AS  Vol.10 No.12 , December 2019
Effect of Plant Growth-Promoting Rhizobacteria at Various Nitrogen Rates on Corn Growth
Abstract: Plant growth-promoting rhizobacteria (PGPR) colonize plant roots and promote plant growth by producing and secreting various chemical regulators in the rhizosphere. With the recent interest in sustainable agriculture, an increasing number of researchers are investigating ways to improve the efficiency of PGPR use to reduce chemical fertilizer inputs needed for crop production. Accordingly, greenhouse studies were conducted to evaluate the impact of PGPR inoculants on biomass production and nitrogen (N) content of corn (Zea mays L.) under different N levels. Treatments included three PGPR inoculants (two mixtures of PGPR strains and one control without PGPR) and five N application levels (0%, 25%, 50%, 75%, and 100% of the recommended N rate of 135 kg N ha−1). Results showed that inoculation of PGPR significantly increased plant height, stem diameter, leaf area, and root morphology of corn compared to no PGPR application under the same N levels at the V6 growth stage, but few differences were observed at the V4 stage. PGPR with 50% of the full N rate produced corn biomass and N concentrations equivalent to or greater than that of the full N rate without inoculants at the VT stage. In conclusion, mixtures of PGPR can potentially reduce inorganic N fertilization without affecting corn plant growth parameters. Future research is needed under field conditions to determine if these PGPR inoculants can be integrated as a bio-fertilizer in crop production nutrient management strategies.
Cite this paper: Lin, Y. , Watts, D. , Kloepper, J. , Adesemoye, A. and Feng, Y. (2019) Effect of Plant Growth-Promoting Rhizobacteria at Various Nitrogen Rates on Corn Growth. Agricultural Sciences, 10, 1542-1565. doi: 10.4236/as.2019.1012114.

[1]   Malik, A.S., Boyko, O., Atkar, N. and Young, W.F. (2001) A Comparative Study of MR Imaging Profile of Titanium Pedicle Screws. Acta Radiologica, 42, 291-293.

[2]   Hu, T. and Desai, J.P. (2004) Soft-Tissue Material Properties under Large Deformation: Strain Rate Effect. Proceedings of the 26th Annual International Conference of the IEEE EMBS, San Francisco, CA, 1-5 September 2004, 2758-2761.

[3]   Ortega, R., Loria, A. and Kelly, R. (1995) A Semiglobally Stable Output Feedback PI2D Regulator for Robot Manipulators. IEEE Transactions on Automatic Control, 40, 1432-1436.

[4]   Wit, E. and McClure, J. (2004) Statistics for Microarrays: Design, Analysis, and Inference. 5th Edition, John Wiley & Sons Ltd., Chichester.

[5]   Prasad, A.S. (1982) Clinical and Biochemical Spectrum of Zinc Deficiency in Human Subjects. In: Prasad, A.S., Ed., Clinical, Biochemical and Nutritional Aspects of Trace Elements, Alan R. Liss, Inc., New York, 5-15.

[6]   Giambastiani, B.M.S. (2007) EvoluzioneIdrologicaedIdrogeologica Della Pineta di san Vitale (Ravenna). Ph.D. Thesis, Bologna University, Bologna.

[7]   Wu, J.K. (1994) Two Problems of Computer Mechanics Program System. Proceedings of Finite Element Analysis and CAD, Peking University Press, Beijing, 9-15.

[8]   Honeycutt, L. (1998) Communication and Design Course.

[9]   Wright, O. and Wright, W. (1906) Flying-Machine. US Patent No. 821393.

[10]   Tilman, D (1998). The Greening of the Green Revolution. Nature, 396, 211-212.

[11]   Gadagi, R.S., Krishnaraj, P.U., Kulkarni, J.H. and Sa, T. (2004) The Effect of Combined Azospirillum Inoculation and Nitrogen Fertilizer on Plant Growth Promotion and Yield Response of the Blanket Flower Gaillardia pulchella. Scientia Horticulturae, 100, 323-332.

[12]   Adesemoye, A.O., Torbert, H.A. and Kloepper, J.W. (2008) Enhanced Plant Nutrient Use Efficiency with PGPR and AMF in an Integrated Nutrient Management System. Canadian Journal of Microbiology, 54, 876-886.

