Effect of Fluorescent-Producing Rhizobacteria on Cereal Growth Through Siderophore Exertion
DOI:
https://doi.org/10.38211/joarps.2023.04.02.168Keywords:
Siderophore, Fluorescence, Wheat, Maize, Iron solubilization, RhizobacteriaAbstract
Despite soil having an abundance of iron (Fe), it is unavailable for proper plant growth and development. One of the mechanisms plants use to deal with iron deficiency is the uptake of iron by chelating phytosiderophores. Pseudomonas fluorescence can produce pyoverdine-type siderophore and has potential application in agriculture as an iron chelator. Therefore, bacterial isolates collected from different areas of district Faisalabad were screened for their fluorescent, siderophore production and indole acetic acid equivalents. After selecting efficient strains from a screening test, they were evaluated for improving wheat and maize production under field conditions. The results showed that out of 15 isolates, 7 were found to have significant plant-beneficial microbial traits. Efficient strains promoted grain yield by 24.2% and 20.2%, plant height by 30.9% and 23.7%, total grain weight by 25.3% and 13.4% over control in wheat and maize, respectively. Similarly, significant improvements in the number of grains per cob/spike were also observed. Analyses of grain iron contents depicted 67% increase as compared to control in for maize. Therefore, based on the results, it is concluded that bio-fortification of cereal crops through fluorescent producing siderophoric microbes is an effective strategy favorable for plant growth and development through nutrient solubilization/mobilization.
Downloads
References
Adjanohoun, A., Allagbe, M., Noumavo, P. A., Gotoechan-Hodonou, H., Sikirou, R., Dossa, K. K., .& Baba-Moussa, L. (2011). Effects of plant growth promoting rhizobacteria on field grown maize. Journal of Animal & Plant Sciences, 11(3), 1457-1465.
Aguado-Santacruz, G. A., Moreno-Gómez, B., Jiménez-Francisco, B., García-Moya, E., & Preciado-Ortiz, R. E. (2012). Impact of the microbial siderophores and phytosiderophores on the iron assimilation by plants: a synthesis. Revista fitotecnia mexicana, 35(1), 9-21.
Ahmed, E., & Holmström, S. J. (2014). Siderophores in environmental research: roles and applications. Microbial biotechnology, 7(3), 196-208. DOI: https://doi.org/10.1111/1751-7915.12117
Alori, E. T., Babalola, O. O., & Prigent-Combaret, C. (2019). Impacts of microbial inoculants on the growth and yield of maize plant. The Open Agriculture Journal, 13(1).
Beneduzi, A., Ambrosini, A., & Passaglia, L. M. (2012). Plant growth-promoting rhizobacteria (PGPR): their potential as antagonists and biocontrol agents. Genetics and molecular biology, 35, 1044-1051. DOI: https://doi.org/10.1590/S1415-47572012000600020
Benkeblia, N. (2020). Biofortification of edible plants: Set the stage for better nutrition. Vitamins and minerals biofortification of edible plants, 1-25. DOI: https://doi.org/10.1002/9781119511144.ch1
Bertani, G. (1951). Studies on lysogenesis. I. The mode of phage liberation by lysogenic Escherichia coli. J Bacteriol., 62(3):293-300. DOI: https://doi.org/10.1128/jb.62.3.293-300.1951
Buziashvili, A. & Yemets, A. (2022) Lactoferrin and its role in biotechnological strategies for plant defense against pathogens. Transgenic Research. Pp 01-16 DOI:10.1007/s11248-022-00331-9. DOI: https://doi.org/10.1007/s11248-022-00331-9
Bouis, H. E., Hotz, C., McClafferty, B., Meenakshi, J. V., & Pfeiffer, W. H. (2011). Biofortification: a new tool to reduce micronutrient malnutrition. Food and nutrition bulletin, 32(1_suppl1), S31-S40. DOI: https://doi.org/10.1177/15648265110321S105
Brick, J.M., Bostock, R.M. & Silversone, S.E. (1991). Rapid in situ assay for Indole acetic acid production by bacteria immobilized on nitrocellulose membrane. Applied Environmental Microbiology. 57: 535-538. DOI: https://doi.org/10.1128/aem.57.2.535-538.1991
Cavaglieri, L., Orlando, J., & Etcheverry, M. (2009). Rhizosphere microbial community structure at different maize plant growth stages and root locations. Microbiological Research, 164(4), 391-399.
