Abstract
Intensification of sodic soil due to increasing pH is an emerging environmental issue. The present study aimed to isolate and characterise alkaline stress-tolerant and plant growth-promoting bacterial strains from moderately alkaline soil (pH 8–9), strongly alkaline soil (pH 9–10), and very strongly alkaline soil (> 10). Total 68 bacteria were isolated, and screened for multiple plant growth promoting (PGP) attributes. Out of total, 42 isolates demonstrating at least three plant growth promoting PGP traits selected for further assays. Then out of 42, 15 bacterial isolates were selected based on enhanced maize plant growth under greenhouse experiment, and 16S rRNA gene sequencing revealed Bacillus spp. as a dominant genus. Furthermore, based on improved seed germination percentage and biomass of maize (Zea mays L.) under alkaline stress conditions Alcaligenes sp. NBRI NB2.5, Bacillus sp. NBRI YE1.3, and Bacillus sp. NBRI YN4.4 bacterial strains were selected, and evaluated for growth-promotion and alkaline stress amelioration under greenhouse condition. Amongst the selected 3 plant growth promoting rhizobacterial (PGPR) strains, Bacillus sp. NBRI YN4.4 significantly improved the photosynthetic pigments and soluble sugar content, and decreased proline level in inoculated maize plants as compared to uninoculated control under stress conditions. Moreover, significantly enhanced soil enzymes such as dehydrogenase, alkaline phosphatase and betaglucosidase due to inoculation of Bacillus sp. NBRI YN4.4 in maize plants grown in alkaline soil attributes to its role in improving the soil health. Therefore, alkaline stress-tolerant PGPR NBRI YN4.4 can be useful for developing strategies for the reclamation of saline/sodic soils and improving the plant growth and soil health in sustainable manner.
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References
Ahemad M, Kibret M (2014) Mechanisms and applications of plant growth promoting rhizobacteria: current perspective. J King Saud Univ Sci 26(1):1–20. https://doi.org/10.1016/j.jksus.2013.05.001
Ahmad M, Ahmad I, Hilger TH, Nadeem SM, Akhtar MF, Jamil M, Hussain A, Zahir ZA (2018) Preliminary study on phosphate solubilizing Bacillus subtilis strain Q3 and Paenibacillus sp. strain Q6 for improving cotton growth under alkaline conditions. Peer J 6:e5122. https://doi.org/10.7717/peerj.5122
Alef K, Nannipieri P (1995) Methods in applied soil microbiology and biochemistry, 1st edn. Academic Press, London
Ali S, Hameed S, Shahid M, Iqbal M, Lazarovits G, Imran A (2020) Functional characterization of potential PGPR exhibiting broad-spectrum antifungal activity. Microbiol Res 232:126389. https://doi.org/10.1016/j.micres.2019.126389
Backer R, Rokem JS, Ilangumaran G, Lamont J, Praslickova D, Ricci E, Subramanian S, Smith DL (2018) Plant growth-promoting rhizobacteria: context, mechanisms of action, and roadmap to commercialization of biostimulants for sustainable agriculture. Front Plant Sci 9:1473. https://doi.org/10.3389/fpls.2018.01473
Bisht N, Tiwari S, Singh PC, Niranjan A, Chauhan PS (2019) A multifaceted rhizobacterium Paenibacillus lentimorbus alleviates nutrient deficiency-induced stress in Cicer arietinum L. Microbiol Res 223:110–119. https://doi.org/10.1016/j.micres.2019.04.007
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(2):535–538
Bromham L, Saslis-Lagoudakis CH, Bennett TH, Flowers TJ (2013) Soil alkalinity and salt tolerance: adapting to multiple stresses. Biol Lett 9:20130642. https://doi.org/10.1098/rsbl.2013.0642
Bui EN, Thornhill A, Miller JT (2014) Salt-and alkaline-tolerance are linked in Acacia. Biol Lett 10:20140278. https://doi.org/10.1098/rsbl.2014.0278
Cao D, Shi F, Koike T, Lu Z, Sun J (2014) Halophyte plant communities affecting enzyme activity and microbes in saline soils of the Yellow River Delta in China. Clean Soil Air Water 42(10):1433–1440. https://doi.org/10.1002/clen.201300007
