Multifaceted Plant Growth Promoting Traits and Abiotic Stress Resistance Abilities Exhibited by Chrysanthemum Rhizobacteria

Main Article Content

Mohammad Nazmul Ahmed Chowdhury
Tanim Jabid Hossain
Subrina Akter Zedny
Mohammed Sajjad Hossain Bappi
Minhajur Rahman
Md. Monir Hossen
Iqbal Hossain Nafiz
Raihanul Islam

Abstract

Plant growth-promoting rhizobacteria (PGPR) boost plant growth and agricultural sustainability in an ecologically friendly way. The cultivation of chrysanthemum, a globally significant flower crop, has relied heavily on substantial agrochemical inputs that have detrimental impact on the environment. To assess the potential of chrysanthemum rhizobacteria to reduce this reliance, bacterial strains were retrieved from the plant rhizosphere and subjected to an assessment of various plant growth-promoting traits. Out of the 34 rhizobacterial isolates, 21 demonstrated the production of the plant growth hormone auxin, 21 had phosphate solubilization ability, 22 were capable of nitrogen fixation, and 21 could produce ammonia. Based on these findings, seven preeminent PGPR strains, characterized by multifaceted plant growth-promoting traits, were selected for subsequent studies and identified as species belonging to Acinetobacter, Bacillus, Pantoea, Serratia and Staphylococcus. The selected strains were systematically analyzed for their capacity to endure an array of abiotic stresses. A majority of these strains demonstrated adaptation under osmotic stress ranging from -0.15 to -0.49 MPa, temperatures of 20°C and 30°C, and salt stress within the range of 3 to 7% NaCl, which suggests their potential to promote plant growth across diverse environmental conditions. Additionally, the secretion of hydrolytic enzymes such as protease, pectinase and amylase was examined, and only the Staphylococcus hominis PGPR-12 strain demonstrated the ability to produce all three extracellular hydrolases. These findings underscore the potential application of multiple isolates possessing promising plant-probiotic properties to enhance plant growth across various conditions, thereby necessitating further exploration through pot and field assays.

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References

Kaur, J. and Pandove, G., 2023. Understanding the beneficial interaction of plant growth promoting rhizobacteria and endophytic bacteria for sustainable agriculture: a bio-revolution approach. Journal of Plant Nutrition, 46(14), 3569-3597, https://doi.org/10.1080/01904167.2023.2206425.

Chauhan, A., Saini, R. and Sharma, J.C., 2021. Plant growth promoting rhizobacteria and their biological properties for soil enrichment and growth promotion. Journal of Plant Nutrition, 45(2), 273-299, https://doi.org/10.1080/01904167.2021.1952221.

Serri, F., Souri, M.K. and Rezapanah, M., 2021. Growth, biochemical quality and antioxidant capacity of coriander leaves under organic and inorganic fertilization programs. Chemical and Biological Technologies in Agriculture, 8(1), https://doi.org/10.1186/s40538-021-00232-9.

Neher, D., 2018. Ecological sustainability in agricultural systems: definition and measurement. In: R. Olson, ed. Integrating Sustainable Agriculture, Ecology, and Environmental Policy. New York: Routledge, pp. 51-61.

Mishra, M., Desul, S., Santos, C.A.G., Mishra, S.K., Kamal, A.H.M., Goswami, S., Kalumba, A.M., Biswal, R., da Silva, R.M., Santos, C.A.C.D. and Baral, K., 2023. A bibliometric analysis of sustainable development goals (SDGs): a review of progress, challenges, and opportunities. Environment, Development and Sustainability, 26, 11101-11143, https://doi.org/10.1007/s10668-023-03225-w.

Zhou, L., Ma, Y., Yao, J., Zhang, M., Fu, H., Yang, J. Liu, J. Zhao, M. and Marchioni, E., 2023. Discrimination of chrysanthemum varieties using lipidomics based on UHPLC–HR-AM/MS/MS. Journal of the Science of Food and Agriculture, 103(2), 837-845, https://doi.org/10.1002/jsfa.12195.

Kentelky, E., Szekely-Varga, Z., Bálint, J. and Balog, A., 2021. Enhance growth and flower quality of Chrysanthemum indicum L. with application of plant growth retardants. Horticulturae, 7(12), https://doi.org/10.3390/horticulturae7120532.