Colombo, C., Palumbo, G., He, J. Z., Pinton, R., & Cesco, S. (2014). Review on iron availability in soil: interaction of Fe minerals, plants, and microbes. Journal of soils and sediments, 14(3), 538-548.
Delaporte-Quintana, P., Lovaisa, N.C. Rapisarda, V.A. & Pedraza, R.O. (2020). The plant growth promoting bacteria Gluconacetobacter diazotrophicus and Azospirillum brasilense contribute to the iron nutrition of strawberry plants through siderophores production. Plant Growth Regulators. 91: 185. DOI: https://doi.org/10.1007/s10725-020-00598-0
Ehsan, S., A. Riaz, M.A. Qureshi, A. Ali, I. Saleem, M. Aftab, K. Mehmood, F. Mujeeb, M.A> Ali, H. Javed, F. Ijaz, A. Haq, K. Rehman and M.U. Saleem. 2022. Isolation, purification and application of siderophore producing bacteria to improve wheat growth. Pakistan Journal of Agricultural Research, 35(2): 449-459. DOI: https://doi.org/10.17582/journal.pjar/2022/35.2.449.459
Ekin, Z., 2019. Integrated use of humic acid and plant growth promoting rhizobacteria to ensure higher potato productivity in sustainable agriculture. Sustainability, 11(12): 3417. DOI: https://doi.org/10.3390/su11123417
Etesami, H., 2020. Halotolerant plant growth promoting bacteria: prospects for alleviating salinity stress in plants. Environmental Experimental Botamy. 178: 104–124. DOI: https://doi.org/10.1016/j.envexpbot.2020.104124
García-Bañuelos, M. L., Sida-Arreola, J. P., & Sánchez, E. (2014). Biofortification-promising approach to increasing the content of iron and zinc in staple food crops. Journal of Elementology, 19(3).
Ghazy, N., & El-Nahrawy, S. (2021). Siderophore production by Bacillus subtilis MF497446 and Pseudomonas koreensis MG209738 and their efficacy in controlling Cephalosporium maydis in maize plant. Archives of microbiology, 203(3), 1195-1209. DOI: https://doi.org/10.1007/s00203-020-02113-5
Glick, B. R. (2012). Plant growth-promoting bacteria: mechanisms and applications. Scientifica, 2012.
Gopalakrishnan, S., Srinivas, V., Sree Vidya, M., & Rathore, A. (2013). Plant growth-promoting activities of Streptomyces spp. in sorghum and rice. SpringerPlus, 2(1), 1-8. DOI: https://doi.org/10.1186/2193-1801-2-574
Gorshkov, V., & Tsers, I. (2022), Plant susceptible responses: the underestimated side of plant–pathogen interactions. Biol. Rev., 97: 45-66 DOI: https://doi.org/10.1111/brv.12789
He, L., Z. Yue, Chen, C. Li, C. Li, J. & Sun, Z. (2020). Enhancing iron uptake and alleviating iron toxicity in wheat by plant growthpromoting bacteria: Theories and practices. International Journal of Agriculture and Biology. 23: 190–196.
