Halotolerant Plant Growth Promoting Bacilli from Sundarban Mangrove Mitigate the Effects of Salinity Stress on Pearl Millet (Pennisetum glaucum L.) Growth

Pallavi; Rohit Kumar Mishra; Ajit Varma; Neeraj Shrivastava; Swati Tripathi

doi:10.18006/2023.11(4).746.755

Authors

Pallavi Amity Institute of Microbial Technology, Amity University Uttar Pradesh, Noida201301, India
Rohit Kumar Mishra Centre of Science and Society, University of Allahabad, Prayagraj, Uttar Pradesh- 211002, India
Ajit Varma Amity Institute of Microbial Technology, Amity University Uttar Pradesh, Noida201301, India
Neeraj Shrivastava Amity Institute of Microbial Technology, Amity University Uttar Pradesh, Noida201301, India
Swati Tripathi Amity Institute of Microbial Technology, Amity University Uttar Pradesh, Noida201301, India

DOI:

https://doi.org/10.18006/2023.11(4).746.755

Keywords:

Pearl millet, Salt stress, PGPR, Antioxidants, Bacillus

Abstract

Pearl millet (Pennisetum glaucum L.) is one of the major crops in dry and saline areas across the globe. During salinity stress, plants encounter significant changes in their physio and biochemical activities, leading to decreased growth and yield. Bacillus species are used as biofertilizers and biopesticides for pearl millet and other crops to promote growth and yield. The use of Bacillus in saline soils has been beneficial to combat the negative effect of salinity on plant growth and yield. In this context, the present study emphasizes the use of two Bacillus species, i.e. Bacillus megaterium JR-12 and B. pumilus GN-5, which helped in alleviating the impact of salinity stress on the growth activities in salt-stressed pearl millet. Pearl millet seeds were treated with two strains, B. megaterium JR-12 and B.pumilus GN-5, individually and in combination under 50, 100 and 150 mM of sodium chloride stress. The treated plants showed higher plant height, biomass accumulation, and photosynthetic apparatus than the non-treated plants. Additionally, the treated plants showed increased osmoprotectant levels under salinity stress compared to control plants. The antioxidant enzyme content was improved post-inoculation, indicating the efficient stress-alleviating potential of both strains of Bacillus species. Moreover, inoculation of these microbes significantly increased plant growth attributes in plants treated with a combination of Bp-GN-5 + Bm-JR-12 and the reduction rates of plant growth were found to be alleviated to 9.12%, 20.30% and 33%, respectively. Overall, the results of the present study suggested that these microbes could have a higher potential to improve the productivity of pearl millet under salinity stress.

Author Biography

Pallavi, Amity Institute of Microbial Technology, Amity University Uttar Pradesh, Noida201301, India

ICAR- National Bureau of Agriculturally Important Microorganism, Kushmaur, Mau, Uttar Pradesh- 275103, India

References

Aebi, H. (1984). Catalase in vitro. Methods in Enzymology,105,121-126 DOI: https://doi.org/10.1016/S0076-6879(84)05016-3

Alotaibi, N.M., Kenyon, E.J, Bertelli, C.M., Al-Qthanin, R.N., Mead, J., Parry, M., & Bull, J.C. (2022). Environment predicts seagrass genotype, phenotype, and associated biodiversity in a temperate ecosystem. Frontiers in Plant Science, 13, 887474. doi: 10.3389/fpls.2022.887474 DOI: https://doi.org/10.3389/fpls.2022.887474

Arnon, D. I. (1949). Copper Enzymes in Isolated Chloroplasts. Polyphenoloxidasein Beta vulgaris. Plant physiology, 24(1), 1–15. https://doi.org/10.1104/pp.24.1.1 DOI: https://doi.org/10.1104/pp.24.1.1

Auta, H. S., Emenike, C. U., & Fauziah, S. H. (2017). Screening of Bacillus strains isolated from mangrove ecosystems in Peninsular Malaysia for microplastic degradation. Environmental pollution (Barking, Essex : 1987), 231(Pt 2), 1552–1559. https://doi.org/10.1016/j.envpol.2017.09.043 DOI: https://doi.org/10.1016/j.envpol.2017.09.043

Ayaz, M., Ali, Q., Jiang, Q., Wang, R., Wang, Z., et al. (2022). Salt tolerant Bacillus strains improve plant growth traits and regulation of phytohormones in wheat under salinity stress. Plants, 11(20), 2769. https://doi.org/10.3390/plants11202769 DOI: https://doi.org/10.3390/plants11202769

