enzymes in isolated chloroplasts. Polyphenoloxidase in Beta vulgaris. Plant Physiol 24:1–15
Ashraf M, Hasnain S, Berge O, Mahmood T (2004) Inoculating wheat seedlings with exopolysaccharide-producing bacteria restricts sodium uptake and stimulates plant growth under salt stress. Biol Fertil Soils 40:157–162
Bal HB, Nayak L, Das S, Adhya TK (2012) Isolation of ACC deaminase producing PGPR from rice rhizosphere and evaluating their plant growth-promoting activity under salt Stress. Plant Soil 355:1011–1014
Bates LS, Waldren RP, Teare ID (1973) Rapid determination of free proline for water-stress studies. Plant Soil 39:205–207
Beauchamp C, Fridovich I (1971) Superoxide dismutase: improved assays and an assay applicable to acrylamide gels. Anal Biochem 44:276–287
Bric JM, Bostock RM, Silverstone SE (1991) Rapid in situ assay for indole acetic acid production by bacteria immobilized on a nitrocellulose membrane. Appl Environ Microbiol 57:535–538
Chakraborty U, Chakraborty BN, Chakraborty AP, Dey PL (2013) Water stress amelioration and plant growth promotion in wheat plants by osmotic stress tolerant bacteria. World J Microbiol Biotechnol 29:789–803
Chauhan PS, Nautiyal CS (2010) The purB gene controls rhizosphere colonization by Pantoea agglomerans. Lett Appl Microbiol 50(2):205–210
Chen D, Ma X, Li C, Zhang W, Xia G, Wang M (2014) A wheat aminocyclopropane-1-carboxylate oxidase gene, TaACO1, negatively regulates salinity stress in Arabidopsis thaliana. Plant Cell Rep 33:1815–1827
Choudhary DK, Kasotia A, Jain S, Vaishnav A, Kumari S, Sharma KP, Varma A (2016) Bacterial-mediated tolerance and resistance to plants under abiotic and biotic stresses. J Plant Growth Regul 35:276–300
Curá JA, Franz DR, Filosofía JE, Balestrasse KB, Burgueño LE (2017) Inoculation with Azospirillum sp. and Herbaspirillum sp. bacteria increases the tolerance of maize to drought stress. Microorganisms 5:1–16
Dodd IC, Perez-Alfocea F (2012) Microbial amelioration of crop salinity stress. J Exp Bot 63:3415–3428
Douriet-Gámez NR, Maldonado-Mendoza IE, Ibarra-Laclette E, Blom J, Calderón-Vázquez CL (2018) Genomic analysis of Bacillus sp. strain B25, a biocontrol agent of maize pathogen Fusarium verticillioides. Curr Microbiol 75:247–255
DuBois M, Gilles KA, Hamilton JK, Rebers PA, Smith F (1956) Colorimetric method for determination of sugars and related substances. Anal Chem 28:350–356
Dubois M, Broeck LV, Inzé D (2018) The pivotal role of ethylene in plant growth. Trends Plant Sci 23:311–323
Etesami H, Beattie GA (2018) Mining halophytes for plant growth promoting halotolerant bacteria to enhance the salinity tolerance of non-halophytic crops. Front Microbiol 9:148
Fukami J, Cerezini P, Hungria M (2018) Azospirillum: benefits that go far beyond biological nitrogen fixation. AMB Express 8:73
Glick BR (2014) Bacteria with ACC deaminase can promote plant growth and help to feed the world. Microbiol Res 169:30–39
Goswami D, Dhandhukia P, Patel P, Thakker JN (2014) Screening of PGPR from saline desert of Kutch: growth promotion in Arachis hypogea by Bacillus licheniformis A2. Microbiol Res 169:66–75
Gothwal RK, Nigam VK, Mohan MK, Saamal D, Gosh P (2007) Screening of nitrogen fixer from rhizospheric bacterial isolates associated with important desert plants. AEER 6:101–109
Gouda S, Kerry RG, Das G, Paramithiotis S, Shin S, Patra JK (2018) Revitalization of plant growth promoting rhizobacteria for sustainable development in agriculture. Microbiol Res 206:131–140
