Abstract
The rising demand for agricultural commodities in developing countries has put increasing pressure on land resources for higher yields, with associated growth in the demand for phosphate fertilizers. However, there are a number of adverse environmental impacts associated with the use of inorganic P fertilizers that is pushing global fertilizer prices up. In this context, phosphate solubilizing microorganisms, such as Bacillus, are the most eco-friendly and inexpensive option for enhancing P availability for plants, once they are capable of transforming insoluble P into soluble (plant accessible) forms and are regarded as plant growth-promoting microorganisms. This work aimed to understand the effect of tropical Bacillus strains on maize root morphology and growth using a hydroponic system and to evaluate their performance under two phosphorus fertilization conditions in the field. Maize root was inoculated separately with six Bacillus strains and grown in nutrient solution. Several root traits, dry weight and nutrient content were measured in maize seedlings. Moreover, we measured bacterial IAA-like molecules in vitro production and evaluated inoculated maize performance under field conditions with no P added (P0) and triple superphosphate (TSP) soil fertilization. All the Bacillus strains increased shoot and total dry weight and strains B2084, B119 and B32 had the greatest performance, producing the highest biomass, shoot nutrient content and root surface area compared to other strains in hydroponics. All strains that produced IAA-like molecules demonstrated a positive effect on plant growth by stimulating root elongation. In the field experiments, strain B116 inoculation increased maize yield and P grain accumulation by around 36% and 58%, respectively, and B119 increased P grain in 21% in soils with no P added. Even in soils fertilized with TSP, maize yield increase and P grain accumulation was around 20% after inoculation with these two strains comparing to non-inoculated control. Our results indicated that maize plants inoculated with Bacillus strains capable of producing IAA-like molecules and solubilizing phosphate, presented enhanced root system, dry matter and nutrient accumulation in hydroponics and higher yield and grain P content with and without addition of phosphate fertilizer under field conditions.
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References
Abreu CS, Figueiredo JE, Oliveira CA, Dos Santos VL, Gomes EA, Ribeiro VP, Barros BA, Lana UGP, Marriel IE (2017) Maize endophytic bacteria as mineral phosphate solubilizers. Genet Mol Res 16:16. https://doi.org/10.4238/gmr16019294
Altschul SF, Madden TL, Schäffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25:3389–3402
Anzuay MS, Ciancio MGR, Ludueña LM, Angelini JG, Barros G, Pastor N, Taurian T (2017) Growth promotion of peanut (Arachis hypogaea L.) and maize (Zea mays L.) plants by single and mixed cultures of efficient phosphate solubilizing bacteria that are tolerant to abiotic stress and pesticides. Microbiol Res 199:98–109
Binenbaum J, Weinstain R, Shani E (2018) Gibberellin localization and transport in plants. Trends Plant Sci 23:410–421
Cássan F, Diaz-Zorita M (2016) Azospirillum sp. in current agriculture: from the laboratory to the field. Soil Biol Biochem 103:117–130
Chaman A, Sanguin H, Bellvert F, Meiffren G, Comte G, Wisniewski-Dyé F, Bertrand C, Prigent-Combaret C (2013) Plant secondary metabolite profiling evidences strain-dependent effect in the Azospirillum-Oryza sativa association. Phytochemisty 87:65–77
Chen YH, Chao YY, Hsu YY, Hong CY, Kao CH (2012) Heme oxygenase is involved in nitric oxide and auxin-induced lateral root formation in rice. Plant Cell Rep 31:1085–1091