Herlihy, J.H., Long, T. A. & McDowell, J.M. (2020). Iron homeostasis and plant immune responses: Recent insights and translational implications. J Biol. Chem., 295(39):13444-13457. DOI: https://doi.org/10.1074/jbc.REV120.010856
Hu, X., Page, M. T., Sumida, A., Tanaka, A., Terry, M. J., & Tanaka, R. (2017). The iron–sulfur cluster biosynthesis protein SUFB is required for chlorophyll synthesis, but not phytochrome signaling. The Plant Journal, 89(6), 1184-1194. DOI: https://doi.org/10.1111/tpj.13455
Islam, F., Yasmeen, T., Ali, Q., Ali, S., Arif, M. S., Hussain, S., & Rizvi, H. (2014). Influence of Pseudomonas aeruginosa as PGPR on oxidative stress tolerance in wheat under Zn stress. Ecotoxicology and Environmental Safety, 104, 285-293. DOI: https://doi.org/10.1016/j.ecoenv.2014.03.008
Jha, C. K., & Saraf, M. (2015). Plant growth promoting rhizobacteria (PGPR). J. Agric. Res. Dev, 5, 108-119.
Johnstone, T. C., & Nolan, E. M. (2015). Beyond iron: non-classical biological functions of bacterial siderophores. Dalton Transactions, 44(14), 6320-6339. DOI: https://doi.org/10.1039/C4DT03559C
Joshi, R. S., Shaikh, S. H., & Joshi, S. S. (2018). Optimization and partial characterization of siderophore produced by Pseudomonas species isolated from agricultural soil. J Glob Biosci, 7(1), 5342-5349.
Kabiraj, A., K. Majhi, U. Halder, Let, M. & Bandopadhyay, R. (2020). Role of plant growthpromoting rhizobacteria (PGPR) for crop stress management. In: Sustainable agriculture in the era of climate change. Springer, Cham. pp. 367-389. DOI: https://doi.org/10.1007/978-3-030-45669-6_17
Kapoore, R. V., Huete-Ortega, M., Day, J. G., Okurowska, K., Slocombe, S. P., Stanley, M. S., & Vaidyanathan, S. (2019). Effects of cryopreservation on viability and functional stability of an industrially relevant alga. Scientific Reports, 9(1), 1-12. DOI: https://doi.org/10.1038/s41598-019-38588-6
Kaur, T., Rana, K.L. Kour, D. Sheikh, I. Yadav, N. Kumar, V. Yadav, A.N. Dhaliwal, H.S. & Saxena, A.K. (2020). Microbe-mediated biofortification for micronutrients: Present status and future challenges. In: New and Future Developments in Microbial Biotechnology and Bioengineering. Elsevier, pp. 1-17. DOI: https://doi.org/10.1016/B978-0-12-820528-0.00002-8
Khan, A., Singh, J., Upadhayay, V. K., Singh, A. V., & Shah, S. (2019). Microbial biofortification: a green technology through plant growth promoting microorganisms. In Sustainable green technologies for environmental management (pp. 255-269). Springer, Singapore.
Kim, S. A., & Guerinot, M. L. (2007). Mining iron: iron uptake and transport in plants. FEBS letters, 581(12), 2273-2280.
King, E. D.,Ward M. K, Raney, D.E. (1954). Two simple media for the demonstration of pyocyanin and fluorescin. Journal of Laboratory and Clinical Medicine 44, 301–7.
