Yield, yield components and nutrients uptake in Zuri Guinea grass inoculated with plant growth-promoting bacteria

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Gilmar Cotrin de Lima
Mariangela Hungria
Marco Antonio Nogueira
Marcelo Carvalho Minhoto Teixeira Filho
Adônis Moreira
Reges Heinrichs
Cecilio Viega Soares Filho


The objective of this study was to evaluate the effects of strains of Azospirillum brasilense, Pseudomonas fluorescens and Rhizobium tropici on biomass yield and nutrients uptake of shoots and roots of Megathyrsus (syn. Panicum) maximus cultivar BRS Zuri (Zuri Guinea grass) inoculated with plant growth-promoting bacteria (PGPB). Treatments consisted of inoculation and re-inoculation with A. brasilense strains Ab-V5 and Ab-V6, P. fluorescens strain CCTB 03 and of co-inoculation with R. tropici strain CIAT 899 + A. brasilense Ab-V6, with or without N-fertilizer (100 mg dm-3). Evaluations were performed on three cuts for the determination of root and shoot dry weight yield, morphological compositions, tiller mass, number of tillers, and nutrient uptake. Inoculation with bacteria in association with N-fertilizer increased N, NH4+, Ca, Fe, Mn and Zn accumulation in shoots and P and K uptake in roots. P. fluorescens and co-inoculation with R. tropici CIAT 899 + A. brasilense Ab-V6 increased the relative chlorophyll index in relation to the non-inoculated control. As expected, PGPB were not able to fully replace N-fertilization. However, when combined with N-fertilizer, the PGPB increased yield, the relative chlorophyll index, and the uptake of N, NH4+, Ca, Zn, Mn and Fe of Zuri Guinea grass. The results indicate that PGPB can represent a sustainable alternative for reducing the use of N-fertilizers. There were no effects of re-inoculation with PGPB on the nutrition or yield of Zuri Guinea grass, demonstrating that the determination of the method of application and periodicity of inoculation still require investigation.


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Lima, G. C. de, Hungria, M., Nogueira, M. A., Teixeira Filho, M. C. M. ., Moreira, A., Heinrichs, R., & Soares Filho, C. V. (2020). Yield, yield components and nutrients uptake in Zuri Guinea grass inoculated with plant growth-promoting bacteria. International Journal for Innovation Education and Research, 8(4), 103-124. https://doi.org/10.31686/ijier.vol8.iss4.2268


[1] Gilabel, A.P., Nogueirol, R.C., Garbo, A.I. & Monteiro, F.A. The role of sulfur in increasing guinea grass tolerance of copper phytoxicity. Water Air soil Pollut. 225, 1806 (2014). https://doi.org/10.1007/s11270-013-1806-8

[2 ] Cook, R. Beef2 Live. In:http://beef2live.com/story-world-beef-productionranking-countries-0-106885. (2017). Acess 05.03.2019.

[3] Silva, E.B. et al. Availability and toxicity of cádmium to forage grasses grown in contaminated soil. Int. J. Phytoremediat. 18, 847-852 (2016). https://doi.org/10.1080/15226514.2016.1146225

[4] Santos, J.H.S., De Bona, F.D. & Monteiro, F.A. Growth and productive responses of tropical grass Panicum maximum to nitrate and ammonium supply. Rev. Bras. Zootecn. 42, 622-628 (2013). http://dx.doi.org/10.1590/S1516-35982013000900003

[5] Soares Filho, C.V. et al. The impact of organic biofertilizer application in dairy cattle manure on the chemical properties of the soil and the growth and nutritional status of Urocholoa grass. Communications in soil science and plant analysis. 49, 358-370 (2018). https://doi.org/10.1080/00103624.2018.1427261

[6] Costa, R.R. et al. Efficiency of inoculant with Azospirillum brasilense on the growth and yield of second-harvest maize. Pesqu. Agropecu. Trop. 45, (3): 304-311 (2015). https://dx.doi.org/10.1590/1983-40632015v4534593

[7] Lal, R. Soil carbon sequestration for sustaining agricultural production and improving the environment with particular reference to Brazil. Journal Sustainable Agric. 26, 23-42 (2005). https://dx.doi.org/10.1300/J064v26n04_04

[8] Sá, J.C. et al. Carbon depletion by plowing and its restoration by no-till cropping systems in oxisols of sub-tropical and tropical agro-ecoregions in Brazil. Land Degrad. Dev. 26, 531-543 (2015). https://doi.org/10.1002/ldr.2218

[9] Carvalahais, L.C. et al. Linking plant nutritional status to plant-microbe interactions. PLoS One. 8, (7): e68555 (2013). https://doi.org/10.1371/journal.pone.0068555

[10] Hungria, M., Campo, R.J., Souza, E.M. & Pedrosa, F.O. Inoculation with selected strains of Azospirillum brasilense and A. lipoferum improves yields of maize and wheat in Brazil. Plant and Soil. 331, (1/2): 413-425(2010). https://doi.org/10.1007/s11104-009-0262-0

[11] Hungria, M., Mendes, I.C. & Mercante, F.M. A fixação biológica do nitrogênio como tecnologia de baixa emissão de carbono para as culturas do feijoeiro e da soja. Embrapa Soja, Londrina (2013).