Damodaran T, Sah V, Rai RB, Sharma DK, Mishra VK, Jha K, Kannan R (2013) Isolation of salt tolerant endophytic and rhizospheric bacteria by natural selection and screening for promising plant growth-promoting rhizobacteria (PGPR) and growth vigour in tomato under sodic environment. Afr J Microbiol Res 7(44):5082–5089. https://doi.org/10.5897/AJMR2013.6003
Damodaran T, Mishra VK, Jha SK, Pankaj U, Gupta G, Gopal R (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(1):36–43. https://doi.org/10.1007/s40003-018-0343-5
Danish S, Zafar-ul-Hye M (2019) Co-application of ACC-deaminase producing PGPR and timber-waste biochar improves pigments formation, growth and yield of wheat under drought stress. Sci Rep 9(1):5999. https://doi.org/10.1038/s41598-019-42374-9
Delgado-García M, Contreras-Ramos SM, Rodríguez JA, Mateos-Díaz JC, Aguilar CN, Camacho-Ruíz RM (2018) Isolation of halophilic bacteria associated with saline and alkaline-sodic soils by culture dependent approach. Heliyon 4(11):e00954. https://doi.org/10.1016/j.heliyon.2018.e00954
Din BU, Sarfraz S, Xia Y, Kamran MA, Javed MT, Sultan T, Munis MF, Chaudhary HJ (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
Eida AA, Ziegler M, Lafi FF, Michell CT, Voolstra CR, Hirt H, Saad MM (2018) Desert plant bacteria reveal host influence and beneficial plant growth properties. PLoS ONE 13(12):e0208223. https://doi.org/10.1371/journal.pone.0208223
Eivazi F, Tabatabai MA (1977) Phosphatases in soils. Soil Biol Biochem 9:167–172. https://doi.org/10.1016/0038-0717(77)90070-0
Eivazi F, Tabatabai MA (1988) Glucosidases and galactosidases in soils. Soil Biol Biochem 20:601–606. https://doi.org/10.1016/0038-0717(88)90141-1
Esringu A, Kaynar D, Turan M, Ercisli S (2016) Ameliorative effect of humic acid and plant growth-promoting rhizobacteria (PGPR) on Hungarian vetch plants under salinity stress. Commun Soil Sci Plant Anal 47(5):602–618. https://doi.org/10.1080/00103624.2016.1141922
Fukami J, Cerezini P, Hungria M (2018) Azospirillum: benefits that go far beyond biological nitrogen fixation. AMB Exp 8(1):73. https://doi.org/10.1186/s13568-018-0608-1
Gontia-Mishra I, Sapre S, Kachare S, Tiwari S (2017) Molecular diversity of 1-aminocyclopropane-1-carboxylate (ACC) deaminase producing PGPR from wheat (Triticum aestivum L.) rhizosphere. Plant Soil 414(1–2):213–227. https://doi.org/10.1007/s11104-016-3119-3
Islam F, Yasmeen T, Arif MS, Ali S, Ali B, Hameed S, Zhou W (2016) Plant growth promoting bacteria confer salt tolerance in Vigna radiata by up-regulating antioxidant defense and biological soil fertility. Plant Growth Regul 80(1):23–36. https://doi.org/10.1007/s10725-015-0142-y
Kaiser C, Kilburn MR, Clode L, Fuchslueger L, Koranda M, Cliff JB, Solaiman ZM, Murphy DV (2015) Exploring the transfer of recent plant photosynthates to soil microbes: mycorrhizal pathway vs direct root exudation. New Phytol 205(4):1537–1551. https://doi.org/10.1111/nph.13138
Kamjumphol W, Chareonsudjai S, Chareonsudjai P, Wongratanacheewin S, Taweechaisupapong S (2013) Environmental factors affecting Burkholderia pseudomallei biofilm formation. Southeast Asian J Trop Med Public Health 44(1):72–81
Khan N, Bano A, Rahman MA, Guo J, Kang Z, Babar MA (2019) Comparative physiological and metabolic analysis reveals a complex mechanism involved in drought tolerance in chickpea (Cicer arietinum L.) induced by PGPR and PGRs. Sci Rep 9(1):2097. https://doi.org/10.1038/s41598-019-38702-8
Kumar M, Mishra S, Dixit V, Kumar M, Agarwal L, Chauhan PS, Nautiyal CS (2016) Synergistic effect of Pseudomonas putida and Bacillus amyloliquefaciens ameliorates drought stress in chickpea (Cicer arietinum L.). Plant Signal Behav 11(1):e1071004. https://doi.org/10.1080/15592324.2015.1071004
Lal S, Kumar R, Ahmad S, Dixit VK, Berta G (2019) Exploring the survival tactics and plant growth promising traits of root-associated bacterial strains under Cd and Pb stress: a modelling-based approach. Ecotoxicol Environ Saf 170:267–277. https://doi.org/10.1016/j.ecoenv.2018.11.100
Lata C, Jha S, Dixit V, Sreenivasulu N, Prasad M (2011) Differential antioxidative responses to dehydration-induced oxidative stress in core set of foxtail millet cultivars [Setaria italica (L.)]. Protoplasma. 248(4):817–828. https://doi.org/10.1007/s00709-010-0257-y