Combes-Meynet E, Pothier JF, Moenne-Loccoz Y, Prigent-Combaret C (2011) The Pseudomonas secondary metabolite 2,4-diacetylphloroglucinol is a signal inducing rhizoplane expression of Azospirillum genes involved in plant-growth promotion. Mol Plant Microbe Interact 24:271–284
Depuydt S, Hardtke CS (2011) Hormone signaling crosstalk in plant growth regulation. Curr Biol 21:365–373
De Sousa SM, Clark RT, Mendes FF, Oliveira AC, Vasconcelos MJV, Parentoni SN, Kochian LV, Guimaraes CT, Magalhaes JV (2012) A role for root morphology and related candidate genes in P acquisition efficiency in maize. Funct Plant Biol 39(11):925–935
Dumas JBA (1831) Procédés de l’analyse organique. Ann Chem Phys 47(2):198–213
Ehteshami SM, Khavazi K, Asgharzadeh A (2018) Forage sorghum quantity and quality as affected by biological phosphorous fertilization. Grass Forage Sci 73:926–937. https://doi.org/10.1111/gfs.12388
Etesami H, Maheshwari DK (2018) Use of plant growth promoting rhizobacteria (PGPRs) with multiple plant growth promoting traits in stress agriculture: action mechanisms and future prospects. Ecotoxicol Environ Saf 156:225–246
Ferreira DF (2011) Sisvar: a computer statistical analysis system. Ciênc Agrotec 35:1039–1042
Ferreira MH, Sorares HMVM, Soares EF (2019) Promising bacterial genera for agricultural practices: an insight on plant growth-promoting properties and microbial safety aspects. Sci Total Environ 682:779–799
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 7:153–163
Garay-Arroyo A, de La Paz SM, Gracía-Ponce B, Azpeitia E, Alvarez-Buylla ER (2012) Hormone symphony during root growth and development. Dev Dyn 241:1867–1885
Geldner N, Anders N, Wolters H, Keicher J, Kornberger W, Muller P, Delbarre A, Ueda T, Nakano A, Jürgens G (2003) The Arabidopsis GNOM ARF-endosomal recycling, auxin transport and auxin dependent plant growth. Cell 112(2):219–230
Gomes EA, Silva UC, Marriel IE, Oliveira CA, Lana UGP (2014) Rock phosphate solubilizing microorganisms isolated from maize rhizosphere soil. Rev Bras Milho Sorgo 13:69–81
Hodkinson BP, Lutzoni F (2009) A microbiotic survey of lichen-associated bacteria reveals a new lineage from the Rhizobiales. Symbiosis 49:163–180. https://doi.org/10.1007/s13199-009-0049-3
Hossain MT, Khan A, Harun-Or-Rashid M, Chung YR (2019) A volatile producing endophytic Bacillus siamensis YC7012 promotes root development independent on auxin or ethylene/jasmonic acid pathway. Plant Soil. https://doi.org/10.1007/s11104-019-04015-y
Irizarry I, White JF (2017) Application of bacteria from non-cultivated plants to promote growth, alter root architecture and alleviate salt stress of cotton. J Appl Microbiol 122:1110–1120
Ikeda AC, Bassani LL, Adamoski D, Stringari D, Kava-Cordeiro V, Glienke C, Steffens MBR, Hungria M, Galli-Terasawa LV (2013) Morphological and genetic characterization of endophytic bacteria isolated from roots of different maize genotypes. Microb Ecol 4:154–160
Jacoby R, Peukert M, Succurro A, Koprivova A, Kopriva S (2017) The role of soil microorganisms in plant mineral nutrition—current knowledge and future directions. Front Plant Sci 8:1617. https://doi.org/10.3389/fpls.2017.01617
Kahiluoto H, Ketoja E, Vestberg M, Saarela I (2001) Promotion of AM utilization through reduced P fertilization. 2 Field studies. Plant Soil 231:65–79
Le S, Josse J, Husson F (2008) FactoMineR: an R package for multivariate analysis. J Stat Softw 25:1–18
Leggett M, Newlands NK, Greenshields D, West L, Inman S, Koivunen ME (2015) Maize yield response to a phosphorus-solubilizing microbial inoculant in field trials. J Agric Sci 153:1464–1478
Lenth RV (2019) emmeans: estimated marginal means, aka least-squares means. R package version 1.3.2. https://CRAN.R-project.org/package=emmeans