[12] Hungria, M., Nogueira, M.A. & Araujo, R.S. Co-inoculation of soybeans and common beans with rhizobia and azospirilla: strategies to improve sustainability. Biol. Fertil. Soils. 49, 791–801 (2013) https://doi.org/10.1007/s00374-012-0771-5

[13] Bashan, Y. & De-Bashan, L.E. How the plant growth-promoting bacterium Azospirillum promotes plant growth-a critical assessment. Adv Agronomy. 108, 77–136 (2010). https://doi.org/10.1016/S0065-2113(10)08002-8

[14] Marques, A.C. et al. Biological nitrogen fixation in C4 grasses of different growth strategies of South America natural grasslands. Appl Soil Ecology. 113, 54-56 (2017). https://doi.org/10.1016/j.apsoil.2017.01.011

[15] Ardakani, M.R., Mazaheri, D., Mafakheri, S. & Moghaddam, A. Absorption efficiency of N, P, K through triple inoculation of wheat (Triticum aestivum L.) by Azospirillum brasilense, Streptomyces sp., Glomus intraradices and manure application. Physiol Mol Biol Plants. 17,(2): 181–192 (2011). https://doi.org/10.1007/s12298-011-0065-7

[16] Spaepen, S. & Vanderleyden, J. Auxin signaling in Azospirillum brasilense: a proteome analysis. Wiley, Hoboken. (2015). https://doi.org/10.1002/9781119053095.ch91

[17] Tien, T.M., Gaskins, M.H. & Hubbell, D.H. Plant growth substances produced by Azospirillum brasilense and their effect on the growth of Pearl Millet (Pennisetum americanum L.). Appl Environ Microbiol. 37, (5): 1016–1024 (1979).

[18] Bottini, R., Fulchieri, M., Pearce, D. & Pharis, R.P. Identification of gibberellins A1, A3, and iso-A3 in cultures of Azospirillum lipoferum. Plant Physiology. 90, 45–47 (1989). https://doi.org/10.1104/pp.90.1.45

[19] Sahoo, R.K. et al. Phenotypic and molecular characterization of native Azospirillum strains from rice fields to improve crop productivity. Protoplasma. 251, (4):943–953 (2014). https://doi.org/10.1007/s00709-013-0607-7

[20] Fukami et al. Revealing different strategies of quorum sensing in Azospirillum brasilense strains Ab-V5 and Ab-V6. Archives of Microbiology, 200, (1), 47-56, (2018). https://doi.org/ 10.1007/s00203-017-1422-x).

[21]Rodriguez, H., Gonzalez, T., Goire, I. & Bashan, Y. Gluconic acid production and phosphate solubilization by the plant growth-promoting bacterium Azospirillum spp. Naturwissenschaften. 91, 552–555 (2004). https://doi.org/10.1007/s00114-004-0566-0

[22] Fukami J, Ollero FJ, 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 7:153-166 https://dx.doi.org/10.1186%2Fs13568-017-0453-7

[23] Fukami, J. et al. Co-inoculation of maize with Azospirillum brasilense and Rhizobium tropici as a strategy to mitigate salinity stress. Functional Plant Biology. 45, 328-339 (2017) https://doi.org/10.1071/FP17167

[24] Hungria, M., Nogueira, M.A. & Araújo, R.S. Inoculation of Brachiaria spp. with the plant growth-promoting bacterium Azospirillum brasilense: An environment-friendly component in the reclamation of degraded pastures in the tropics. Agriculture, Ecosystems and Environment. 221, 125–131 (2016). https://doi.org/10.1016/j.agee.2016.01.024

[25] Sandini, I.E, Pacentchuk. F., Hungria, M., Nogueira, M.A., Cruz, S.P., Nakatani, A.S., Araujo, R.S. (2019) Seed inoculation with Pseudomonas fluorescens promotes growth, yield and reduces nitrogen application in maize. Int J Agric Biol https://doi:10.17957/IJAB/15.1210

[26] Santos, H.G. et al. Brazilian system of soil classification (5th ed.). Brasilia, DF. Embrapa. (2018).

[27] Van Raij. et al. Chemical analysis for fertility evaluation of tropical soils. P.284. Campinas: Instituto Agronômico. (2001).