Lefèvre CT, Frankel RB, Pósfai M, Prozorov T, Bazylinski DA (2011) Isolation of obligately alkaliphilic magnetotactic bacteria from extremely alkaline environments. Environ Microbiol 13(8):2342–2350. https://doi.org/10.1111/j.1462-2920.2011.02505.x
Li HQ, Jiang XW (2017) Inoculation with plant growth-promoting bacteria (PGPB) improves salt tolerance of maize seedling. Russ J Plant Physiol 64(2):235–241. https://doi.org/10.1134/S102144371702007
Li H, Lei P, Pang X, Li S, Xu H, Xu Z, Feng X (2017) Enhanced tolerance to salt stress in canola (Brassica napus L.) seedlings inoculated with the halotolerant Enterobacter cloacae HSNJ4. Appl Soil Ecol 119:26–34. https://doi.org/10.1016/j.apsoil.2017.05.033
Liu X-M, Li Q, Liang WJ, Jiang Y (2008) Distribution of soil enzyme activities and microbial biomass along a latitudinal gradient in farmlands of Songliao Plain Northeast China. Pedosphere 18(4):431–440. https://doi.org/10.1016/S1002-0160(08)60034-X
Liu J, Tang L, Gao H, Zhang M, Guo C (2019) Enhancement of alfalfa yield and quality by plant growth-promoting rhizobacteria under saline-alkali conditions. J Sci Food Agric 99(1):281–289. https://doi.org/10.1002/jsfa.9185
Luna DF, Aguirre A, Pittaro G, Bustos D, Ciacci B, Taleisnik E (2017) Nutrient deficiency and hypoxia as constraints to Panicum coloratum growth in alkaline soils. Grass Forage Sci 72(4):640–653. https://doi.org/10.1111/gfs.12263
Machado R, Serralheiro R (2017) Soil salinity: effect on vegetable crop growth. Management practices to prevent and mitigate soil salinization. Horticulturae 3(2):30. https://doi.org/10.3390/horticulturae3020030
Mehta S, Nautiyal CS (2001) An efficient method for qualitative screening of phosphate-solubilizing bacteria. Curr Microbiol 43(1):51–56. https://doi.org/10.1007/s002840010
Meyer JA, Abdallah MA (1978) The fluorescent pigment of Pseudomonas fluorescens: biosynthesis, purification and physicochemical properties. Microbiology 107(2):319–328. https://doi.org/10.1099/00221287-107-2-319
Mishra SK, Khan MH, Misra S, Dixit VK, Khare P, Srivastava S, Chauhan PS (2017) Characterisation of Pseudomonas spp. and Ochrobactrum sp. isolated from volcanic soil. Antonie Leeuwenhoek 110(2):253–270. https://doi.org/10.1007/s10482-016-0796-0
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. https://doi.org/10.1016/j.micres.2017.08.007
Misra S, Dixit V, 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(4):419–434. https://doi.org/10.1007/s13213-018-1428-x
Nannipieri P, Ascher J, Ceccherini M, Landi L, Pietramellara G, Renella G (2003) Microbial diversity and soil functions. Eur J Soil Sci 54(4):655–670. https://doi.org/10.1046/j.1351-0754.2003.0556.X
Nautiyal CS (1997) A method for selection and characterization of rhizosphere-competent bacteria of chickpea. Curr Microbiol 34(1):12–17. https://doi.org/10.1007/s0028499001
Nautiyal CS (1999) An efficient microbiological growth medium for screening phosphate solubilizing microorganisms. FEMS Microbiol Lett 170(1):265–270. https://doi.org/10.1111/j.1574-6968.1999.tb13383.x
Nautiyal CS, Bhadauria S, Kumar P, Lal H, Mondal R, Verma D (2000) Stress induced phosphate solubilization in bacteria isolated from alkaline soils. FEMS Microbiol Lett 182(2):291–296. https://doi.org/10.1111/j.1574-6968.2000.tb08910.x
Nazir Q, Akhtar MJ, Imran M, Arshad M, Hussain A, Mahmood S, Hussain S (2017) Simultaneous use of plant growth promoting rhizobacterium and nitrogenous fertilizers may help in promoting growth, yield, and nutritional quality of okra. J Plant Nutr 40(9):1339–1350. https://doi.org/10.1080/01904167.2016.1267747
Penrose DM, Glick BR (2003) Methods for isolating and characterizing ACC deaminase-containing plant growth-promoting rhizobacteria. Physiol Plant 118(1):10–15. https://doi.org/10.1034/j.1399-3054.2003.00086.x
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. https://doi.org/10.3389/fphys.2017.00667
Ratzke C, Gore J (2018) Modifying and reacting to the environmental pH can drive bacterial interactions. PLoS Biol 16(3):e2004248. https://doi.org/10.1371/journal.pbio.2004248