Ayyam, V., Palanivel, S., & Chandrakasan, S. (2019). Approaches in land degradation management for productivity enhancement. In V. Ayyam, S. Palanivel, & S. Chandrakasan (Eds.), Coastal Ecosystems of the Tropics—Adaptive Management (pp. 463–491); Singapore Springer. DOI: https://doi.org/10.1007/978-981-13-8926-9_20

Bates, L.S., Waldren, R.P., & Teare, I.D. (1973).Rapid determination of free proline for water stress studies. Plant and Soil, 39, 205-207 DOI: https://doi.org/10.1007/BF00018060

Bhat, M.A., Kumar, V., Bhat, M.A., Wani, I.A., Dar, F.L., Farooq, I., Bhatti, F., Koser, R., Rahman, S., & Jan, A.T. (2020). Mechanistic insights of the interaction of plant growth-promoting rhizobacteria (PGPR) with plant roots toward enhancing plant productivity by alleviating salinity stress. Frontiers in Microbiology, 11, 1952. doi: 10.3389/fmicb.2020.01952 DOI: https://doi.org/10.3389/fmicb.2020.01952

Bradford, M.M. (1976). A rapid and sensitive method for the quantification of microgram quantities of protein utilizing the principle of protein-dye binding. Analytical Biochemistry, 72, 248-254 DOI: https://doi.org/10.1016/0003-2697(76)90527-3

Brick, J.M., Bostock, R.M., & Silverstones, S.E. (1991). Rapid in situ assay for indole acetic acid production by bacteria immobilized on nitrocellulose membrane. Applied Environment Microbiology, 57(2), 535-538 DOI: https://doi.org/10.1128/aem.57.2.535-538.1991

Cappuccino, J.C., & Sherman, N. (1992). Microbiology “A Laboratory Manual“, Benjamin/Cummings, New Yorkpp. Pp. 125–179

Dhindsa, R.H., & Thorpe, T.A. (1981). Leaf senescence correlated with increased level of membrane permeability, lipid peroxidation and decreased level of SOD and CAT. Journal of Experimental Botany, 32, 93-101 DOI: https://doi.org/10.1093/jxb/32.1.93

Dodd, I.C., & Pérez-Alfocea, F. (2012). Microbial amelioration of crop salinity stress. Journal of Experimental Botany, 63, 3415-28 DOI: https://doi.org/10.1093/jxb/ers033

Edi-Premono, M., Moawad, A.M., & Vleck, P.L.G. (1996). Effect of phosphate solubilizing Pseudomonas putida on the growth of maize and its survival in the rhizosphere. Indonesian Journal of Crop Science,11 (1), 13-23.

Evans, L. (2006). Millet for reclaiming irrigated saline soils. Prime facts, Profitable and sustainable primary industries www.dpi.nsw.gov.au

Habib, S. H., Kausar, H., & Saud, H. M. (2016). Plant growth-promoting rhizobacteria enhance salinity stress tolerance in okra through ROS-scavenging enzymes. Biomed Research International, 2016, 6284547.doi: 10.1155/2016/6284547 DOI: https://doi.org/10.1155/2016/6284547

Hussain, K., Ashraf, M., & Ashraf, M.Y. (2008). Relationship between growth and ion relation in pearl millet (Pennisetum glaucum (L.) R. Br.) at different growth stages under salt stress. African Journal of Plant Science, 3(2), 23- 27

Hussain, K., Nawaz, K., Majeed, A., Khan, F., Lin, F., et al. (2010). Alleviation of salinity effects by exogenous applications of salicylic acid in pearl millet (Pennisetum glaucum (L.) R. Br.) Seeding. African Journal of Biotechnology, 9(50), 8602-8607

Khan, M. Y., Nadeem, S. M., Sohaib, M., Waqas, M. R., Alotaibi, F., Ali, L., Zahir, Z. A., & Al-Barakah, F. N. I. (2022). Potential of plant growth promoting bacterial consortium for improving the growth and yield of wheat under saline conditions. Frontiers in microbiology, 13, 958522. https://doi.org/10.3389/fmicb.2022.958522 DOI: https://doi.org/10.3389/fmicb.2022.958522

Kumar, A., Kumar, R., Yadav, V.P.S., & Kumar, R. (2010). Impact assessment of frontline demonstrations of Bajra in Haryana state. Indian Research Journal of Extension Education, 10(1), 105–108.

