Bioprospecting of elite plant growth-promoting bacteria for the maize crop
Abstract
The use of plant growth-promoting bacteria (PGPB), which aims to replace chemical fertilizers and biological control, is a goal for achieving agriculture sustainability. In this scenario, our goal was to identify and evaluate the potential of bacteria isolated from maize roots to promote plant growth and be used as inoculants. We evaluated 173 bacterial strains isolated from the maize (Zea mays L.) rhizosphere for the properties of their PGPB in vitro. Twelve strains were positive for siderophores, indole acetic acid (IAA) production, biological nitrogen fixation (BNF), and phosphate solubilization. Sequence analysis of 16S rRNA identified these strains as belonging to the genera Cellulosimicrobium, Stenotrophomonas, Enterobacter, and Bacillus. The elite strains were evaluated under greenhouse conditions upon the inoculation of two maize hybrids, ATL100 and KWX628. The ability of the isolates to promote plant growth was dependent on the maize genotype; Enterobacter sp. LGMB208 showed the best ability to promote growth of hybrid ATL100, while Enterobacter sp. strains LGMB125, LGMB225, and LGMB274 and Cellulosimicrobium sp. strain LGMB239 showed the best ability to promote growth of hybrid KWX628. The results highlight the potential of bacterial genera little explored as maize PGPB but indicate the need to investigate their interactions with different plant genotypes.
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Ahemad, M., & Kibret, M. (2014). Mechanisms and applications of plant growth promoting rhizobacteria: current perspective. Journal of King Saud University Science, 26(1), 1-20. DOI: 10.1016/j.jksus.2013.05.001
Alavi, P., Muller, H., Cardinale, M., Zachow, C., Sanchez, M. B., Martinez, J. L., & Berg, G. (2013). The DSF quorum sensing system controls the positive influence of Stenotrophomonas maltophilia on plants. PLoS ONE, 8(7), 7-8. DOI: 10.1371/journal.pone.0067103
Araújo, L. M., Monteiro, R. A., Souza, E. M., Steffens, M. B., Rigo, L. U., Pedrosa, F. O., & Chubastsu, L. S. (2004) GlnB is specifically required for Azospirillum brasilense NifA activity in Escherichia coli. Research in Microbiology, 155(6), 491-495. DOI: 10.1016/j.resmic.2004.03.002
Armada, E., Probanza, A., Roldanc, A., & Azcona, R. (2016). Native plant growth promoting bacteria Bacillus thuringiensis and mixed or individual mycorrhizal species improved drought tolerance and oxidative metabolism in Lavandula dentata plants. Journal of Plant Physiology, 192, 1-12. DOI: 10.1016/j.jplph.2015.11.007
Beneduzi, A., Ambrosini, A. A., & Passaglia, M. P. (2012). Plant growth-promoting rhizobacteria (PGPR): their potential as antagonists and biocontrol agents. Genetic and Molecular Biology, 35(Suppl. 4), 1044-1051. DOI: 10.1590/s1415-47572012000600020
Broughton, W. J., & Dilworth, M.J. (1971). Control of leghaemoglobin synthesis in snake beans. Biochemistry Journal, 125(4), 1075-1080. DOI: 10.1042/bj1251075
Cardoso, J. D., Hungria, M., & Andrade, D. S. (2012). Polyphasic approach for the characterization of rhizobial symbionts effective in fixing N2 with common bean (Phaseolus vulgaris L.). Applied Microbiology and Biotechnology, 93(5), 2035-2049. DOI: 10.1007/s00253-011-3708-2
Chagas Jr., A. F., Oliveira, L. A., Oliveira, A. N., & Willerding, A. L. (2010). Capacidade de solubilização de fosfatos e eficiência simbiótica de rizóbios isolados de solos da Amazônia. Acta Scientiarum. Agronomy, 32(2), 359-366. DOI: 10.4025/actasciagron.v32i2.3185.