Kobayashi, T., & Nishizawa, N. K. (2012). Iron uptake, translocation, and regulation in higher plants. Annu Rev Plant Biol, 63(1), 131-152. DOI: https://doi.org/10.1146/annurev-arplant-042811-105522
Kotasthane, A.S., Agrawal, T. Zaidi, N.W. & Singh, U. (2017). Identification of siderophore producing and cynogenic fluorescent Pseudomonas and a simple confrontation assay to identify potential bicontrol agent for collar rot of chickpea. Biotechnology. 7(3): 1-8. DOI: https://doi.org/10.1007/s13205-017-0761-2
Kumar, P., Pandey, P., Dubey, R. C., & Maheshwari, D. K. (2016). Bacteria consortium optimization improves nutrient uptake, nodulation, disease suppression and growth of the common bean (Phaseolus vulgaris) in both pot and field studies, Rhizosphere, 2, 13-23. DOI: https://doi.org/10.1016/j.rhisph.2016.09.002
Kumari, S., S. Kiran, S. Kumari, P. Kumar and A. Singh. 2021. Optimization of Siderophore production by bacillus subtilis DR2 and its Effect on growth of Coriandrum Sativum. Res. Sq., https://doi.org/10.21203/rs.3.rs-567897/v1 DOI: https://doi.org/10.21203/rs.3.rs-567897/v1
López-Reyes, L., Carcaño-Montiel, M. G., Lilia, T. L., Medina-de la Rosa, G., & Armando, T. H. R. (2017). Antifungal and growth-promoting activity of Azospirillum brasilense in Zea mays L. ssp. Mexicana. Archives of Phytopathology and Plant Protection, 50(13-14), 727-743. DOI: https://doi.org/10.1080/03235408.2017.1372247
Milagres, A.M.F., Napoleao, D & Machuca, A. (1999). Detection of siderophore production from several fungi and bacteria by a modification of chrome azurol S (CAS) agar plate assay. J. Microbiol. Method, 37: 1-6. DOI: https://doi.org/10.1016/S0167-7012(99)00028-7
Mushtaq, Z., Faizan, S., & Hussain, A. (2021). Role of microorganisms as biofertilizers. In Microbiota and Biofertilizers (pp. 83-98). Springer, Cham. DOI: https://doi.org/10.1007/978-3-030-48771-3_6
Nozoye, T., Nagasaka, S., Kobayashi, T., Takahashi, M., Sato, Y., Sato, Y., ... & Nishizawa, N. K. (2011). Phytosiderophore efflux transporters are crucial for iron acquisition in graminaceous plants. Journal of Biological Chemistry, 286(7), 5446-5454.
Radzki, W., F.G. Manero, E. Algar, J.L. Garcia, A. Garcia-Villaraco and B.R. Solano. 2013. Bacterial siderophores efficiently provide iron to iron starved tomato plants in hydroponics culture. Antonie Van Leeuwenhoek, 104(3): 321–330. DOI: https://doi.org/10.1007/s10482-013-9954-9
Rana, A., Joshi, M., Prasanna, R., Shivay, Y. S., & Nain, L. (2012). Biofortification of wheat through inoculation of plant growth promoting rhizobacteria and cyanobacteria. European Journal of Soil Biology, 50, 118-126.
Riaz, U., M. Ghulam, A. Wajiha, S. Tayyaba, S. Muhammad, M. Nazir and M. Zulqernain. 2021. Plant growth-promoting rhizobacteria (PGPR) as biofertilizers and biopesticides. In: Microbiota and Biofertilizers. Spinger, pp.181-196. DOI: https://doi.org/10.1007/978-3-030-48771-3_11
Roriz, M., Carvalho, S. M., Castro, P. M., & Vasconcelos, M. W. (2020). Legume biofortification and the role of plant growth-promoting bacteria in a sustainable agricultural era. Agronomy, 10(3), 435. DOI: https://doi.org/10.3390/agronomy10030435
Saha, M., Sarkar, S., Sarkar, B., Sharma, B. K., Bhattacharjee, S., & Tribedi, P. (2016). Microbial siderophores and their potential applications: a review. Environmental Science and Pollution Research, 23(5), 3984-3999. DOI: https://doi.org/10.1007/s11356-015-4294-0
Satish, L., S. Shamili, Yolcu, S. Lavanya, G. Alavilli, H. & Swamy, M.K. (2020). Biosynthesis of secondary metabolites in plants as influenced by different factors. In: (ed. M. Swamy Plant derived bioactives. Springer, Singapore. pp.61–100. DOI: https://doi.org/10.1007/978-981-15-1761-7_3
Schalk, I. J., & Mislin, G. L. (2017). Bacterial iron uptake pathways: gates for the import of bactericide compounds. Journal of medicinal chemistry, 60(11), 4573-4576.