Habib SH, Kausar H, Saud HM (2016) Plant growth-promoting rhizobacteria enhance salinity stress tolerance in okra through ROS-scavenging enzymes. Biomed Res Int 2016:6284547
Hemeda HM, Klein BP (1990) Effects of naturally occurring antioxidants on peroxidase activity of vegetable extracts. J Food Sci 55:184–185
Kang SM, Khan AL, Waqas M, You Y, Kim J, Kim J, Hamayun M, Lee I (2014) Plant growth promoting rhizobacteria reduce adverse effects of salinity and osmotic stress by regulating phytohormones and antioxidants in Cucumis sativus. J Plant Interact 9:673–682
Kang SM, Radhakrishnan R, Lee KE, You YH, Ko JH, Kim JH, Lee IJ (2015) Mechanism of plant growth promotion elicited by Bacillus sp. LKE15 in oriental melon. Acta Agric Scand Sect B Soil Plant Sci 65:637–647
Khan A, Sirajuddin ZXQ, Javed MT, Khan KS, Bano A, Shen RF, Masood S (2016) Bacillus pumilus, enhances tolerance in rice (Oryza sativa, L.) to combined stresses of NaCl and high boron due to limited uptake of Na+. Environ Exp Bot 124:120–129
Kukreja S, Nandwal A, Kumar N, Sharma S, Unvi V, Sharma P (2005) Plant water status, H2O2 scavenging enzymes, ethylene evolution and membrane integrity of Cicer arietinum roots as affected by salinity. Biol Plant 49:305–308
Laditi MA, Nwoke OC, Jemo M, Abaidoo RC, Ogunjobi AA (2012) Evaluation of microbial inoculants as biofertilizers for the improvement of growth and yield of soybean and maize crops in savanna soils. Afr J Agric Res 7:405–413
Lata S (2019) Measurement of agricultural productivity and water productivity of crops. In: Nusser M (ed) Irrigation water management for agricultural development in Uttar Pradesh, India. Advances in Asian human-environmental research. Springer, Berlin, https://doi.org/10.1007/978-3-030-00952-6_6
Lei P, Xu Z, Liang J, Luo X, Zhang Y, Feng X (2016) Poly (γ-glutamic acid) enhanced tolerance to salt stress by promoting proline accumulation in Brassica napus L. Plant Growth Regul 78:233
Li HQ, Jiang XW (2017) Inoculation with plant growth-promoting bacteria (PGPB) improves salt tolerance of maize seedling. Russ J Plant Physiol 64:235–241
Li J, Xu H, Liu W, Zhang X, Lu Y (2015) Ethylene inhibits root elongation during alkaline stress through AUXIN1 and associated changes in auxin accumulation. Plant Physiol 168:1777–1791
Madhaiyan M, Poonguzhali S, Ryu J, Sa T (2006) Regulation of ethylene levels in canola (Brassica campestris) by 1-aminocyclopropane-1-carboxylate deaminase-containing Methylobacterium fujisawaense. Planta 224:268–278
Madhaiyan M, Poonguzhali S, Sa T (2007) Characterization of 1-aminocyclopropane- 1-carboxylate (ACC) deaminase containing Methylobacterium oryzae and interactions with auxins and ACC regulation of ethylene in canola (Brassica campestris). Planta 226:867–876
Mendis HC, Thomas VP, Schwientek P, Salamzade R, Chien JT, Waidyarathne P, Kloepper J, De La Fuente L (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 13:2
Mishra A, Chauhan PS, Chaudhry V, Tripathi M, Nautiyal CS (2011) Rhizosphere competent Pantoea agglomerans enhances maize (Zea mays) and chickpea (Cicer arietinum L.) growth, without altering the rhizosphere functional diversity. Antonie Van Leeuwenhoek 100:405–413
Mishra S, Mishra A, Chauhan PS, Mishra SK, Kumari M, Niranjan A, Nautiyal CS (2012) Pseudomonas putida NBRIC19 dihydrolipoamide succinyltransferase (SucB) gene controls degradation of toxic allelochemicals produced by Parthenium hysterophorus. J Appl Microbiol 112:793–808