López-Bucio J, Campos-Cuevas JC, Hernández-Calderón E, Velásquez-Becerra C, Farías-Rodríguez R, Macías-Rodríguez LI, Valencia-Cantero E (2007) Bacillus megaterium rhizobacteria promote growth and alter root-system architecture through an auxin- and ethylene-independent signaling mechanism in Arabidopsis thaliana. Mol Plant Microbe Interact 20:207–217
Liu C, Muchhal US, Uthappa M, Kononowicz AK, Raghothama KG (1998) Tomato phosphate transporter genes are differentially regulated in plant tissue by phosphorus. Plant Physiol 116:91–99
Loper JE, Schroth MN (1986) Influence of bacterial source of indole-3-acetic acid for root elongation of sugar beet. Phytopathology 76:386–389
Lynch JP, Brown KM (2012) New roots for agriculture: exploiting the root phenome. Philos Trans R Soc Lond B 367(1595):1598–1604
Marschner H (2012) Mineral nutrition of higher plants, 3rd edn. Academic Press, Cambridge
Mehnaz S, Lazarovits G (2006) Inoculation effects of Pseudomonas putida, Gluconacetobacter azotocaptans and Azospirillum lipoferum on corn plant growth under greenhouse conditions. Microb Ecol 51:326–335
McCormack ML, Dickie IA, Eissenstat DM, Fahey T, Fernandez CW, Guo D, Helmisaari HS, Hobbie EA, Iversen CM, Jackson RB, Leppälammi-Kujansuu J, Norby RJ, Phillips RP, Pregitzer KS, Pritchard SG, Rewald B, Zadworny M (2015) Redefining fine roots improves understanding of below-ground contributions to terrestrial biosphere processes. New Phytol 207:505–518
Montañez A, Blanco AR, Barlocco C, Beracochea M, Sicardi M (2012) Characterization of cultivable putative endophytic plant growth promoting bacteria associated with maize cultivars (Zea mays L.) and their inoculation effects in vitro. Appl Soil Ecol 58:21–28
Nogueira ARA, Souza GB (2005) Manual de laboratórios: solo, água, nutrição vegetal, nutrição animal e alimentos. Embrapa Pecuária Sudeste, São Carlos, p 313
Oliveira CA, Alves VMC, Marriel IE, Gomes EA, Scotti MR, Carneiro NP, Guimarães CT, Schaffert RE, Sá NMH (2009) Phosphate solubilizing microorganisms isolated from rhizosphere of maize cultivated in an oxisol of the Brazilian Cerrado Biome. Soil Biol Biochem 41:1782–1787
Oliveira CA, Marriel IE, Gomes EA, Mattos BB, dos Santos FC, de Oliveira MC, Alves VMC (2013) Metodologia de aplicação de microrganismos solubilizadores de fósforo em sementes visando melhor aproveitamento deste nutriente pelas plantas. Boletim de Pesquisa e Desenvolvimento, Embrapa Milho e Sorgo, Sete Lagoas, 2p. ISSN 1679-0154; 88.
Patten C, Glick BR (1996) Bacterial biosynthesis of indole-3-acetic acid. Can J Microbiol 42:207–220
Penn CJ, Camberato J (2019) A critical review on soil chemical processes that control how soil pH affects phosphorus availability to plants. Agriculture 9:1–18
Pereira SIA, Castro PML (2014) Phosphate-solubilizing rhizobacteria enhance Zea mays growth in agricultural P-deficient soils. Ecol Eng 73:526–535
Pereira NCM, Galindo FS, Gazola RPD, Dupas E, Rosa PAL, Mortinho ES, Teixeira Filho MCM (2020) Corn yield and phosphorus use efficiency response to phosphorus rates associated with plant growth promoting bacteria. Front Environ Sci. https://doi.org/10.3389/fenvs.2020.00040
Perrot-Rechenmann C (2010) Cellular responses to auxin: division versus expansion. Cold Spring Harb Perspect Biol 2(5):a001446
Price AL, Patterson NJ, Plenge RM, Weinblatt ME, Shadick NA, Reich D (2006) Principal components analysis corrects for stratification in genome-wide association studies. Nat Genet 38:904–909
R Core Team (2018) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.R-project.org/
Ribeiro VP, de Marriel IE, Sousa SM, Lana UGP, Mattos BB, Oliveira CA, Gomes EA (2018) Endophytic Bacillus strains enhance pearl millet growth and nutrient uptake under low-P. Braz J Microbiol 49S:40–46