Schwabe, R., Senges, C. H. R., Bandow, J. E., Heine, T., Lehmann, H., Wiche, O., & Tischler, D. (2020). Cultivation dependent formation of siderophores by Gordonia rubripertincta CWB2. Microbiological Research, 238, 126481. DOI: https://doi.org/10.1016/j.micres.2020.126481
Singh, D., and R. Prasanna. 2020. Potential of microbes in the biofortification of Zn and Fe in dietary food grains. A review. Agron. Sustainable Development. 40: 1–21. DOI: https://doi.org/10.1007/s13593-020-00619-2
Tsai, H. H., & Schmidt, W. (2017). Mobilization of iron by plant-borne coumarins. Trends in Plant Science, 22(6), 538-548.
Vacheron, J., Moënne-Loccoz, Y., Dubost, A., Gonçalves-Martins, M., Muller, D., & Prigent-Combaret, C. (2016). Fluorescent Pseudomonas strains with only few plant-beneficial properties are favored in the maize rhizosphere. Frontiers in plant science, 7, 1212. DOI: https://doi.org/10.3389/fpls.2016.01212
Velu, G., & Singh, R. P. (2019). Genomic approaches for biofortification of grain zinc and iron in wheat. In Quality breeding in field crops (pp. 193-198). Springer, Cham.
Zhao, Q. Y., Xu, S. J., Zhang, W. S., Zhang, Z., Yao, Z., Chen, X. P., & Zou, C. Q. (2020). Identifying key drivers for geospatial variation of grain micronutrient concentrations in major maize production regions of China. Environmental Pollution, 266, 115114. DOI: https://doi.org/10.1016/j.envpol.2020.115114
Zarei, T., Moradi, A., Kazemeini, S. A., Akhgar, A., & Rahi, A. A. (2020). The role of ACC deaminase producing bacteria in improving sweet corn (Zea mays L. var saccharata) productivity under limited availability of irrigation water. Scientific reports, 10(1), 1-12. DOI: https://doi.org/10.1038/s41598-020-77305-6
Zulfiqar, U., Maqsood, M., Hussain, S., & Anwar-ul-Haq, M. (2020). Iron nutrition improves productivity, profitability, and biofortification of bread wheat under conventional and conservation tillage systems. Journal of soil science and plant nutrition, 20(3), 1298-1310. DOI: https://doi.org/10.1007/s42729-020-00213-1
Zunjare, R. U., Chhabra, R., Hossain, F., Baveja, A., Muthusamy, V., & Gupta, H. S. (2018). Molecular characterization of 5′ UTR of the lycopene epsilon cyclase (lcyE) gene among exotic and indigenous inbreds for its utilization in maize biofortification. 3 Biotech, 8(1), 1-9.
Yavarian, S., Jafari, P. Akbari, N. & Feizabadi, M.M. (2021). Selective screening and characterization of plant growth promoting bacteria for growth enhancement of tomato, Lycopersicon esculentum. Iran. Journal of Microbiology. 13(1): 121. DOI: https://doi.org/10.18502/ijm.v13i1.5502
Yadav, R., P. Ror, P. Rathore, S. Kumar and W. Ramakrishna. 2020. Bacillus subtilis CP4, isolated from native soil in combination with arbuscular mycorrhizal fungi promotes biofortification, yield and metabolite production in wheat under field conditions. Journal of Applied Microbiology. 131: 339–359. DOI: https://doi.org/10.1111/jam.14951
Aguado-Santacruz, G. A., Moreno-Gómez, B., Jiménez-Francisco, B., García-Moya, E., & Preciado-Ortiz, R. E. Impact of the microbial siderophores and phytosiderophores on the iron assimilation by plants: a synthesis. Revista fitotecnia mexicana, 35(1), 9-21(2012). DOI: https://doi.org/10.35196/rfm.2012.1.9
Alori, E. T., Babalola, O. O., & Prigent-Combaret, C. Impacts of microbial inoculants on the growth and yield of maize plant. The Open Agriculture Journal, 13(1)(2019). DOI: https://doi.org/10.2174/1874331501913010001
Cavaglieri, L., Orlando, J., & Etcheverry, M. Rhizosphere microbial community structure at different maize plant growth stages and root locations. Microbiological Research, 164(4), 391-399(2009). DOI: https://doi.org/10.1016/j.micres.2007.03.006
Colombo, C., Palumbo, G., He, J.-Z., Pinton, R., & Cesco, S. Review on iron availability in soil: interaction of Fe minerals, plants, and microbes. Journal of soils and sediments, 14(3), 538-548(2014). DOI: https://doi.org/10.1007/s11368-013-0814-z
García-Bañuelos, M. L., Sida-Arreola, J. P., & Sánchez, E. Biofortification-promising approach to increasing the content of iron and zinc in staple food crops. Journal of Elementology, 19(3)(2014).