[28] Döbereiner, J., Marriel, I. & Nery, M. Ecological distribution of Spirillum lipoferum. Can. J. Microbiol. 22, 1464–1473 (1976) https://doi.org/10.1139/m76-217

[29] Hungria, M. & Araujo, R.S. Manual de métodos empregados em estudos de microbiologia agrícola. EMBRAPA, Brasília (1994). Available at: https://www.embrapa.br/busca-de-publicacoes/-/publicacao/199952/manual-de-metodos-empregados-em-estudos-de-microbiologia-agricola>

[30] Fukami, J.; Cerezin, P.; Hungria, M. Azospirillum: benefits that go far beyond biological nitrogen fixation. AMB Express, 8, (1), 73, (2018). https://doi.org/10.1186/s13568-018-0608-1

[31] Malavolta, E., Vitti, G.C. & Oliveira, S.A. Avaliação do estado nutricional das plantas: princípios e aplicações. In: Potafós. Princípios e aplicações. 2ed. Piracicaba, São Paulo (1997).

[32] Ronnegard, L., Shen, X., Alam, M. hglm: A Package for Fitting Hierarchical Generalized Linear Models. The R Journal. 2, 20-28 (2010).

[33] R Core Team. R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria https://www.r-project.org (2017).

[34] Roesch, L.F., Camargo, F.O., Selbach, P.A., Sá, E.S. Reinoculação de bactérias diazotróficas aumentando o crescimento de plantas de trigo. Ciência Rural. 35, 1201 1204 (2005). http://dx.doi.org/10.1590/S0103-84782005000500035

[35] Lana, M.C., Dartora, J., Marini, D. & Hann, J.E. Inoculation with Azospirillum, associated with nitrogen fertilization in maize. Revista Ceres. 59, (3):399-405 (2012). http://dx.doi.org/10.1590/S0034-737X2012000300016

[36] Duca, D. et al. Indole-3-acetic acid in Plant-microbe interactions. Antonie van Leeuwenhoek. 106, 85-125 (2014) https://doi.org/10.1007/s10482-013-0095-y

[37] Taiz, L. & Zeiger, E. Fisiologia vegetal. Artemed, Porto Alegre (2013).

[38] Tullio LD et al. Revealing the roles of y4wF and tidC genes in Rhizobium tropici CIAT 899: Biosynthesis of indolic compounds and impact on symbiotic properties. Archives of Microbiology, 201, n.2, 171-183, (2019). https://doi.org/10.1007/s0023-018-1607-y

[39] Cerri, C.C. et al. Greenhouse gas mitigation options in Brazil for land-use change, livestock and 43 agriculture. Sci. Agri. 67, 102–116 (2010). http://dx.doi.org/10.1590/S0103-90162010000100015

[40] Muleta, D., Assefa, F., Börjesson, E. & Granhall, U. Phosphate-solubilising rhizobacteria associated with Coffea arabica L. in natural coffee forests of southwestern Ethiopia. Journal of the Saudi Society of Agricultural Sciences. 12, 73-84(2013). https://doi.org/10.1016/j.jssas.2012.07.002

[41] Criollo, P., Obando, M., Sánchez, L. & Bonilla, R. Efecto de bacterias promotoras del crecimiento vegetal (PGPR) asociadas a Pennisetum clandestinum en el altiplano cundiboyacense‖. Revista Corpoica – Ciencia y Tecnologia Agropecuaria. 13, (2): 189-195 (2012). https://doi.org/10.21930/rcta.vol13_num2_art:254

[42] Bárbaro, I.M. et al. Técnica alternativa: co-inoculação de soja com Azospirillum e Bradyrhizobium visando incremento de produtividade. http://www.infobibos.com/Artigos/2008_4/coinoculacao/index.htm (2008).

[43] Ferlini, H.A. Co-Inoculación en Soja (Glicyne max) con Bradyrhizobium japonicum y Azospirillum brasilense. International Business Comunity Related to Animal Production (2006). http://www.engormix.com/co_inoculacion_soja_glicyne_s_articulos_800_AGR.htm

[44] Ilyas, N. & Bano, A. Azospirillum strains isolated from roots and rhizosphere soil of wheat (Triticum aestivum.) grown under different soil moisture conditions. Biology Fertility Soil. 46, 393-406 (2010). https://doi.org/10.1007/s00374-009-0438-z

[45] García-Fraile, P. et al. Rhizobium promotes non-legumes growth and quality in several production steps: towards a biofertilization of edible raw vegetables healthy for humans. PLoS One. 7, (5): e38122 (2012). https://doi.org/10.1371/journal.pone.0038122

[46] Yanni, Y.G. & Dazzo, F.B. Occurrence and ecophysiology of the natural endophytic Rhizobium–rice association and translational assessment of its biofertilizer performance within the Egypt Nile delta. Biological nitrogen fixation. (Ed. FJ de Bruijn) 747–756 (2015). https://doi.org/10.1002/9781119053095.ch111