[13]   Adesemoye, A.O. and Kloepper, J.W. (2009) Plant-Microbes Interactions in Enhanced Fertilizer-Use Efficiency. Applied Microbiology and Biotechnology, 85, 1-12.

[14]   Cong, P.T., Dung, T.D., Hien, T.M., Hien, N.T., Choudhury, A.T., Kecskes, M.L. and Kennedy, I.R. (2009) Inoculant Plant Growth-Promoting Microorganisms Enhance Utilization of Urea-N and Grain Yield of Paddy Rice in Southern Vietnam. European Journal of Soil Biology, 45, 52-61.

[15]   Ahmad, S., Imran, M., Hussain, S., Mahmood, S., Hussain, A. and Hasnain, M. (2017) Bacterial Impregnation of Mineral Fertilizers Improves Yield and Nutrient Use Efficiency of Wheat. Journal of the Science of Food and Agriculture, 97, 3685-3690.

[16]   Kloepper, J.W., Lifshitz, R. and Zablotowicz, R.M. (1989) Free Living Bacterial Inocula for Enhancing Crop Productivity. Trends in Biotechnology, 7, 39-44.

[17]   Kloepper, J.W., Zablotowick, R.M., Tipping, E.M. and Lifshitz, R. (1991) Plant Growth Promotion Mediated by Bacterial Rhizosphere Colonizers. In: Keister, D.L. and Cregan, P.B., Eds., The Rhizosphere and Plant Growth, Kluwer Academic Press, Dordrecht.

[18]   Canbolat, M.Y., Bilen, S., Çakmakçi, R., Şahin, F. and Aydin, A. (2006) Effect of Plant Growth-Promoting Bacteria and Soil Compaction on Barley Seedling Growth, Nutrient Uptake, Soil Properties and Rhizosphere Microflora. Biology and Fertility of Soils, 42, 350-357.

[19]   Adesemoye, A.O., Torbert, H.A. and Kloepper, J.W. (2009) Plant Growth-Promoting Rhizobacteria Allow Reduced Application Rates of Chemical Fertilizers. Microbial Ecology, 58, 921-929.

[20]   Figueiredo, M., Seldin, L., Araujo, F. and Mariano, R. (2010) Plant Growth Promoting Rhizobacteria: Fundamentals and Applications. In: Maheshwari, D.K., Ed, Plant Growth and Health Promoting Bacteria, Springer, Berlin, 21-43.

[21]   Kumar, S., Pandey, P. and Maheshwari, D.K. (2009) Reduction in Dose of Chemical Fertilizers and Growth Enhancement of Sesame (Sesamum indicum L.) with Application of Rhizospheric Competent Pseudomonas Aeruginosa LES4. European Journal of Soil Biology, 45, 334-340.

[22]   Shahzad, S.M., Arif, M.S., Riaz, M., Iqbal, Z. and Ashraf, M. (2013) PGPR with Varied ACC-Deaminase Activity Induced Different Growth and Yield Response in Maize (Zea mays L.) under Fertilized Conditions. European Journal of Soil Biology, 57, 27-34.

[23]   Wong, W.T., Tseng, C.H., Hsu, S.H., Lur, H.S., Mo, C.W., Huang, C.N., Hsu, S.C., Lee, K.T. and Liu, C.T. (2014) Promoting Effects of a Single Rhodopseudomonas palustris Inoculant on Plant Growth by Brassica rapachinensis under Low Fertilizer Input. Microbes and Environments, 29, 303-313.

[24]   Kumar, A., Prakash, A. and Johri, B.N. (2011) Bacillus as PGPR in Crop Ecosystem. In: Maheshwari, D.K., Ed., Bacteria in Agrobiology: Crop Ecosystems, Springer, Heidelberg, Berlin, 37-59.

[25]   Mandic-Mulec, I. and Prosser, J.I. (2011) Diversity of Endospore-Forming Bacteria in Soil: Characterization and Driving Mechanisms. In: Logan, A.N. and Vos, P., Eds., Endospore-Forming Soil Bacteria, Springer, Heidelberg Berlin, 31-59.