Revelle W (2018) psych: procedures for personality and psychological research, Northwestern University, Evanston, Illinois, USA. https://CRAN.R-project.org/package=psych Version = 1.8.4
Rocha I, Ma Y, Souza-Alonso P, Vosátka M, Freitas H, Oliveira RS (2019) Seed coating: a tool for delivering beneficial microbes to agricultural crops. Front Plant Sci 10:1357. https://doi.org/10.3389/fpls.2019.01357
Ruzicka K, Ljung K, Vanneste S, Podhorská R, Beeckman T, Friml J, Benková E (2007) Ethylene regulates root growth through effects on auxin biosynthesis and transport-dependent auxin distribution. Plant Cell 19:2197–2212
Saeid A, Prochownik E, Dobrowolska-Iwanek J (2018) Phosphorus solubilization by Bacillus species. Molecules (Basel, Switzerland) 23:2897. https://doi.org/10.3390/molecules23112897
Santos MS, Nogueira MA, Hungria M (2019) Microbial inoculants: reviewing the past, discussing the present and previewing an outstanding future for the use of beneficial bacteria in agriculture. AMB Express 9:1–22
Schwartz AR, Ortiz I, Maymon M, Herbold CW, Fujishige NA, Vijanderan JA, Villella W, Hanamoto K, Diener A, Sanders ER, DeMason DA, Hirsch AM (2013) Bacillus simplex—a little known PGPB with anti-fungal activity—alters pea legume root architecture and nodule morphology when coinoculated with Rhizobium leguminosarum bv. Viciae. Agronomy 3:595–620
Shimomura S (2006) Identification of a glycosylphosphatidylinositol-anchored plasma membrane protein interacting with the C-terminus of auxin-binding protein 1: a photoaffinity crosslinking study. Plant Mol Biol 60:663–677
Spaepen S, Vanderleyden J (2011) Auxin and plant-microbe interactions. Cold Spring Harbor Perspect Biol 3(4):a001438. https://doi.org/10.1101/cshperspect.a001438
Turner S, Pryer KM, Miao VPW, Palmer JD (1999) Investigating deep phylogenetic relationships among cyanobacteria and plastids by small subunit rRNA sequence analysis. J Eukaryot Microbiol 46:327–338
Vanstraelen M, Benková E (2012) Hormonal interactions in the regulation of plant development. Annu Rev Cell Dev Biol 28:463–487
Vacheron J, Desbrosses G, Bouffaud ML, Touraine B, Moënne-Loccoz Y, Muller D, Legendre L, Wisniewski-Dyé F, Prigent-Combaret C (2013) Plant growth-promoting rhizobacteria and root system functioning. Front Plant Sci 4:1–19
Wagi S, Ahmed A (2019) Bacillus spp.: potent microfactories of bacterial IAA. PeerJ 7:e7258. https://doi.org/10.7717/peerj.7258
Waidmann S, Rosquete MR, Schöller M, Sarkel E, Lindner H, LaRue T, Petřík I, Dünser K, Martopawiro S, Sasidharan R, Novak O, Wabnik K, Dinneny JR, Kleine-Vehn J (2019) Cytokinin functions as an asymmetric and anti-gravitropic signal in lateral roots. Nat Commun 10:1–14
Wen Z, Li H, Shen J, Rengel Z (2017) Maize responds to low shoot P concentration by altering root morphology rather than increasing root exudation. Plant Soil 416:377–389
Wu L, Wu H-J, Qiao J, Gao X, Borriss R (2015) Novel routes for improving biocontrol activity of Bacillus based bioinoculants. Front Microbiol 6:1395
Acknowledgments
This work was supported by Fundação de Amparo à Pesquisa do Estado de Minas Gerais—Fapemig (Grant No MPR-00172-16), Empresa Brasileira de Pesquisa Agropecuária—Embrapa (Grant No 01.13.05.001.02-0, Simbiose) and Conselho Nacional de Desenvolvimento Científico e Tecnológico-CNPq/INCT-Plant-Growth Promoting Microorganisms for Agricultural Sustainability and Environmental Responsibility (Grant No 465133/2014-2, Fundação Araucária-STI, Capes).
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de Sousa, S.M., de Oliveira, C.A., Andrade, D.L. et al. Tropical Bacillus Strains Inoculation Enhances Maize Root Surface Area, Dry Weight, Nutrient Uptake and Grain Yield. J Plant Growth Regul 40, 867–877 (2021). https://doi.org/10.1007/s00344-020-10146-9
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DOI: https://doi.org/10.1007/s00344-020-10146-9