Kumar, V. & Gera, R. (2014). Isolation of a multi-trait plant growth promoting Brevundimonas sp. and its effect on the growth of Bt-cotton. 3 Biotech, 4, 97-101 DOI: https://doi.org/10.1007/s13205-013-0126-4

Ling, N., Wang, T., & Kuzyakov, Y. (2022). Rhizosphere bacteriome structure and functions. Nature Communications, 13, 836 https://doi.org/10.1038/s41467-022-28448-9 DOI: https://doi.org/10.1038/s41467-022-28448-9

Miller, G.L. (1959). Use of dinitrosalicylic acid reagent for determination of reducing sugar. Analytical Chemistry, 31(3), 426-428 DOI: https://doi.org/10.1021/ac60147a030

Munns, R., & Tester, M. (2008). Mechanisms of salinity tolerance. The Annual Review of Plant Biology, 59, 651–681 DOI: https://doi.org/10.1146/annurev.arplant.59.032607.092911

Orhan, F. (2016). Alleviation of salt stress by halotolerant and halophilic plant growth-promoting bacteria in wheat (Triticum aestivum). Brazilian Journal of Microbiology, 47(3), 621–627. https://doi.org/10.1016/j.bjm.2016.04.001. DOI: https://doi.org/10.1016/j.bjm.2016.04.001

Pallavi, Mishra, R. K., Sahu, P. K., Mishra, V., Jamal, H., Varma, A., & Tripathi, S. (2023). Isolation and characterization of halotolerant plant growth promoting rhizobacteria from mangrove region of Sundarbans, India for enhanced crop productivity. Frontiers in Plant Science, 14, 1122347. https://doi.org/10.3389/fpls.2023.1122347 DOI: https://doi.org/10.3389/fpls.2023.1122347

Patel, M., Vurukonda, S.S.K.P., & Patel, A. (2023). Multi-trait halotolerant plant growth-promoting bacteria mitigate induced salt stress and enhance growth of Amaranthus viridis. Journal of Soil Science and Plant Nutrition, 23 (2), 1860-1883. doi: 10.1007/s42729-023-01143-4 DOI: https://doi.org/10.1007/s42729-023-01143-4

Pérez-Miranda, S., Cabirol, N., & George-Téllez, R. (2007). O-CAS, a fast and universal method for siderophore detection. Journal of Microbiological Methods, 70 (1), 127–131 DOI: https://doi.org/10.1016/j.mimet.2007.03.023

Pikovskaya, R.I. (1948). Mobilization of phosphorus in soil in connection with the vital activity of some microbial species. Mikrobiologiya,17, 362-370

Sadasivam, S., & Manickam, A. (1996). Biochemical Methods for Agricultural Sciences. New Delhi: New Age International (P) Ltd. pp. 1–97

Sahu, P.K., Singh, S., Singh, U.B., Chakdar, H., Sharma, P.K., et al. (2021). Inter-Genera colonization of Ocimum tenuiflorum endophytes in tomato and their complementary effects on Na+/K+ Balance, Oxidative Stress Regulation, and Root Architecture Under Elevated Soil Salinity. Frontiers in Microbiology, 18(12), 744733. doi: 10.3389/fmicb.2021.744733. DOI: https://doi.org/10.3389/fmicb.2021.744733

Sahu, P.K., Tilgam, J., Mishra, S., Hamid, S., Gupta, A., Verma, S.K., & Kharwar, R.N. (2022). Surface sterilization for isolation of endophytes: Ensuring what (not) to grow. Journal of Basic Microbiology, 62(6), 647-668. doi: 10.1002/jobm.202100462 DOI: https://doi.org/10.1002/jobm.202100462

Sairam, R.K., Rao, K.V., & Srivastava, G.C. (2002). Differential response of wheat genotypes to long term salinity stress relation to oxidative stress, antioxidant activity and osmolyte concentration. Plant Sciences, 163, 1037– 1046 DOI: https://doi.org/10.1016/S0168-9452(02)00278-9