Mishra SK, Khan MH, Misra S, Kant VK, Khare P, Srivastava S, Chauhan PS (2017) Characterization of Pseudomonas spp. and Ochrobactrum sp. isolated from volcanic soil. Antonie Van Leeuwenhoek 110:253–270
Misra S, Dixit VK, Khan MH, Mishra SK, Dviwedi G, Yadav S, Lehri A, Chauhan PS (2017) Exploitation of agro-climatic environment for selection of 1-aminocyclopropane-1-carboxylic acid (ACC) deaminase producing salt-tolerant indigenous plant growth promoting rhizobacteria. Microbiol Res 205:25–34
Misra S, Dixit VK, Mishra SK, Chauhan PS (2019) Demonstrating the potential of abiotic stress-tolerant Jeotgalicoccus huakuii NBRI 13E for plant growth promotion and salt stress amelioration. Ann Microbiol 69:419–434
Nakano Y, Asada K (1981) Hydrogen peroxide is scavenged by ascorbate-specific peroxidase in Spinach chloroplasts. Plant Cell Physiol 22:867–880
Nautiyal CS (1997) A method for selection and characterization of rhizosphere-competent bacteria of chickpea. Curr Microbiol 34:12–17
Nautiyal CS (1999) An efficient microbiological growth medium for screening phosphate solubilizing microorganisms. FEMS Microbiol Lett 170:265–270
Nautiyal CS, Srivastava S, Chauhan PS, Seem K, Mishra A, Sopory SK (2013) Plant growth-promoting bacteria Bacillus amyloliquefaciens NBRISN13 modulates gene expression profile of leaf and rhizosphere community in rice during salt stress. Plant Physiol Biochem 66:1–9
Panta S, Flowers TJ, Lane P, Doyle R, Haros G, Shabala S (2014) Halophyte agriculture: success stories. Environ Exp Bot 107:71–83
Patra HK, Mishra M (1979) Pyrophosphatase, peroxidase and polyphenol oxidase activities during leaf development and senescence. Plant Physiol 63:318–323
Peng Z, He S, Gong W, Sun J, Pan Z, Xu F, Lu Y, Du X (2014) Comprehensive analysis of differentially expressed genes and transcriptional regulation induced by salt stress in two contrasting cotton genotypes. BMC Genomics 15:760
Penrose DM, Glick BR (2003) Methods for isolating and characterizing ACC deaminase containing plant growth promoting rhizobacteria. Physiol Plant 118:10–15
Radhakrishnan R, Hashem A, Abd-Allah EF, (2017) Bacillus: a biological tool for crop improvement through bio-molecular changes in adverse environments. Front Physiol 8:667
Redmile-Gordon MA, Brookes PC, Evershed RP, Goulding KWT, Hirsch PR (2014) Measuring the soil-microbial interface: extraction of extracellular polymeric substances (EPS) from soil biofilms. Soil Biol Biochem 72:163–171
Sarkar J, Chakraborty B, Chakraborty UJ (2018) Plant growth promoting rhizobacteria protect wheat plants against temperature stress through antioxidant signalling and reducing chloroplast and membrane injury. Plant Growth Regul 37:1396
Siddikee MA, Glick BR, Chauhan PS, Yim WJ, Sa T (2011) Enhancement of growth and salt tolerance of red pepper seedlings (Capsicum annuum L.) by regulating stress ethylene synthesis with halotolerant bacteria containing 1-aminocyclopropane-1-carboxylic acid deaminase activity. Plant Physiol Biochem 49:427–434
Siddikee MA, Chauhan PS, Sa T (2012) Regulation of ethylene biosynthesis under salt stress in red pepper (Capsicum annuum L.) by 1-aminocyclopropane- 1-carboxylic acid (ACC) deaminase-producing halotolerant bacteria. J Plant Growth Regul 31:265–272