Chaiharn, M., Chunhaleuchanon, S., & Lumyong, S. (2009). Screening siderophore produing bacteria as potential biological control agent for fungal rice pathogens in Thailand. World Journal of Microbiology and Biotechnology, 25(11), 1919-1928. DOI: 10.1007/s11274-009-0090-7
Chaiharn, M., & Lumyong, S. (2011). Screening and optimization of indole-acetic-acid production and phosphate solubilization from rhizobacteria aimed at improving plant growth. Current Microbiology, 62(1), 173-181. DOI: 10.1007/s00284-010-9674-6
Chen, Y., Chao, Y., Lin, Q., Bai, J., Tang, L., Wang, S., … Qiu, R. (2016). Survival strategies of the plant-associated bacterium Enterobacter sp. strain EG16 under cadmiun stress. Applied Environmental and Microbiology, 82(6), 174-1744. DOI: 10.1-28/AEM.03689-15
Deepa, C. K., Dastager, S. G., & Pandey, A. (2010). Isolation and characterization of plant growth promoting bacteria from non-rhizospeheric soil and their effect on cowpea (Vinaun guiculata L. Walp.) seedling growth. World Journal of Microbiology and Biotechnology, 26(7), 1233-1240. DOI: 10.1007/s11274-009-0293-y
Döbereiner, J., Day, J. M., & Dart, P. J. (1972) Nitrogenase Activity and Oxygen Sensitivity of the Paspalum notatum-Azotobacter paspali Association. Journal of General Microbiology, 71(1), 103-116. DOI: 10.1099/00221287-71-1-103
Fukami, J., Nogueira, M. A., Araujo, R. S., & Hungria, M. (2016). Accessing inoculation methods of maize and wheat with Azospirillum brasilense. AMB Express, 6(3), 1-13. DOI: 10.1186/s13568-015-0171-y
Fukami, J., Ollero, F. J., Megías, M., & Hungria, M. (2017). Phytohormones and induction of plant-stress tolerance and defense genes by seed and foliar inoculation with Azospirillum brasilense cells and metabolites promote maize growth. AMB Express, 7(153), 1-13. DOI: 10.1186/s13568-017-0453-7
Hall, T. A. (1999). BioEdit: a user-friendly biological sequence alignment editor and analysis program for.95/98/NT version 7.2.5. Nucleic Acids Symposium Series, 41(1), 95-98.
Halvorson, A. D., Peterson, G. A., & Reule, C. A. (2002). Tillage system and crop rotation effects on dry land crop yields and soil carbon in the central great plains. Agronomy Journal, 94(6), 1429-1436. DOI: 10.2134/agronj2002.1429
Hoffmann, H., Stindl, S., Stumpf, A., Mehlen, A., Monget, D., Heesemann, J., … Roggenkamp, A. (2005). Description of Enterobacter ludwigii sp. nov., a novel Enterobacter species of clinical relevance. Systematic Applied Microbiology, 28(3), 206-212. DOI: 10.1016/j.syapm.2004.12.009
Hungria, M., Campo, R. J., Souza, E. M., & Pedrosa, F. O. (2010). Inoculation with selected strains of Azospirillum brasilense and A. lipoferum improves yields of maize and wheat in Brazil. Plant Soil, 331(1), 413-425. DOI: 10.1007/s11104-009-0262-0
Ikeda, A., Bassani, L. L., Adamoski, D., Stringari, D., Cordeiro, V. K., Glienke, C., ... Galli-Terasawa, L. (2013). Morphological and genetic characterization of endophytic bacteria isolated from roots of different maize genotypes. Microbiology and Ecology, 65(1), 154-160. DOI: 10.1007/s00248-012-0104-0
Islam, S., Akanda, A. M., Prova, A., Islam, M. T., & Hossain, M. M. (2016). Isolation and identification of plant growth promoting rhizobacteria from cucumber rhizosphere and their effect on plant growth promotion and disease suppression. Frontiers in Microbiology, 6, 1-12. DOI: 10.3389/fmicb.2015.01360
Karthik, C., Oves, M., Thangabalu, R., Sharma, R., Santhosh, S.B., & Arulselvi, I. P. (2016). Cellulosimicrobium funkei-like enhances the growth of Phaseolus vulgaris by modulating oxidative damage under Chromium (VI) toxicity. Journal of Advanced Research, 7(6), 839-850. DOI: 10.1016/j.jare.2016.08.007
Kavamura, V. N., Santos, S. N., Silva, J. L., Parma, M. M., Avila, L. A., Visconti, A., ... Melo, I. S. (2013). Screening of Brazilian cacti rhizobacteria for plant growth promotion under drought. Microbial Research, 168(4), 183-191. DOI: 10.1016/j.micres.2012.12.002
Kearse, M., Moir, R., Wilson, A., Stones-Havas, S., Cheung, M., Sturrock, S., … Drummond, A. (2012). Genious basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics, 28(12), 1647-1649. DOI: 10.1093/bioinformatics/bts199
Kumar, N. P., & Audipudi, A. V. (2015). Exploration of a novel plant growth promoting bacteria Stenotrophomonas maltophilia AVP27 isolated from the chilli rhizosphere soil. International Journal of Engineering Research and General Science, 3(1), 265-273.
