Effect of Fluorescent-Producing Rhizobacteria on Cereal Growth Through Siderophore Exertion

Authors

  • Shabana Ehsan Ayub Agricultural Research Institute, Faisalabad, Pakistan
  • Amjad Qureshi Ayub Agricultural Research Institute, Faisalabad, Pakistan image/svg+xml
  • Neelam Chaudhary University of Agriculture, Faisalabad
  • Asif Ali Soil Science Research Unit image/svg+xml
  • Abid Niaz Ayub Agricultural Research Institute, Faisalabad, Pakistan image/svg+xml
  • Hina Javed Ayub Agricultural Research Institute, Faisalabad, Pakistan image/svg+xml
  • Fraza Ijaz Ayub Agricultural Research Institute, Faisalabad, Pakistan image/svg+xml
  • Shakeel Ahmed Anwar Ayub Agricultural Research Institute, Faisalabad, Pakistan image/svg+xml

DOI:

https://doi.org/10.38211/joarps.2023.04.02.168

Keywords:

Siderophore, Fluorescence, Wheat, Maize, Iron solubilization, Rhizobacteria

Abstract

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

Download data is not yet available.

Metrics

Metrics Loading ...

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

Downloads

Published

2023-05-26

How to Cite

Ehsan, S., Qureshi, A., Chaudhary, N., Ali, A., Niaz, A., Javed, H., … Anwar, S. A. (2023). Effect of Fluorescent-Producing Rhizobacteria on Cereal Growth Through Siderophore Exertion. Journal of Applied Research in Plant Sciences , 4(02), 601–611. https://doi.org/10.38211/joarps.2023.04.02.168