Verma, S., Angadi, S., Patil, V., Mokashi, A., Mathad, J. and Mummigatti, U., 2012. Growth, yield and quality of chrysanthemum (Chrysanthemum morifolium Ramat.) Cv. Raja as influenced by integrated nutrient management. Karnataka Journal of Agricultural Sciences, 24(5), 681-683.

Khallouki, F., Hmamouchi, M., Younos, C., Soulimani, R., Bessiere, J.M. and Essassi, E.M., 2000. Antibacterial and molluscicidal activities of the essential oil of Chrysanthemum viscidehirtum. Fitoterapia, 71(5), 544-546, https://doi.org/10.1016/S0367-326X(00)00154-4.

Andoğan, B.C., Baydar, H., Kaya, S., Demirci, M., Özbaşar, D. and Mumcu, E., 2002. Antimicrobial activity and chemical composition of some essential oils. Archives of Pharmacal Research, 25(6), 860-864, https://doi.org/10.1007/BF02977005.

Tsuji-Naito, K., Saeki, H. and Hamano, M., 2009. Inhibitory effects of Chrysanthemum species extracts on formation of advanced glycation end products. Food Chemistry, 116(4), 854-859, https://doi.org/10.1016/j.foodchem.2009.03.042.

Malpani, M.O., Rajput, P.R., Chinchole, K.V., Kapse, S.S. and Ambarkar, K.S., 2019. Phytochemical screening and antioxidant activity of extracts of Xanthium strumarium, Chrysanthemum and their mixture. Inflammation, 12(4), 1901-1908, https://doi.org/10.31788/RJC.2019.1245447.

Zhang, S., Dong, S., Chi, L., He, P., Wang, Q. and Fang, Y., 2008. Simultaneous determination of flavonoids in chrysanthemum by capillary zone electrophoresis with running buffer modifiers. Talanta, 76(4), 780-784, https://doi.org/10.1016/j.talanta.2008.04.025.

Wu, L.-Y., Gao, H.-Z., Wang, X.-L., Ye, J.-H., Lu, J. and Liang, Y.-R., 2010. Analysis of chemical composition of Chrysanthemum indicum flowers by GC/MS and HPLC. Journal of Medicinal Plants Research, 4(5), 421-426.

Tahri, W., Chatti, A., Romero-González, R., López-Gutiérrez, N., Frenich, A.G. and Landoulsi, A., 2016. Phenolic profiling of the aerial part of Chrysanthemum trifurcatum using ultra high performance liquid chromatography coupled to Orbitrap high resolution mass spectrometry. Analytical Methods, 8(17), 3517-3527, https://doi.org/10.1039/C6AY00365F.

Han, S.H., An, J.Y., Hwang, J., Kim, S.B. and Park, B.B., 2016. The effects of organic manure and chemical fertilizer on the growth and nutrient concentrations of yellow poplar (Liriodendron tulipifera Lin.) in a nursery system. Forest Science and Technology, 12(3), 137-143, https://doi.org/10.1080/21580103.2015.1135827.

Htwe, A.Z., Moh, S.M., Soe, K.M., Moe, K. and Yamakawa, T., 2019. Effects of biofertilizer produced from bradyrhizobium and streptomyces griseoflavus on plant growth, nodulation, nitrogen fixation, nutrient uptake, and seed yield of mung bean, cowpea, and soybean. Agronomy, 9(2), https://doi.org/10.3390/agronomy9020077.

Dai, P., Cong, P., Wang, P., Dong, J., Dong, Z. and Song, W., 2021. Alleviating soil acidification and increasing the organic carbon pool by long-term organic fertilizer on tobacco planting soil. Agronomy, 11(11), https://doi.org/10.3390/agronomy11112135.

Singh, M., Singh, D., Gupta, A., Pandey, K.D., Singh, P.K. and Kumar, A., 2019. Application in biofertilizers and biocontrol of phytopathogens. In: A.K. Singh, A. Kumar and P.K. Singh, eds. PGPR Amelioration in Sustainable Agriculture: Food Security and Environmental Management. Cambridge: Woodhead Publishing, pp. 41-66.

Biochemistry and Pathogenesis of Microbes Research Group, 2023. Microbial Culture Media. [online] Available at: https://sites.google.com/view/bpm-research-group/news-info/culture-media.