[26]   Huang, X., Zhou, D., Guo, J., Manter, D.K., Reardon, K.F. and Vivanco, J.M. (2015) Bacillus spp. from Rainforest Soil Promote Plant Growth under Limited Nitrogen Conditions. Journal of Applied Microbiology, 118, 672-684.

[27]   Wani, P.A. and Khan, M.S. (2010) Bacillus Species Enhance Growth Parameters of Chickpea (Cicerarietinum L.) in Chromium Stressed Soils. Food and Chemical Toxicology, 48, 3262-3267.

[28]   Meng, Q., Jiang, H. and Hao, J. (2016) Effects of Bacillus velezensis Strain BAC03 in Promoting Plant Growth. Biological Control, 98, 18-26.

[29]   de Freitas, J.R., Banerjee, M.R. and Germida, J.J. (1997) Phosphate-Solubilizing Rhizobacteria Enhance the Growth and Yield But Not Phosphorus Uptake of Canola (Brassica napus L.). Biology and Fertility of Soils, 24, 358-364.

[30]   Kuan, K.B., Othman, R., Rahim, K.A. and Shamsuddin, Z.H. (2016) Plant Growth-Promoting Rhizobacteria Inoculation to Enhance Vegetative Growth, Nitrogen Fixation and Nitrogen Remobilization of Maize under Greenhouse Conditions. PLoS ONE, 11, e0152478.

[31]   Bullied, W.J., Buss, T.J. and Vessey, J.K. (2002) Bacillus cereus UW85 Inoculation Effects on Growth, Nodulation, and N Accumulation in Grain Legumes: Field Studies. Canadian Journal of Plant Science, 82, 291-298.

[32]   Çakmakçi, R., Donmez, F., Aydin, A. and Sahin, F. (2006) Growth Promotion of Plants by Plant Growth-Promoting Rhizobacteria under Greenhouse and Two Different Field Soil Conditions. Soil Biology and Biochemistry, 38, 1482-1487.

[33]   de Freitas, J.R. (2000) Yield and N Assimilation of Winter Wheat (Triticum aestivum L., var. Norstar) Inoculated with Rhizobacteria. Pedobiologia, 44, 97-104.

[34]   Lucy, M., Reed, E. and Click, B.R. (2004) Application of Free Living Plant Growth-Promoting Rhizobacteria. Antonic Van Leewenhoek, 86, 1-25.

[35]   Belimov, A.A., Kojemiakov, A.P. and Chuvarliyeva, C.V. (1995) Interaction between Barley and Mixed Cultures of Nitrogen Fixing and Phosphate-Solubilizing Bacteria. Plant and Soil, 173, 29-37.

[36]   Ryu, C.M., Murphy, J.F., Reddy, M.S. and Kloepper, J.W. (2007) A Two-Strain Mixture of Rhizobacteria Elicits Induction of Systemic Resistance against Pseudomonas syringae and Cucumber mosaic virus Coupled to Promotion of Plant Growth on Arabidopsis thaliana. Journal of Microbiology and Biotechnology, 17, 280-286.

[37]   Jarak, M., Mrkovački, N., Bjelić, D., Jošić, D., Hajnal-Jafari, T. and Stamenov, D. (2012) Effects of Plant Growth Promoting Rhizobacteria on Maize in Greenhouse and Field Trial. African Journal of Microbiology Research, 6, 5683-5690.

[38]   Egamberdiyeva, D. (2007) The Effect of Plant Growth Promoting Bacteria on Growth and Nutrient Uptake of Maize in Two Different Soils. Applied Soil Ecology, 36, 184-189.

[39]   Shaharoona, B., Naveed, M., Arshad, M. and Zahir, Z.A. (2008) Fertilizer-Dependent Efficiency of Pseudomonads for Improving Growth, Yield, and Nutrient Use Efficiency of Wheat (Triticum aestivumL.). Journal of Microbiology and Biotechnology, 79, 147-155.

[40]   Hue, N.V. and Evans, C.E. (1986) Procedures Used for Soil and Plant Analysis by the Auburn University Soil Testing Laboratory. Auburn University, Auburn.

[41]   Mitchell, C.C. and Huluka, G. (2012) Nutrient Recommendation Tables for Alabama Crops. Agronomy and Soils Departmental Series No. 324B. Alabama Agricultural Experiment Station, Auburn, AL.