Glick, B. R. Plant growth-promoting bacteria: mechanisms and applications. Scientifica, 2012(2012). DOI: https://doi.org/10.6064/2012/963401
Jha, C. K., & Saraf, M. Plant growth promoting rhizobacteria (PGPR). J. Agric. Res. Dev, 5, 108-119(2015).
Khan, A., Singh, J., Upadhayay, V. K., Singh, A. V., & Shah, S. Microbial biofortification: a green technology through plant growth promoting microorganisms Sustainable green technologies for environmental management (pp. 255-269): Springer.(2019) DOI: https://doi.org/10.1007/978-981-13-2772-8_13
Kim, S. A., & Guerinot, M. L. Mining iron: iron uptake and transport in plants. FEBS letters, 581(12), 2273-2280(2007). DOI: https://doi.org/10.1016/j.febslet.2007.04.043
Nozoye, T., Nagasaka, S., Kobayashi, T., Takahashi, M., Sato, Y., Sato, Y., . . . Nishizawa, N. K. Phytosiderophore efflux transporters are crucial for iron acquisition in graminaceous plants. Journal of Biological Chemistry, 286(7), 5446-5454(2011). DOI: https://doi.org/10.1074/jbc.M110.180026
Rana, A., Joshi, M., Prasanna, R., Shivay, Y. S., & Nain, L. Biofortification of wheat through inoculation of plant growth promoting rhizobacteria and cyanobacteria. European Journal of Soil Biology, 50, 118-126(2012). DOI: https://doi.org/10.1016/j.ejsobi.2012.01.005
Schalk, I. J., & Mislin, G. L. Bacterial iron uptake pathways: gates for the import of bactericide compounds (Vol. 60, pp. 4573-4576).(2017). ACS Publications. DOI: https://doi.org/10.1021/acs.jmedchem.7b00554
Tsai, H. H., & Schmidt, W. Mobilization of iron by plant-borne coumarins. Trends in Plant Science, 22(6), 538-548(2017). DOI: https://doi.org/10.1016/j.tplants.2017.03.008
Velu, G., & Singh, R. P. Genomic approaches for biofortification of grain zinc and iron in wheat Quality breeding in field crops (pp. 193-198): Springer.(2019) DOI: https://doi.org/10.1007/978-3-030-04609-5_9
Zunjare, R. U., Chhabra, R., Hossain, F., Baveja, A., Muthusamy, V., & Gupta, H. S. Molecular characterization of 5′ UTR of the lycopene epsilon cyclase (lcyE) gene among exotic and indigenous inbreds for its utilization in maize biofortification. 3 Biotech, 8(1), 1-9(2018). DOI: https://doi.org/10.1007/s13205-018-1100-y
Published
How to Cite
Issue
Section
License
Copyright (c) 2023 shabana ehsan, Amjad Qureshi, Neelam Chaudhary, Asif Ali, Abid Niaz, Hina Javed, Fraza Ijaz, Shakeel Ahmed Anwar
This work is licensed under a Creative Commons Attribution 4.0 International License.