Zobaer, M., Ali, F., Anwar, M.N., Bappi, M.S.H., Bakar, T.B., Hossain, T.J., 2023. Isolation of Biosurfactant Producing Bacteria from Oil-spilled Soil and Characterization of Their Secreted Biosurfactants in Pathogen-inhibition and Oil-emulsification. [online] Available at: https://ssrn.com/abstract=4320992.

Hossain, T.J., Alam, M. and Sikdar, D., 2011. Chemical and microbiological quality assessment of raw and processed liquid market milks of Bangladesh. Continental Journal of Food Science and Technology, 5(2), 6-17, https://doi.org/10.5281/zenodo.5568945.

Hossain, T.J., Chowdhury, S.I., Mozumder, H.A., Chowdhury, M.N.A., Ali, F., Rahman, N. and Dey, S., 2020. Hydrolytic exoenzymes produced by bacteria isolated and identified from the gastrointestinal tract of Bombay duck. Frontiers in Microbiology, 11, https://doi.org/10.3389/fmicb.2020.02097.

Basharat, T., Ali, F., Das, T., Bakar, T.B., Mishi, N.T., Ferdouse, J., Uddin, M.S. and Hossain, T.J., 2022. Phosphate solubilizing rhizobacteria of rice: analysis of plant growth promoting activity and environmental stress tolerance. Annals of Agri-Bio Research, 28(2), 197-208, https://doi.org/10.2139/ssrn.4249001.

Singh, T.B., Sahai, V., Ali, A., Prasad, M., Yadav, A., Shrivastav, P., Goyal, D. and Dantu, P.K., 2020. Screening and evaluation of PGPR strains having multiple PGP traits from hilly terrain. Journal of Applied Biology and Biotechnology, 8(4), 38-44, https://doi.org/10.7324/JABB.2020.80406.

Kirui, C.K., Njeru, E.M. and Runo, S., 2022. Diversity and phosphate solubilization efficiency of phosphate solubilizing bacteria isolated from semi-arid agroecosystems of eastern Kenya. Microbiology Insights, 15, https://doi.org/10.1177/11786361221088991.

Ferioun, M., Srhiouar, N., Tirry, N., Belahcen, D., Siang, T.C., Louahlia, S. and Ghachtouli, N.E., 2023. Optimized drought tolerance in barley (Hordeum vulgare L.) using plant growth-promoting rhizobacteria (PGPR). Biocatalysis and Agricultural Biotechnology, 50, https://doi.org/10.1016/j.bcab.2023.102691.

AlAli, H.A., Khalifa, A., Almalki, M., 2021. Plant growth-promoting rhizobacteria from Ocimum basilicum improve growth of Phaseolus vulgaris and Abelmoschus esculentus. South African Journal of Botany, 139, 200-209, https://doi.org/10.1016/j.sajb.2021.02.019.

Mei, C., Chretien, R.L., Amaradasa, B.S., He, Y., Turner, A. and Lowman, S., 2021. Characterization of phosphate solubilizing bacterial endophytes and plant growth promotion in vitro and in greenhouse. Microorganisms, 9(9), https://doi.org/10.3390/microorganisms9091935.

Ali, F., Das, S., Hossain, T.J., Chowdhury, S.I., Zedny, S.A., Das, T., Chowdhury, M.N.A. and Uddin, M.S., 2021. Production optimization, stability and oil emulsifying potential of biosurfactants from selected bacteria isolated from oil-contaminated sites. Royal Society Open Science, 8(10), https://doi.org/10.1098/rsos.211003.

Carvalho, T.S. and Lima, A.C.P., 2020. Mitigation of osmotic stress by Serratia nematodiphila in tomato seedlings. Research, Society and Development, 9(10), https://doi.org/10.33448/rsd-v9i10.8694.

Jagtap, R.R., Mali, G.V., Waghmare, S.R., Nadaf, N.H., Nimbalkar, M.S. and Sonawane, K.D., 2023. Impact of plant growth promoting rhizobacteria Serratia nematodiphila RGK and Pseudomonas plecoglossicida RGK on secondary metabolites of turmeric rhizome,

Biocatalysis and Agricultural Biotechnology, 47, https://doi.org/10.1016/j.bcab.2023.102622.