Santos, A. D. A., Silveira, J. A. G. D., Bonifacio, A., Rodrigues, A. C., & Figueiredo, M. D. V. B. (2018). Antioxidant response of cowpea co-inoculated with plant growth-promoting bacteria under salt stress. Brazilian Journal of. Microbiology, 49, 513–521. doi: 10.1016/j.bjm.2017.12.003 DOI: https://doi.org/10.1016/j.bjm.2017.12.003

Schirawski, J., & Perlin, M. H. (2017). Plant-microbe interaction. The good, the bad and the diverse. International Journal of Molecular Sciences, 19, 1374. DOI: https://doi.org/10.3390/ijms19051374

Schwyn, B., & Neilands, J.B. (1987). Universal chemical assay for the detection and determination of siderophores. Analytical Biochemistry, 160, 47–56 DOI: https://doi.org/10.1016/0003-2697(87)90612-9

Shahbaz, M., & Ashraf, M. (2013). Improving salinity tolerance in cereals. Critical Review in Plant Sciences, 32, 237–249 DOI: https://doi.org/10.1080/07352689.2013.758544

Sharma, A., Dev, K., Sourirajan, A., & Choudhary, M. (2021). Isolation and characterization of salt-tolerant bacteria with plant growth-promoting activities from saline agricultural fields of Haryana, India. Journal of Genetic Engineering and Biotechnology, 19, 99 (2021). https://doi.org/10.1186/s43141-021-00186-3. DOI: https://doi.org/10.1186/s43141-021-00186-3

Sharma, P., Jha, A. B., Dubey, R. S., & Pessarakli, M. (2012). Reactive oxygen species, oxidative damage, and antioxidative defense mechanism in plants under stressful conditions. Journal of Botany, 2012, 217037. doi: 10.1155/2012/217037 DOI: https://doi.org/10.1155/2012/217037

Singh, T.B., Sahai, V., Ali A., Prasad, M., Yadav, A., Shrivastav, P., Goyal, D., & Dantu, P.K. (2020). Screening and evaluation of PGPR strains having multiple PGP traits from the hilly terrain.Journal of Applied Biology & Biotechnology, 8(04), 38-44.

Thant, S., Aung, N.N., Aye, O.M., Oo, N.N., et al. (2018). Phosphate solubilization of Bacillus megaterium isolated from non-saline soils under salt stressed conditions. Bacteriol Mycology, 6(6), 335‒341. DOI: https://doi.org/10.15406/jbmoa.2018.06.00230

Toro, G., Pimentel, P., & Salvatierra, A. (2021). Effective categorization of tolerance to salt stress through clustering Prunus rootstocks according to their physiological performances. Horticulturae,7, 542. doi: 10.3390/horticulturae7120542 DOI: https://doi.org/10.3390/horticulturae7120542

Tripathi, S., Bahuguna, R., Shrivastava, N., Singh, S., Chatterjee, A., Varma, A., & Jagadish, K. (2022). Microbial biofortification: A sustainable route to grow nutrient-rich crops under changing climate. Field Crops Research, 287. 10.1016/j.fcr.2022.108662. DOI: https://doi.org/10.1016/j.fcr.2022.108662

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. Canadian Journal of Microbiology, 61(4), 307-13. DOI: https://doi.org/10.1139/cjm-2014-0668

Upadhyay, S.K., Singh, D.P., & Saikia, R. (2009). Genetic diversity of plant growth promoting rhizobacteria isolated from rhizospheric soil of wheat under saline condition. Current Microbiology, 59(5), 489-96.doi: 10.1007/s00284-009-9464-1 DOI: https://doi.org/10.1007/s00284-009-9464-1

Venieraki, A., Chorianopoulou, S. N., Katinakis, P., & Bouranis, D. L. (2021). Multi-trait wheat rhizobacteria from calcareous soil with biocontrol activity promote plant growth and mitigate salinity stress. Microorganisms, 9(8), 1588. https://doi.org/10.3390/ microorganisms9081588 DOI: https://doi.org/10.3390/microorganisms9081588

Watanabe, F.S., & Olsen, S.R. (1965). Test of an ascorbic acid method for determining phosphorous in water and NaHCO3 extracts from soil. Soil Science Society of American Journal, 29, 677-678 DOI: https://doi.org/10.2136/sssaj1965.03615995002900060025x

Yemm, E., & Willis, A.J. (1954). The estimation of carbohydrate in plant extracts by Anthrone. Journal of Biochemistry, 57, 508-514 DOI: https://doi.org/10.1042/bj0570508