Kundan, R., Pant, G., Jadon, N., & Agrawal, P. K. (2015). Plant growth promoting rhizobacteria: mechanism and current prospective. Journal of Agriculture and Science and Food, 6(2), 1-9. DOI: 10.4172/2471-2728.1000155
Kuss, A. V., Kuss, V. V., Lovato, T., & Flores, M. L. (2007). Fixação de nitrogênio e produção de ácido indol acético in vitro por bactérias diazotróficas endofíticas. Pesquisa Agropecuária Brasileira, 42(10), 1459-1465. DOI: 10.1590/S0100-204X2007001000013
Lana, M. C., Dartora, J., Marini, D., & Hann, J. E. (2012). Inoculation with Azospirillum, associated with nitrogen fertilization in maize. Revista Ceres, 59(3), 1-7. DOI: 10.1590/S0034-737X2012000300016
Li, H., Huang, W., Xu, L., Zhou, X., Liu, H., & Cheng, Z. (2016). Stenotrophomonas maltophilia HW2 enhanced cucumber resistance against cucumber green mottle mosaic virus. Journal of Plant Biology, 59, 488-495. DOI: 10.1007/s12374-016-0246-6.
Lin, L., Li, Z., Hu, C., Zhang, X., Chang, S., Yang, L., … An, Q. (2012). Plant growth-promoting nitrogen-fixing enterobacteria are in association with sugarcane plants growing in Guangxi, China. Microbes Environments, 27(4), 391-398. DOI: 10.1264/jsme2.ME11275
Majeed, A., Abbasi, M. K., Hameed, S., Imran, A., & Rahim, N. (2015). Isolation and characterization of plant growth promoting rhizobacteria from wheat rhizosphere and their effect on plant growth promotion. Frontiers in Microbiology, 6, 1-10. DOI: 10.3389/fmicb.2015.00198
Menna, P., Hungria, M., Barcellos, F. G., Bangel, E. V., Hess, P. N., & Martinez-Romero, E. (2006). Molecular phylogeny based on the 16S rRNA gene of elite rhizobial strains used in Brazilian commercial inoculants. Systematic and Applied Microbiology, 29(4), 315-332. DOI: 10.1016/j.syapm.2005.12.002
Miethke, M., & Marahiel, M. A. (2007). Siderophore-based iron acquisition and pathogen control. Microbiology and Molecular Biology Review, 71(3), 413-451. DOI: 10.1128/MMBR.00012-07
Montañez, A., & Sicardi, M. (2013). Effects of inoculation on growth promotion and biological nitrogen fixation in maize (Zea mays L.) under greenhouse and field conditions. Basic Research Journal of Agricultural Science and Review, 2(4), 102-110.
Nautiyal, C. S., Srivastava, S., Chauhan, P. S., Seem, K., Mishra, A., & Sopory, S. K. (2013). Plant growth-promoting bacteria Bacillus amyloliquefaciens NBRISN13 modulates gene expression profile of leaf and rhizosphere community in rice during salt stress. Plant Physiology and Biochemistry, 66, 1-9. DOI: 10.1016/j.plaphy.2013.01.020
Olibone, D., & Rosolem, C. A. (2010). Phosphate fertilization and phosphorus forms in an Oxisol under no-till. Scientia Agricola, 67(4), 465-471. DOI: 10.1590/S0103-90162010000400014
Rambaut, A. (2012). Tree Figure Drawing Tool Version 1.4.0. Edinburgh, UK: University of Edinburgh.
Reena, A., Aysha, O. S., Valli, S., Nirmala, P., & Vinothkumar, P. (2013). Isolation of siderophore producing bacteria from rhizosphere soil and their antagonistic activity against selected fungal plant pathogens. International Journal of Current Microbiology and Applied Sciences, 2(1), 59-65.