Gomes, G.L.B. and Scortecci, K.C., 2021. Auxin and its role in plant development: structure, signalling, regulation and response mechanisms. Plant Biology, 23(6), 894-904, https://doi.org/10.1111/plb.13303.

Zope, V.P., Enshasy, H.A.E. and Sayyed, R.Z., 2019. Plant growth-promoting rhizobacteria: an overview in agricultural perspectives. In: R.Z. Sayyed, ed. Plant Growth Promoting Rhizobacteria for Sustainable Stress Management. Vol. 2: Rhizobacteria in Biotic Stress Management. Singapore: Springer, pp. 345-361.

Ahmed, A. and Hasnain, S., 2014. Auxins as one of the factors of plant growth improvement by plant growth promoting rhizobacteria. Polish Journal of Microbiology, 63(3), http://doi.org/10.33073/pjm-2014-035.

Kumar, N., Srivastava, P., Vishwakarma, K., Kumar, R., Kuppala, H., Maheshwari, S.K. and Vats, S., 2020. The rhizobium–plant symbiosis: state of the art. In: A. Varma, S. Tripathi, and R. Prasad, eds. Plant Microbe Symbiosis. Cham: Springer, pp. 1-20.

Karimi, N., Zarea, M.J. and Mehnaz, S., 2018. Endophytic Azospirillum for enhancement of growth and yield of wheat. Environmental Sustainability, 1, 149-158, http://doi.org/10.1007/s42398-018-0014-2.

Galindo, F.S., Pagliari, P.H., Fernandes, G.C., Rodrigues, W.L., Boleta, E.H.M., Jalal, A., Céu, E.G.O., de Lima, B.H., Lavres, J. and Filho, M.C.M.T., 2022. Improving sustainable field-grown wheat production with Azospirillum brasilense under tropical conditions: a potential tool for improving nitrogen management. Frontiers in Environmental Science, 10, https://doi.org/10.3389/fenvs.2022.821628.

Shahid, M. and Khan, M.S., 2022. Tolerance of pesticides and antibiotics among beneficial soil microbes recovered from contaminated rhizosphere of edible crops. Current Research in Microbial Sciences, 3, https://doi.org/10.1016/j.crmicr.2021.100091.

Kour, D., Rana, K.L., Yadav, N., Yadav, A.N., Kumar, A., Meena, V.S., Singh, B., Chauhan, V.S., Dhaliwal, H.S. and Saxena, A.K., 2019. Rhizospheric microbiomes: biodiversity, mechanisms of plant growth promotion, and biotechnological applications for sustainable agriculture. In: A. Kumar and V.S. Meena, eds. Plant Growth Promoting Rhizobacteria for Agricultural Sustainability: From Theory to Practices, Singapore: Springer, pp. 19-65.

Rafi, M.M., Krishnaveni, M.S. and Charyulu, P.B.B.N., 2019. Phosphate-solubilizing microorganisms and their emerging role in sustainable agriculture. In: V. Buddolla, ed. Recent Developments in Applied Microbiology and Biochemistry. Cambridge: Academic Press, pp. 223-233.

Cherif-Silini, H., Thissera, B., Bouket, A.C., Saadaoui, N., Silini, A., Eshelli, M., Alenezi, F.N., Vallat, A., Luptakova, L., Yahiaoui, B., Cherrad, S., Vancher, S., Rateb, M.E. and Belbahri, L. 2019. Durum wheat stress tolerance induced by endophyte Pantoea agglomerans with genes contributing to plant functions and secondary metabolite arsenal. International Journal of Molecular Sciences, 20(16), https://doi.org/10.3390/ijms20163989.

Rawat, P., Sharma, A., Shankhdhar, D. and Shankhdhar, S.C., 2022. Comparative response of phosphate solubilizing indigenous Bacillus licheniformis, Pantoea dispersa and Staphylococcus sp. from rice rhizosphere for their multifarious growth promoting characteristics. Geomicrobiology Journal, 39(6), 445-452, http://doi.org/10.1080/01490451.2022.2027049.

Dastager, S.G., Deepa, C.K. and Pandey, A., 2011. Potential plant growth-promoting activity of Serratia nematodiphila NII-0928 on black pepper (Piper nigrum L.). World Journal of Microbiology and Biotechnology, 27(2), 259-265, http://doi.org/10.1007/s11274-010-0454-z.