[42]   Bauhus, J. and Messier, C. (1999) Evaluation of Fine Root Length and Diameter Measurements Obtained Using RHIZO Image Analysis. Agronomy Journal, 91, 142-147.

[43]   Costa, C., Dwyer, L.M., Hamilton, R.I., Hamel, C., Nantais, L. and Smith, D.L. (2000) A sampling Method for Measurement of Large Root Systems with Scanner-Based Image Analysis. Agronomy Journal, 92, 621-627.

[44]   SAS Institute (2013) Version 9.4. SAS Institute, Cary, NC.

[45]   Akintoye, H.A. (1996) Thesis Abstract. The International Institute of Tropical Agriculture Research, 25-27.

[46]   LustosaFilho, J.F., Nőbrega, CA, Nőbrega, R.S.A., Andrade, F.R., Pacheco, L.P., Pires, L.C. and de Aquino, J.M. (2014) Effect of Rates and Forms of Nitrogen Splitting on Corn in the Brazilian Cerrado of Piauí State. African Journal Agricultural Research, 9, 2648-2656.

[47]   Marini, D., Guimarães, V.F., Dartora, J., Lana, M.C. and Pinto Jr., A.S. (2015) Growth and Yield of Corn Hybrids in Response to Association with Azospirillum brasilense and Nitrogen Fertilization. Revista Ceres Viçosa, 62, 117-123.

[48]   Arnon, I. (1975) Mineral Nutrition of Maize. International Potash Institute, Bern, 454.

[49]   Fancelli, A.L. and Dourado-Neto, D. (2000) Produção de milho. Agropecuária, Guaíba, 360 p

[50]   Amin, M.E.H. (2011) Effect of Different Nitrogen Sources on Growth, Yield and Quality of Fodder Maize (Zea mays L.). Journal of the Saudi Society of Agricultural Sciences, 10, 17-23.

[51]   Dicko, A.H. and Verma, R.K. (2014) Effect of Growth Promoting Microbes on Initial Growth of Maize. Indian Journal of Tropical Biodiversity, 22, 64-69.

[52]   Calvo, P., Watts, D.B., Kloepper, J.W. and Torbert, H.A. (2017) Effects of Microbial-Based Inoculants on Nutrient Concentrations and Early Root Morphology of Corn (Zea mays). Journal of Plant Nutrition and Soil Science, 180, 56-70.

[53]   Gholami, A., Biyari, A., Gholipoor, M. and Rahmani, H.A. (2012) Growth Promotion of Maize (Zea mays L.) by Plant-Growth-Promoting Rhizobacteria under Field Conditions. Communications in Soil Science and Plant Analysis, 43, 1263-1272.

[54]   Picazevicz, A.A.C., Kusdra, J.F. and Moreno, A.D. (2017) Maize Growth in Response to Azospirillum brasilense, Rhizobium tropici, Molybdemum and Nitrogen. RevistaBrasileira de EngenhariaAgrícola e Ambiental, 21, 623-627.

[55]   Nezarat, S. and Gholami, A. (2009) Screening Plant Growth Promoting Rhizobacteria for Improving Seed Germination, Seedling Growth and Yield of Maize. Pakistan Journal of Biological Sciences, 12, 26-32.

[56]   Sengupta, C., Bhosale, A. and Malusare, S. (2015) Effect of Plant Growth Promoting Rhizobacteria on Seed Germination and Seedling Development of Zea mays. IJRAT. Special Issue National Conference “AGGT 2015”, 32-40.

[57]   Carlier, E., Rovera, M., Rossi, J. and Rosas, S.B. (2008) Improvement of Growth, under Field Conditions, of Wheat Inoculated with Pseudomonas chlororaphis subsp. aurantiaca SR1. World Journal of Microbiology & Biotechnology, 24, 2653-2658.

[58]   Zabihi, H.R., Savaghebi, G.R., Khavazi, K., Ganjali, A. and Miransari, M. (2010) Pseudomonas Bacteria and Phosphorous Fertilization, Affecting Wheat (Triticum aestivum L.) Yield and P Uptake under Greenhouse and Field Conditions. Acta Physiologiae Plantarum, 33, 145-152.