Rodrigues Neto, J., Malavolta Jr., V. A., & Victor, O. (1986). Meio simples para o isolamento e cultivo de Xanthomonas campestris pv. citri tipo B. Summa Phytopathologica, 12(1-2), 16.
Sambrook, J., Fritsch, E. F., & Maniatis, T. (1989). Molecular cloning: A laboratory manual (2. ed.). New York, US: Cold Spring Harbor Laboratory Press.
Schwyn, B., & Neilands, J. B. (1987). Universal assay for the detection and determination of siderophores. Analytical Biochemistry, 160(1), 47-56. DOI: 10.1016/0003-2697(87)90612-9
Sharma, S. B., Sayyed, R. Z., Trivedi, M. H., & Gobi, T. A. (2013). Phosphate solubilizing microbes: sustainable approach for managing phosphorus deficiency in agricultural soils. Srpingerplus, 2, 1-14. DOI: 10.1186/2193-1801-2-587
Sharma, S., Kulkarni, J., & Jha, B. (2016). Halotolerant rhizobacteria promote growth and enhance salinity tolerance in peanut. Frontiers in Microbiology, 7, 1-11. DOI: 10.3389/fmicb.2016.01600
Shoebitz, M., Ribaudo, C. M., Parodo, M. A., Cantore, M. L., Ciampi, L., & Cura, J. A. (2009). Plant growth promoting properties of a strain of Enterobacter ludwigii isolated from Lolium perenne rhizosphere. Soil Biology and Biochmestry, 41, 1768-1774. DOI: 10.1016/j.soilbio.2007.12.031
Silva, F. A., & Azevedo, C. A. V. (2016). The Assistat Software Version 7.7 and its use in the analysis experimental data. African Journal of Agricultural Research, 11(39), 3733-3740. DOI: 10.5897/ajar2016.11522
Singh, R. P. (2013). Isolation and characterization of multifarious plant growth promoting bacteria Enterobacter ludwigii PGP 19 isolated form pearl millet. International Journal of Science and Research, 4(6), 261-265.
Singh, P., Kumar, V., & Agrawal, S. (2014). Evaluation of phytase producing bacteria for their plant growth promoting activities. International Journal of Microbiology, 1, 1-7. DOI: 10.1155/2014/426483.
Souza, R. de, Ambosini, A., & Passaglia, L. M. P. (2015). Plant growth-promoting bacteria as inoculants in agricultural soils. Genetics and Molecular Biology, 38(4), 401-419. DOI: 10.1590/S1415-475738420150053
Sultanpuram, V. R., Mothe, T., Chintalapati, S., & Chintalapati, V. R. (2015). Cellulosimicrobium aquatile sp. nov., isolated from Panagal reservoir, Nalganda, India. Antonie Leeuwenhoek, 108(6), 1357-1364. DOI: 10.1007/s10482-015-0588-y
Szilagyi-Zecchin, V. J., Ikeda, A. C., & Mógor, A. F. (2017). Contribution of plant growth-promoting bacteria to the maize yield. In H. B. Singh, B. K. Sarma, & C. Keswani (Ed.). Advances in PGPR Research (p. 234-245). Boston, US: CABI.
Tamura, K., Stecher, G., Peterson, D., Filipski, A., & Kumar, S. (2013) MEGA6: Molecular Evolutionary Genetics Analysis version 6.0. Molecular Biology and Evolution, 30(12), 2725-2729. DOI: 10.1093/molbey/mst197
Yazdani, M., Bahamanyar, M. A., Pirdashti, H., & Esmaili, M. A. (2009). Effect of phosphate solubilization microorganisms (PSM) and plant growth promoting Rhizobacteria (PGPR) on yield and yield components of corn (Zea mays L.). International Journal of Agriculture and Biological Engineering, 3(1), 50-52.
Zahid, M., Abbasi, M. K., Hameed, S., & Rahim, N. (2015). Isolation and identification of indigenous plant growth promoting rhizobacteria from Himalayan region of Kashmir and their effect on improving growth and nutrient contents of maize (Zea mays L.). Frontiers in Microbiology, 6, 1-10. DOI: 10.3389/fmicb.2015.00207
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