[47] Itzigsohn, R. et al. Plant-growth promotion in natural pastures by inoculation with Azospirillum brasilense under suboptimal growth conditions. Arid Soil Research. 13, 151-158 (2000). https://doi.org/10.1080/089030600263076

[48] Malik, K.A. et al. Association of nitrogen-fixing, plant-growth-promoting rhizobacteria (PGPR) with kallar grass and rice. Plant and Soil. 194, 37-44 (1997). https://doi.org/10.1023/A:1004295714181

[49] Aguirre, P.F. et al. Forage yield of Coastcross-1 pastures inoculated with Azospirillum brasilense. Acta Sci., Ani Sci. 40, e36392. (2018). http://dx.doi.org/10.4025/actascianimsci.v40i0.36392

[50] Larcher, W. Ecofisiologia vegetal. Rima, São Carlos. (2000).

[51] Guimarães, S.L. et al. Nutritional characteristics of marandu grass (Brachiaria brizantha cv. marandu) subjected to inoculation with associative diazotrophic bacteria. African Journal of Microbiology Research. 10, (24): 873-882 (2016). https://doi.org/10.5897/AJMR2016.7951

[52] Sá, G.C.R., Carvalho, C.L.M., Moreira, A., Hungria, M., Nogueira, M.A., Heinrichs, R., Soares Filho, C.V. (2019) Biomass yield, nitrogen accumulation and nutritive value of Mavuno grass inoculated with plant growth-promoting bacteria. Communications in Soil Science and Plant Analysis 50(15):1931-1942 https://doi.org/10.1080/00103624.2019.1648498

[53] Boer, C.A. et al. Ciclagem de nutrientes por plantas de cobertura na entressafra em um solo de cerrado. Pesq. agropec. Bras. 42,(9): 1269-1276 (2007). https://dx.doi.org/10.1590/S0100-204X2007000900008

[54] Torres, J.L. et al. Decomposição e liberação de nitrogênio de resíduos culturais de plantas de cobertura em um solo de cerrado. Rev. Brasi. Ciênc. Solo. 29, (4): 609-618. (2005). http://dx.doi.org/10.1590/S0100-06832005000400013

[55] Gupta, K., Dey, A. & Gupta, B. Plant polyamines in abiotic stress responses. Acta Physiol Plant. 35, (7): 2015–2036 (2013). https://doi.org/10.1007/s11738-013-1239-4

[56] Machado, A.T., Sodek, L., Döbereiner, J. & Reis, V.M. Efeito da adubação nitrogenada e da inoculação com bactérias diazotróficas no comportamento bioquímico da cultivar de milho Nitroflint. Pesq. Agropec. Bras. 33, 961-970 (1998).

[57] Unno, H. et al. Atomic Structure of Plant Glutamine Synthetase. The Journal of Biological Chemistry. 281, (39): 29287-29296 (2006). https://doi.org/10.1074/jbc.M601497200

[58] Barker, A.V. & Mills, H.A. Ammonium and nitrate nutrition of horticultural crops. Horticultural Review. 2, 395–423 (1980). https://doi.org/10.1002/9781118060759.ch8

[59] Duijff, B.J., Gianinazzi-Pearson, V. & Lemanceau, P. Involvement of the outer membrane lipo polysaccharides in the endophytic colonization of tomato roots by biocontrol Pseudomonas fluorescens strain WCS417r. New Phytol. 135, 325–334 (1997) https://doi.org/10.1046/j.1469-8137.1997.00646.x

[60] Vyas, P. & Gulati, A. Organic acid production in vitro and plant growth promotion in maize under control environment by phosphate-solubilizing fluorescent Pseudomonas. BMC Microbiology. 9, 174 (2009). https://doi.org/10.1186/1471-2180-9-174.

[61] Gray, E.J. & Smith, D.L. Intracellular and extracellular PGPR: commonalities and distinctions in the plant-bacterium signaling processes. Soil Biology Biochemical. 37, 395-412 (2005). https://doi.org/10.1016/j.soilbio.2004.08.030

[62] Vandendergh, P.A. & Gonzalez, C.F. Methods for protecting the growth of plants employing mutant siderophore producing strains of Pseudomonas putida. United States Patent Number 4, 479-936 (1984).

[63] Dobbelaere, S., Vanderleyden, J. & Okon, Y. Plant growth-promoting effects of diazotrophs in the rhizosphere. Crit. Rev. in Plants Sci. 22, 107-149 (2003). https://doi.org/10.1080/713610853

[64] Crowley, D.E., Reid, C.P. & Szaniszlo, P.J. Utilization of microbial siderophores in iron acquisition by oat. Plant Physiology. 87, 680–685 (1988). https://doi.org/10.1104/pp.87.3.680

[65] Malavolta, E. Manual de nutrição de plantas. Agronômica Ceres, São Paulo (2006).

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