Kang, S.-M., Khan, A.L., Waqas, M., You, Y.-H., Hamayun, M., Joo, G.-J., Shahzad, R. Choi, K.-S. and Lee, I.-J. 2015. Gibberellin-producing Serratia nematodiphila PEJ1011 ameliorates low temperature stress in Capsicum annuum L. European Journal of Soil Biology, 68, 85-93, https://doi.org/10.1016/j.ejsobi.2015.02.005.

Luo, S., Wan, Y., Xiao, X., Guo, H., Chen, L., Xi, Q., Zeng, G., Liu, C. and Chen, J., 2011. Isolation and characterization of endophytic bacterium LRE07 from cadmium hyperaccumulator Solanum nigrum L. and its potential for remediation. Applied Microbiology and Biotechnology, 89(5), 1637-1644, https://doi.org/10.1007/s00253-010-2927-2.

Akhtar, N., Ilyas, N., Yasmin, H., Sayyed, R.Z., Hasnain, Z., Elsayed, E.A. and Enshasy, H.A.E., 2021. Role of Bacillus cereus in improving the growth and phytoextractability of Brassica nigra (L.) K. Koch in chromium contaminated soil. Molecules, 26(6), https://doi.org/10.3390%2Fmolecules26061569.

Wang, N., Wang, L., Zhu, K., Hou, S., Chen, L., Mi, D., Gui, Y., Qi, Y. Jiang, C. and Guo, J.-H., 2019. Plant root exudates are involved in Bacillus cereus AR156 mediated biocontrol against Ralstonia solanacearum. Frontiers in Microbiology, 10, https://doi.org/10.3389/fmicb.2019.00098.

Cheng, Y., Luo, J., Wang, Y., Ge, J., Zhou, S., Yang, W. and Kou, J., 2021. Staphylococcus hominis YJILJH and Staphylococcus epidermidis YJ101 promote the growth of white clover (Trifolium repens L.) by increasing available phosphorus. Symbiosis, 83, 103-114, https://doi.org/10.1007/s13199-020-00739-z.

Andleeb, S., Shafique, I., Naseer, A., Abbasi, W.A., Ejaz, S., Liaqat, I., Ali, S., Khan, M.F., Ahmed, F. and Ali, N.M., 2022. Molecular characterization of plant growth-promoting vermi-bacteria associated with Eisenia fetida gastrointestinal tract. Plos One, 17(6), https://doi.org/10.1371/journal.pone.0269946.

Lamont, B.B. and Pérez-Fernández, M., 2016. Total growth and root-cluster production by legumes and proteas depends on rhizobacterial strain, host species and nitrogen level. Annals of Botany, 118(4), 725-732, https://doi.org/10.1093/aob/mcw090.

Khanghahi, M.Y., AbdElgawad, H., Verbruggen, E., Korany, S.M., Alsherif, E.A., Beemster, G.T.S. and Crecchio, C., 2022. Biofertilisation with a consortium of growth-promoting bacterial strains improves the nutritional status of wheat grain under control, drought, and salinity stress conditions. Physiologia Plantarum, 174(6), https://doi.org/10.1111/ppl.13800.

Fatima, I., Hakim, S., Imran, A., Ahmad, N., Imtiaz, M., Ali, H., Islam, E.-U., Yousaf, S., Mirza, M.S. and Mubeen, F., 2022. Exploring biocontrol and growth-promoting potential of multifaceted PGPR isolated from natural suppressive soil against the causal agent of chickpea wilt. Microbiological Research, 260, https://doi.org/10.1016/j.micres.2022.127015.

Mohammed, M.A., Chernet, M.T. and Tuji, F.A., 2020. Phenotypic, stress tolerance, and plant growth promoting characteristics of rhizobial isolates of grass pea. International Microbiology, 23, 607-618, https://doi.org/10.1007/s10123-020-00131-3.

Kumar, G.P., Ahmed, S.K.M.H., Desai, S., Amalraj, E.L.D. and Rasul, A., 2014. In vitro screening for abiotic stress tolerance in potent biocontrol and plant growth promoting strains of Pseudomonas and Bacillus spp. International Journal of Bacteriology, 2014, https://doi.org/10.1155/2014/195946.