Singh RP, Jha PN (2016) The multifarious PGPR Serratia marcescens CDP-13 augments induced systemic resistance and enhanced salinity tolerance of wheat (Triticum aestivum L.). PLoS ONE 11:e0155026
Srivastava S, Yadav A, Seem K, Mishra S, Chaudhary V, Nautiyal CS (2008) Effect of high temperature on Pseudomonas putida NBRI0987 biofilm formation and expression of stress sigma factor RpoS. Curr Microbiol 56:453–457
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 69:484–494
Titus S, Gasnkar N, Srivastava KB, Karande AA (1995) Exopolymer production by a fouling marine bacterium Pseudomonas alcaligenes. Indian J Mar Sci 24:45–48
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
Ullah S, Bano A (2015) Isolation of plant-growth-promoting rhizobacteria from rhizospheric soil of halophytes and their impact on maize (Zea mays L.) under induced soil salinity. Can J Microbiol 61:307–313
Upadhyay SK, Singh JS, Singh DP (2011) Exopolysaccharide-producing plant growth-promoting rhizobacteria under salinity condition. Pedosphere 21:214–222
Vardharajula S, Ali SZ, Grover M, Reddy G, Bandi V (2011) Drought tolerant plant growth promoting Bacillus spp: effect on growth, osmolytes, and antioxidant status of maize under drought stress. J Plant Interact 6:1–14
Verma M, Mishra J, Arora NK (2019) Plant growth-promoting rhizobacteria: diversity and applications. In: Sobti R, Arora N, Kothari R (eds) Environmental biotechnology: for sustainable future. Springer, Singapore, https://doi.org/10.1007/978-981-10-7284-0_6
Vurukonda SSKP, Vardharajula S, Shrivastava M, Ali SKZ (2016) Enhancement of drought stress tolerance in crops by plant growth promoting rhizobacteria. Microbiol Res 184:13–24
Wang W, Wu Z, He Y, Huang Y, Li X, Ye B (2018) Plant growth promotion and alleviation of salinity stress in Capsicum annuum L. by Bacillus isolated from saline soil in Xinjiang. Ecotoxicol Environ Saf 164:520–529
Yim WJ, Sundaram S, Kim KY, Lee G, Sa T (2013) Ethylene emission and PR protein synthesis in ACC deaminase producing Methylobacterium spp. inoculated tomato plants (Lycopersicon esculentum Mill.) challenged with Ralstonia solanacearum under greenhouse conditions. Plant Physiol Biochem 67:95–104
Yim WJ, Kim KY, Lee YW, Sundaram SP, Lee Y, Sa T (2014) Real time expression of ACC oxidase and PR-protein genes mediated by Methylobacterium spp. in tomato plants challenged with Xanthomonas campestris pv. Vesicatoria. J Plant Physiol 171:1064–1075
Zörb C, Geilfus CM, Dietz KJ (2018) Salinity and crop yield. Plant Biol 21:31–38
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The authors acknowledge the Director, CSIR National Botanical Research Institute for providing facilities and support during the study.
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The authors acknowledge the financial assistance from the CSIR Network project MLP022 and In-house project OLP105.
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PSC conceived and co-ordinated the research. SM conducted experiments and analyzed the data. PSC and SM wrote the manuscript. Both authors read and approved the manuscript.
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Misra, S., Chauhan, P.S. ACC deaminase-producing rhizosphere competent Bacillus spp. mitigate salt stress and promote Zea mays growth by modulating ethylene metabolism. 3 Biotech 10, 119 (2020). https://doi.org/10.1007/s13205-020-2104-y
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DOI: https://doi.org/10.1007/s13205-020-2104-y