Sapre S, Gontia-Mishra I, Tiwari S (2018) Klebsiella sp. confers enhanced tolerance to salinity and plant growth promotion in oat seedlings (Avena sativa). Microbiol Res 206:25–32. https://doi.org/10.1016/j.micres.2017.09.009
Shulse CN, Chovatia M, Agosto C, Wang G, Hamilton M, Deutsch S, Yoshikuni Y, Blow MJ (2019) Engineered root bacteria release plant-available phosphate from phytate. Appl Environ Microbiol 85(18):e01210–e1219. https://doi.org/10.1128/AEM.01210-19
Siciliano SD, Palme AS, Winsley T, Lamb E, Bissett A, Brow MV, Dorst JV, Ji M, Ferrari BC (2014) Soil fertility is associated with fungal and bacterial richness, whereas pH is associated with community composition in polar soil microbial communities. Soil Biol Biochem 78:10–20. https://doi.org/10.1016/j.soilbio.2014.07.005
Singh K (2016) Microbial and enzyme activities of saline and sodic soils. Land Degrad Dev 27(3):706–718. https://doi.org/10.1002/ldr.2385
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(6):e0155026. https://doi.org/10.1371/journal.pone.0155026
Singh K, Pandey VC, Singh B, Singh RR (2012) Ecological restoration of degraded sodic lands through afforestation and cropping. Ecol Eng 43:70–80. https://doi.org/10.1016/j.ecoleng.2012.02.029
Singh K, Trivedi P, Singh G, Singh B, Patra D (2016) Effect of different leaf litters on carbon, nitrogen and microbial activities of sodic soils. Land Degrad Dev 27(4):1215–1226. https://doi.org/10.1002/ldr.2313
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(5):453–457. https://doi.org/10.1007/s00284-008-9105-0
Titus S, Gaonkar S, Srivastava RB, Karande AA (1995) Exopolymer production by a fouling marine bacterium Pseudomonas alcaligenes. Indian J Mar Sci 24:45–48
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(4):307–313. https://doi.org/10.1139/cjm-2014-0668
Verma M, Mishra J, Arora NK (2019) Plant growth-promoting rhizobacteria: diversity and applications. In: Sobti RC, Arora NK, Kothari R (eds) Environmental biotechnology: for sustainable future. Springer, Singapore, pp 129–173
Wang W, Wu Z, He Y, Huang Y, Li X, Ye BC (2018) Plant growth promotion and alleviation of salinity stress in Capsicum annuum L. by Bacillus isolated from saline soil in Xinjiang. Ecotoxicol Environ Safe 164:20–529. https://doi.org/10.1016/j.ecoenv.2018.08.070
Yadav AN, Sachan SG, Verma P, Saxena AK (2016) Bioprospecting of plant growth promoting psychrotrophic Bacilli from the cold desert of north western Indian Himalayas. Indian J Exp Biol 54:142–150
Yasmin H, Nosheen A, Naz R, Bano A, Keyani R (2017) L-tryptophan-assisted PGPR-mediated induction of drought tolerance in maize (Zea mays L.). J Plant Interact 12(1):567–578. https://doi.org/10.1080/17429145.2017.1402212
Zhang J, Han C, Liu Z (2009) Absorption spectrum estimating rice chlorophyll concentration: preliminary investigations. J Plant Breed Crop Sci 5:223–229
Zheng BX, Zhang DP, Wang Y, Hao XL, Wadaan MA, Hozzein WN, Peñuelas J, Zhu YG, Yang XR (2019) Responses to soil pH gradients of inorganic phosphate solubilizing bacteria community. Sci Rep 9(1):25. https://doi.org/10.1038/s41598-018-37003-w
Acknowledgements
The authors acknowledge the Director, CSIR National Botanical Research Institute for providing facilities and support during the study. VKD acknowledges CSIR, New Delhi for Senior Research Fellowship.
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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, NJ, SKT conceived the idea and designed the experiments; VKD, SM, and SKM carried out the research experiments and analyzed the results. Overall manuscript was written by PSC, VKD, NJ and SKT. All authors read and approved the manuscript.
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Dixit, V.K., Misra, S., Mishra, S.K. et al. Characterization of plant growth-promoting alkalotolerant Alcaligenes and Bacillus strains for mitigating the alkaline stress in Zea mays. Antonie van Leeuwenhoek 113, 889–905 (2020). https://doi.org/10.1007/s10482-020-01399-1
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DOI: https://doi.org/10.1007/s10482-020-01399-1