[59]   Miransari, M. (2011) Soil Microbes and Plant Fertilization. Applied Microbiology and Biotechnology, 92, 875-885.

[60]   Bashan, Y., Holguin, G. and de-Bashan, L.E. (2004) Azospirillum-Plant Relationships: Physiological, Molecular, Agricultural, and Environmental Advances. Canadian Journal of Microbiology, 50, 521-577.

[61]   Vacheron, J., Desbrosses, G., Bouffaud, M.L., Touraine, B., Moënne-Loccoz, Y., Muller, D., Legendre, L., Wisniewski-Dye, F. and Prigent-Combaret, C. (2013) Plant Growth-Promoting Rhizobacteria and Root System Functioning. Frontiers in Plant Science, 4, 356.

[62]   Sattelmacher, B., Klotz, F. and Marschner, H. (1990) Influence of the Nitrogen Level on Root Growth and Morphology of Two Potato Varieties Differing in Nitrogen Acquisition. Plant and Soil, 123, 131-137.

[63]   Kramer, P. and Boyer, J. (1995) Water Relations of Plants and Soils. Academic Press, London, UK.

[64]   El Zemrany, H., Czarnes, S., Hallett, P.D., Alamercery, S., Bally, R. and Jocteur Monrozier, L.J. (2007) Early Changes in Root Characteristics of Maize (Zea mays L.) Following Seed Inoculation with the PGPR Azospirillum lipoferum CRT1. Plant and Soil, 291, 109-118.

[65]   Gamalero, E., Trotta, A., Massa, N., Copetta, A., Martinotti, M.G. and Berta, G. (2004) Impact of Two Fluorescent Pseudomonads and an Arbuscular Mycorrhizal Fungus on Tomato Plant Growth, Root Architecture and P Acquisition. Mycorrhiza, 14, 185-192.

[66]   Lemanceau, P., Offre, P., Mougel, C., Gamalero, E., Dessaux, Y., Moёnne-Loccoz, Y. and Berta, G. (2005) Microbial Ecology of the Rhizosphere. In: Bloem, J., Hopkins, D.W. and Benedetti, A., Eds., Microbiological Methods for Assessing Soil Quality, JCABI Publishing, Wallingford, UK, 228-230.

[67]   Lin, Y., Watts, D.B., Kloepper, J.W. and Torbert, H.A. (2017) Influence of Plant Growth-Promoting Rhizobacteria on Corn Growth under Different Fertility Sources. Communication in Soil Science and Plant Analysis, 49, 1239-1255.

[68]   Subedi, K.D. and Ma, B.L. (2009) Corn Crop Production: Growth, Fertilization and Yield. In: Danforth, A.T., Ed, Corn Crop Production: Growth, Fertilization and Yield, Nova Science Publishers, Hauppauge, NY, 1-84.

[69]   Zhu, J., Liang, Y. and Tremblay, N. (2011) Responses of Nitrogenvstatus Indicators to Nitrogen Rates and Soil Moisture in Corn (Zea mays L.). Acta Agronomica Sinica, 37, 1259-1265.

[70]   Mantelin, S. and Touraine, B. (2004) Plant Growth-Promoting Bacteria and Nitrate Availability: Impacts on Root Development and Nitrate Uptake. Journal of Experimental Botany, 55, 27-34.

[71]   Idris, E.E.S., Iglesias, D.J., Talon, M. and Borriss, R. (2007) Tryptophan-Dependent Production of Indole-3-Acetic Acid (IAA) Affects Level of Plant Growth Promotion by Bacillus amyloliquefaciens FZB42. Molecular Plant-Microbe Interactions, 20, 619-626.

[72]   Calvo, P. (2013) Effect of Microbial Inoculation on Nitrogen Plant Uptake and Nitrogen Losses from Soil and Plant-Soil Systems. Doctoral Dissertation, Auburn University, Auburn, AL.

[73]   Biari, A., Gholami, A. and Rahmani, R.A. (2008) Growth Promotion and Enhanced Nutrient Uptake of Maize (Zea mays L.) by Application of Plant Growth Promoting Rhizobacteria in Arid Region of Iran. Journal of Biological Sciences, 8, 1015-1020.